Nakamura and Takai Progress in Earth and Planetary Science 2014, 1:5
http://www.progearthplanetsci.com/content/1/1/5

REVIEW

Open Access

Theoretical constraints of physical and chemical
properties of hydrothermal fluids on variations inchemolithotrophic microbial communities inseafloor hydrothermal systems
Kentaro Nakamura1,2* and Ken Takai1,3

Abstract
In the past few decades, chemosynthetic ecosystems at deep-sea hydrothermal vents have received attention asplausible analogues to the early ecosystems of Earth, as well as to extraterrestrial ecosystems. These ecosystems are
sustained by chemical energy obtained from inorganic redox substances (e.g., H2S, CO2, H2, CH4, and O2) inhydrothermal fluids and ambient seawater. The chemical and isotope compositions of the hydrothermal fluid are, inturn, controlled by subseafloor physical and chemical processes, including fluid–rock interactions, phase separationand partitioning of fluids, and precipitation of minerals. We hypothesized that specific physicochemical principles
describe the linkages among the living ecosystems, hydrothermal fluids, and geological background in deep-sea
hydrothermal systems. We estimated the metabolic energy potentially available for productivity by chemolithotrophic
microorganisms at various hydrothermal vent fields. We used a geochemical model based on hydrothermal fluid
chemistry data compiled from 89 globally distributed hydrothermal vent sites. The model estimates were compared tothe observed variability in extant microbial communities in seafloor hydrothermal environments. Our calculations clearlyshow that representative chemolithotrophic metabolisms (e.g., thiotrophic, hydrogenotrophic, and methanotrophic)
respond differently to geological and geochemical variations in the hydrothermal systems. Nearly all of the deep-sea
hydrothermal systems provide abundant energy for organisms with aerobic thiotrophic metabolisms; observed
variations in the H2S concentrations among the hydrothermal fluids had little effect on the energetics of thiotrophic
metabolism. Thus, these organisms form the base of the chemosynthetic microbial community in global deep-sea
hydrothermal environments. In contrast, variations in H2 concentrations in hydrothermal fluids significantly impact
organisms with aerobic and anaerobic hydrogenotrophic metabolisms. Particularly in H2-rich ultramafic rock-hostedhydrothermal systems, anaerobic and aerobic hydrogenotrophy is more energetically significant than thiotrophy. The
CH4 concentration also has a considerable impact on organisms with aerobic and anaerobic methanotrophic
metabolisms, particularly in sediment-associated hydrothermal systems. Recently clarified patterns and functions ofexisting microbial communities and their metabolisms are generally consistent with the results of our thermodynamic
modeling of the hydrothermal mixing zones. These relationships provide important directions for future research
addressing the origin and early evolution of life on Earth as well as for the search for extraterrestrial life.
Keywords: Deep-sea hydrothermal systems; Chemosynthetic ecosystems; Hydrothermal fluid chemistry; Host rockgeochemistry; Geochemical modeling; Bioavailable energy yield* Correspondence: kentaron@sys.t.u-tokyo.ac.jp
1
Precambrian Ecosystem Laboratory (PEL), Japan Agency for Marine-Earth
Science and Technology (JAMSTEC), 2-15 Natsushima-cho, Yokosuka,
Kanagawa 237-0061, Japan
2
Current address: Department of Systems Innovation, School of Engineering,
The University of Tokyo, 7-3-1 Hongo, Bunkyo-ku, Tokyo 113-8656, Japan
Full list of author information is available at the end of the article© 2014 Nakamura and Takai; licensee Springer. This is an Open Access article distributed under the terms of the Creative
Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, andreproduction in any medium, provided the original work is properly credited.

Nakamura and Takai Progress in Earth and Planetary Science 2014, 1:5
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Review
Introduction

Deep-sea hydrothermal vents host some of the mostdiverse microbial communities on Earth (Takai andNakamura 2011). Since the first discovery of blacksmoker vents inhabited by dense and unique chemosynthetic macrofaunal communities (Spiess et al. 1980),
submarine hydrothermal systems and their associatedbiota have attracted great interest (e.g., Humphris et al.
1995; Van Dover 2000; Wilcock et al. 2004). Unlike most
biological communities, in which photosynthetic organisms are the base of the food web, deep-sea hydrothermalvent ecosystems are dependent on primary production bysymbiotic and free-living chemolithoautotrophic microorganisms that obtain energy from inorganic redox substances (e.g., H2S, CO2, H2, CH4, and O2) in hydrothermal
fluids and ambient seawater (Karl, 1995; Kelley et al.
2002). Because of the unique features of deep-sea hydrothermal vent ecosystems, they are considered plausible analogues to the early ecosystems of Earth and also to
extraterrestrial life on other planets and moons (e.g.,
Jannasch and Mottl 1985; Nealson et al. 2005; Takai et al.
2006a).
To date, more than 300 high-temperature hydrothermal vent systems have been identified at mid-ocean
ridges (MOR), island arcs, and back-arc spreading centers (Hannington et al. 2011). Deep-sea hydrothermal
fluids vary greatly in their chemical compositions due tosubseafloor physical and chemical processes such as
fluid-rock interactions, magmatic volatile inputs, andphase separation of hydrothermal fluids (Von Damm
1995; Butterfield et al. 2003; German and Von Damm
2004; Tivey 2007). Compositional variations in hydrothermal fluids (particularly energy and carbon sources)
in turn affect biomass production and the diversity ofhydrothermal vent-endemic communities. Consequently,
clarifying the relationships among the geological background of hydrothermal environments, physical andchemical variations in hydrothermal fluids, and the compositional and functional diversity of chemosynthetic
ecosystems has provided important information on thediversification and development of extant deep-sea
hydrothermal ecosystems as well as the generation andsustenance of early ecosystems and possible extraterrestrial life forms.
In deep-sea hydrothermal vents, rapid mixing between
hot reduced hydrothermal fluids and cold oxidized seawater provides chemical energy for microbial activity
and biomass production. To quantify the in situ energetics of chemolithotrophic microorganisms in hydrothermal mixing environments, a thermodynamic model was
first proposed and applied to a basalt-hosted hydrothermal
system at 21° N on the East Pacific Rise (EPR) (McCollom
and Shock 1997). Using batch-mixing models modified

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from this original model, thermodynamic calculations
have been conducted for several hydrothermal vent systems at MOR and arc-backarc (ABA) hydrothermal systems (Shock and Holland 2004; Tivey 2004; McCollom
2007; Amend et al. 2011). These studies have demonstrated differing patterns in the potential energy yields ofvarious in situ metabolic reactions in the mixing zones ofthese habitats, providing the theoretical basis for relationships between hydrothermal fluid chemistry and thediversity of hydrothermal vent-endemic biological communities. However, the hydrothermal systems studied
were quite limited. In addition, the structures and functions of extant chemosynthetic biological communities,
which have been characterized in many previous investigations, have not yet been integrated into development ofthese theoretical relationships.
Many studies have identified high compositional andfunctional diversity of chemosynthetic ecosystems in
geographically and geologically diverse hydrothermal
systems (e.g., in reviews by Huber and Holden 2008;
Nakagawa and Takai 2008; Takai et al. 2006b). Some ofthese studies have noted possible relationships between
the metabolic abundances and compositions of hydrothermal vent-endemic microbial communities and thechemical characteristics of hydrothermal vent fluids indeep-sea hydrothermal systems (Perner et al. 2007, 2010;
Reysenbach and Shock 2002; Takai and Horikoshi 1999;
Takai et al. 2001, 2004a). However, most of these studies
were qualitative and focused mainly on the genetic andphylogenetic diversity of microbial communities andtheir constituents. Thus, the relationships between theabundance and composition of chemolithotrophic microbial communities and the geological and geochemical
environments of global deep-sea hydrothermal systems
remain unclear.
Takai and Nakamura (2010, 2011) first provided clear
evidence of biogeochemical relationships among microbiological community development, the chemical composition of hydrothermal fluids, and the geologicalenvironment of deep-sea hydrothermal systems throughboth thermodynamic calculations of the potential energy
yields of various in situ metabolic reactions and observed compositional and functional diversity of chemosynthetic ecosystems in the mixing zones of thesehabitats. However, examples of hydrothermal systems
for this comparison were still scarce; thus, only microbial populations in chimney habitats adjacent to hightemperature hydrothermal fluids were characterized byquantitative cultivation techniques and included. In thepresent study, we conducted a more comprehensive
evaluation of the relationships among variations in geology, geochemistry, and microbial metabolisms and thediversity of communities in global deep-sea hydrothermal environments, based on compilation of a substantial

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Page 3 of 24hydrothermal fluid chemistry data set and microbialcommunities in the mixing zones of a wide variety ofhabitats.

(2004), and McCollom (2007). The compositions of thehydrothermal solutions in the mixing zones were calculated from those of the end-member vent fluids and seawater (Additional file 1). The model calculation beganwith 1 kg of vent fluid and continued with addition of
successive increments of seawater until a seawater tovent fluid mixing ratio of 1,000:1 was reached. In the
mixing calculations, minerals were not allowed to precipitate and all redox reactions were prohibited, while
acid-base reactions were allowed to equilibrate. In
addition, the temperatures of the calculated mixed solutions were assumed to scale linearly with the temperatures of the end-members, ignoring conductive cooling
and/or heating.
The overall Gibbs free energy for the metabolic reactions was calculated using the following equation:

Methods

We compiled end-member fluid chemistry data for 89
hydrothermal vent sites (Additional file 1). Hydrothermal vent sites were included only if the data set contained complete chemical composition data essential forthe thermodynamic calculations performed in this study,
including H2, H2S, CH4, CO2, Na, Cl, Ca, K, Fe, Mn, and
Si. In addition, the data set included representative geological settings such as MOR hydrothermal systems in
the Pacific, Atlantic, and Indian Oceans; ABA hydrothermal systems in the western Pacific region; and thesediment-associated (SED) hydrothermal systems in theeastern Pacific and Okinawa Trough (Figure 1).
The amount of metabolic energy available for production by chemolithotrophic microorganisms was evaluated as in Takai and Nakamura (2010, 2011). Fouraerobic and anaerobic reactions were considered representative of chemolithotrophic energy metabolisms(Table 1). To simulate mixing of hydrothermal fluidswith seawater in a seafloor hydrothermal system, we
employed a thermodynamic reaction path model, following McCollom and Shock (1997), Shock and Holland

60°W

30°W

0°

30°E

60°E

90°E

ΔGr ¼ ΔGr ˚ þ RT lnQr

ð1Þ

where ΔGr is the Gibbs free energy of the reaction, ΔGr°
is the standard-state Gibbs free energy of the reaction, R
is the universal gas constant, T is the temperature in
Kelvin, and Qr is the activity quotient of the compounds
involved in the reaction. The Qr term takes into accountthe contribution of the fluid composition to the Gibbs
free energy of each reaction, determined based on the

120°E

150°E

180°E

150°W

120°W

MOR
SZ
MOR-B
MOR-U
ABA-M
ABA-F
SED-MORSED-ABA

60°N

Middle Valley
Main Endeavour
Escanaba
Lucky Strike

Menez Gwen
Rainbow
Minami-ensei
Iheya North
Izena

30°N
TAG
SnakePit

30°N
Guaymas Basin
EPR21N

Logatchev

EPR13N
EPR9.50N
Red Lion
Comfortless Cove
Turtle Pits

0°0°Vienna Woods
PACMANUS
EPR17S
EPR18S
EdmondKaireiTow CamTui Malila

30°S

Kilo Moana
ABE

30°S

Mariner
Brother

60°S

60°S

60°W

30°W

0°

30°E

60°E

90°E

120°E

150°E

180°E

150°W

120°W

90°W

Figure 1 Index map showing mid-ocean ridges and subduction zones with active hydrothermal vents used in this study. Abbreviations:
MOR, mid-ocean ridge; SZ, subduction zone; MOR-B, basalt-hosted system in a mid-ocean ridge setting; MOR-U, ultramafic rock-hosted system ina mid-ocean ridge setting; ABA-M, mafic rock-hosted system in an arc-backarc setting; ABA-F, felsic rock-hosted system in an arc-backarc setting;
SED-MOR, sediment-associated system in a mid-ocean ridge setting; SED-ABA, sediment-associated system in an arc-backarc setting.

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Table 1 Metabolic reactions for chemolithoautotrophy considered in this study
Overall chemical reaction

Identified (I)/cultured (C)ΔGr°2, 250 (kJ)aAerobic methanotrophy

CH4 + 2O2 = CO2 + 2H2O

I and C−860.7

Hydrogenotrophic O2 reduction

H2 + 1/2O2 = H2O

I and C

−264.4Thiotrophic (H2S-oxidizing) O2 reduction+
H2S + 2O2 = SO2−
4 + 2HI and C

−758.2Fe(II)-oxidizing O2 reduction

Fe2+ + 1/4O2 + H+ = Fe3+ + 1/2H2O

I and C

−52.6

Hydrogenotrophic methanogenesis

H2 + 1/4CO2 = 1/4CH4 + 1/2H2O

I and C

−49.2

Hydrogenotrophic SO4 reduction+
H2 + 1/4SO2−
4 + 1/2H = 1/4H2S + H2O

I and C

−74.9

Hydrogenotrophic Fe(III) reduction

H2 + 2Fe3+ = 2Fe2+ + 2H+

I and C

−159.2

Anoxic methanotrophy with SO4 reduction−−
CH4 + SO2−
4 = HCO3 + HS + H2O

I but not yet C−30.1

Energy metabolism
Aerobic reactions

Anaerobic reactionsaStandard-state Gibbs free energy of the metabolic reactions at 2°C, 250 bar.

chemical composition of the mixed fluid estimated fromthe reaction path calculations. The energy available fromthe metabolic reactions as a function of temperature(equivalent to the mixing ratio) was calculated by multiplying the calculated Gibbs free energy for the reaction
at each temperature by the concentrations of the reactants in the mixed fluid. This method takes into accountthe stoichiometry of the reaction and the reactants thatare limiting, multiplied by the total amount of mixed
fluid at that temperature (McCollom and Shock 1997;
McCollom 2007).
This calculation yields an estimate of the maximum
energy that is potentially available from the metabolic
reactions per kilogram of mixed fluid. We used the average ΔGr values for four temperature ranges: <25°C, 25°C
to 45°C, 45°C to 80°C, and 80°C to 125°C, representing
the chemolithotrophic metabolisms of psychrophilic,
mesophilic, thermophilic, and hyperthermophilic microbial organisms, respectively.
Geological settings and geochemical characteristics ofseafloor hydrothermal systems

As noted above, we compiled data for 89 deep-sea
hydrothermal vent sites located in various geological settings (Figure 1), including MOR, ABA, and SED hydrothermal systems. These can be further subdivided into
the following six categories: basalt-hosted systems in
MOR settings (MOR-B), ultramafic rock-associated systems in MOR settings (MOR-U), mafic rock-hosted systems in ABA settings (ABA-M), felsic rock-hosted
systems in ABA settings (ABA-F), SED systems in MOR
settings (SED-MOR), and SED systems in ABA settings(SED-ABA).
The molecular and elemental compositions of H2,
H2S, CH4, CO2, Na, Ca, K, Fe, Mn, and Si as well as thepH values of the end-member hydrothermal fluids fromthese sites are plotted against the Cl content in Figure 2.
Nearly all substances exhibited some degree of positiveor negative correlation to the Cl content, reflecting theinfluence of phase separation of hydrothermal fluids.
Here, we focus on hydrothermal fluids with similar Cl
concentrations to seawater in providing a brief overview
of the geological settings and corresponding principal
characteristics of their hydrothermal environments.
MOR hydrothermal systems

The global MOR system is the largest mountain chain in
the world, with a total length of more than 60,000 km.
Magma production in the MOR system far exceeds thatin any other tectonic environment, accounting for morethan 60% by volume of the total annual flux of magmafrom the mantle to the crust (Fisher and Schmincke
1984; Schmincke 2004). Therefore, the MOR system isthe locus of the greatest amount of hydrothermal activity
on Earth. Most MOR hydrothermal vents are hosted bybasalt (often termed mid-ocean-ridge basalt). Therefore,
many studies of deep-sea hydrothermal systems have focused mainly on basalt-hosted hydrothermal systems(Karl 1995; Kelley et al. 2002). However, in recent years,
increasing attention has been paid to hydrothermal systems associated with ultramafic rocks present in the
MOR (Kelley et al. 2001, 2005; Früh-Green et al. 2004),
because the geochemical characteristics of ultramafic
rock-hosted hydrothermal fluids are significantly different from those of basalt-hosted ones (Charlou et al.
2002).
Hydrothermal fluids from basalt-hosted systems arecharacterized by enrichment in base metals, a generally
neutral or weakly acidic in situ pH, and strongly reducing conditions compared to seawater, due to subseafloor hydrothermal reactions between basaltic rocks andseawater at high temperature and pressure (Seyfried
et al. 1991; Wetzel and Shock 2000). However, the fluids
from ultramafic rock-associated systems are often characterized by an abundance of dissolved H2 and CH4compared to basalt-hosted hydrothermal fluids (Figure 2)

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Figure 2 Major elements versus Cl concentration plots for hydrothermal vent fluids. The composition of seawater is also plotted forcomparison.

(Charlou et al. 1998, 2002). This is attributed to differences in the mineralogy and bulk chemistry of the rocks,
resulting in a substantially different alteration reaction
known as serpentinization (Janecky and Seyfried 1986;
Wetzel and Shock 2000; Allen and Seyfried 2003). H2
concentrations of 12 to 16 mmol/kg (roughly 1 to 2

orders of magnitude higher than in basalt-hosted hydrothermal fluids) due to serpentinization have been reported in ultramafic rock-hosted deep-sea hydrothermalvent fluids (Additional file 1) (Charlou et al. 2002; Kelley
et al. 2005). In addition, enrichment of CH4 in ultramafic rock-associated systems is likely associated with

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reduction of CO2 to CH4 under highly reducing (highH2) conditions.

500
MOR-B
MOR-U
ABA-M
ABA-F
SED-MORSED-ABA

450

Although significant global magma production occurs in
the MOR, the second most active volcanic area is the subduction zone (Fisher and Schmincke 1984; Schmincke
2004), where ABA volcanic systems develop. Some arc
volcanoes are subaerial, particularly in continental arc settings, whereas more than 40% of volcanic arcs are oceanicisland arcs where most volcanoes are submarine (Leat and
Larter 2003). In oceanic island arcs and associated backarc basins, many deep-sea hydrothermal vent sites hosted
by active submarine ABA volcanisms have been discovered (Ishibashi and Urabe 1995; Gamo et al. 2006). The
chemical characteristics of these ABA hydrothermal systems are significantly different from those of MOR hydrothermal systems, although they share many common
features derived from the basic reactions and processes ofsubseafloor hydrothermal circulation. In particular, ABA
hydrothermal fluids are characterized by large variations
in chemical composition (Ishibashi and Urabe 1995;
Gamo et al. 2006). This chemical variability is primarily attributed to a variety of host-rock compositions (from basaltic to rhyolitic), abundant input of volatile elementsfrom magmas (e.g., CO2 and SO2), and the variable water
depth (shallow to deep) of the submarine volcanoes.
ABA hydrothermal systems hosted by mafic rocks exhibit chemical characteristics similar to those of basalthosted hydrothermal systems at the MOR (Figure 2). In
contrast, systems hosted by felsic rocks are generally
characterized by lower pH, higher metal concentrations,and a variable redox state compared to mafic rockhosted hydrothermal systems (Figure 2). In addition, because of the subduction of hydrated ocean crust beneathvolcanic arcs and back-arc basins as well as the potential
involvement of more evolved felsic magmas, the volatile
content (H2O, CO2, and SO2) of magmas in ABA settings is much higher than that in MOR settings (e.g.,
Gamo et al. 1997; Embley et al. 2007). ABA hydrothermal systems are also characterized by wide variations inwater depth, and most are significantly shallower thantypical MOR hydrothermal systems (Figure 3). This results in variations in phase separation (boiling) andhydrothermal fluid temperatures in the subseafloor reaction zones, which significantly affect the chemical composition of the hydrothermal fluids. The maximum
temperatures of the hydrothermal vent fluids in thecompiled data were clearly controlled by the two-phaseboundary of seawater (Figure 3).
SED hydrothermal systems

Some hydrothermal vent sites are covered with sediments, which influence the chemical composition of

Temperature (°C)

ABA hydrothermal systems
400
350
300
250
200
150
0

1000

2000

3000

4000

5000

Depth (m)Figure 3 Maximum temperature conditions versus water depth forindividual vent areas. Two-phase curve for seawater (dashed line) is alsoplotted with the liquid field to the lower right of the curve and theliquid + vapor field to the upper left of the curve. The star represents thecritical point of seawater at 407°C and 298 bar. The maximum temperatureof nearly all of the vent fluids is limited by the two-phase boundary.

their hydrothermal fluids. SED hydrothermal systems arefound in both MOR (e.g., Juan de Fuca, Middle Valley,
Escanaba Trough, and Guaymas Basin) and ABA (e.g.,
Okinawa Trough) settings in which hydrothermal ventsites are in close proximity to continental runoff sources.
Irrespective of differences in tectonic setting or hostrock composition, SED hydrothermal systems have characteristic chemical compositions, e.g., relatively high pH,
low metal content, and high CH4 and NH3 concentrations (German and Von Damm 2004). There are only
minor differences in chemical composition between SED
hydrothermal systems in MOR and ABA settings (Figure 2).
Thus, the chemical features of SED hydrothermal ventfluids are more strongly affected by the sediment than by
the tectonic setting or host-rock composition.
Factors controlling hydrothermal fluid chemistry

It is believed that hydrothermal fluid flux is primarily
controlled by the crust (magma) production rate, because magmatic heat derived from creation of new
oceanic crust (cooling from 1,200°C to 350°C) heatshydrothermal fluids from 2°C to 350°C (e.g., Elderfieldand Schultz 1996). Based on this, Kawahata et al. (2001)
estimated that the maximum volume of high-temperaturehydrothermal fluid is twice that of the upper oceanic crust(the volcanic and sheeted dike sequence) and if 65% to
85% of the rocks are altered to secondary minerals, thevolumetric water/rock ratio would be 2.3 to 3.1. This
clearly suggests that high-temperature hydrothermal fluids
are generated under rock-dominated (low water/rockratio) conditions (Kawahata et al. 2001). Therefore, thechemical compositions of hydrothermal fluids are

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predominantly controlled by water-rock reactions andfluid-mineral equilibria (Seyfried et al. 1991; Shock 1992;
Seyfried and Ding 1995). Thus, host-rock geochemistry is
one of the most important factors controlling hydrothermal fluid chemistry. In addition to the chemical compositions of host rocks, however, other processes such as
input of volatiles from magmas, phase separation ofhydrothermal fluids, and interactions with sediment also
have a significant impact on the observed compositions ofhydrothermal fluids.

Basalt-hosted hydrothermal fluids are also highly reducing, as evidenced by the presence of H2S rather
than SO4, as well as by significant amounts of H2,
CH4, Fe2+, and Mn2+. These chemical features are generally consistent with phase-equilibrium calculations
involving the observed primary and secondary minerals(feldspar, chlorite, epidote, quartz, magnetite, anhydrite,
pyrite, and pyrrhotite) and seawater at in situ hydrothermal fluid temperatures and pressures (Bowers
et al. 1988; Seyfried et al. 1988, 1999; Saccocia andSeyfried 1990; Seyfried and Ding 1995; McCollum andShock 1998; Wetzel and Shock 2000). Time-series
measurements of chemical compositions of hydrothermal fluids in MOR regions have indicated steady-state
concentrations of dissolved species (Campbell et al. 1988;
Bowers et al. 1988; Butterfield et al. 1994; Von Damm
1988, 1995, 2000), reflecting clear solubility control bymineral phases in the subseafloor reaction zones and recharge zones.

Chemical composition of host rocks

Differences in the rock types in the reaction zone canlead to large variations in the hydrothermal fluid chemistry, because the bulk chemical composition and primary minerals in the source rock control the reaction
sequences and their chemical equilibria.
Mafic rocks Most ocean basins (including MOR and
ABA settings) are of mafic composition (mainly basaltic).
The chemical systematics of mafic rock-seawater systems (particularly basalt-seawater systems) have been
well characterized based on field observations, hydrothermal experiments, and theoretical studies (Bischoffand Dickson 1975; Mottl and Holland 1978; Seyfried
and Mottl 1982; Mottl 1983; Reed 1983; Bowers andTaylor 1985; Seyfried 1987; Von Damm 1990, 1995;
Seyfried et al. 1988, 1991; Shock 1992; Saccocia et al.
1994; Wetzel and Shock 2000; Butterfield et al. 2003;
Nakamura et al. 2007).
Basalt-hosted hydrothermal fluids have relatively low
pH at 25°C and 1 atm (generally 3 to 4) and notable enrichment in base metals (e.g., Fe and Mn) and dissolved
gases (e.g., H2, CO2, and CH4) compared to seawater(Figure 2). The in situ pH of the basalt-hosted ventfluids are neutral to weakly acidic, significantly different
from the pH measured at 25°C and 1 atm in laboratory
experiments (German and Von Damm 2004). This discrepancy is mainly caused by dissociation of H+-bearing
aqueous complexes (e.g., HCl0) due to cooling during
sample processing (Shock et al. 1989; Seyfried et al.
1991; Ding and Seyfried 1992; Ding et al. 2005). Anotherpossible mechanism of pH change is precipitation of
metal sulfides below the seafloor, producing protons(German and Von Damm 2004).
In high-temperature MOR vent fluids, most metals areenriched by up to 7 to 8 orders of magnitude compared
to seawater. The stability of chloride complexes (e.g.,
FeCl02) increases with increasing temperature, and therefore, most metal ions are present in high-temperature
fluids as chloride complexes (Helgeson et al. 1981; Ding
and Seyfied 1992). The substantial increase in the metalsolubility produces the high concentrations in the ventfluids.

Ultramafic rocks Compared with hydrothermal fluids
in mafic rock-hosted systems, ultramafic rock-associatedhydrothermal fluids are characterized by conspicuous
enrichment in H2 in the presence or absence of phaseseparation processes (Figure 2). Production of H2 duringserpentinization of ultramafic rocks results from reaction of water with Fe2+-bearing minerals, primarily olivine and pyroxene. In these reactions, Fe2+ is partially
oxidized to Fe3+ by the water, resulting in precipitationof magnetite in the serpentinite. The water reduced by
the Fe2+ also produces H2. One of the important chemical features of ultramafic rocks that constrains abundant
H2 production during serpentinization is relatively low
Al concentrations. Low Al activity results in formationof alteration minerals (particularly serpentines and brucite) that have a tendency to exclude Fe2+ from theirstructure. This leads to oxidation of Fe2+ by water toform magnetite. In contrast, because mafic rocks havehigher Al contents than ultramafic rocks, a muchgreater proportion of the Fe2+ is sequestered in Albearing alteration minerals (e.g., chlorite), limiting oxidation of Fe2+ to Fe3+. Thus, hydrothermal alteration ofmafic rocks generates much lower amounts of H2 andmagnetite than serpentinization of ultramafic rocks,
even though the Fe content of basaltic rocks is higher
than that of ultramafic rocks. Basaltic rock-hosted ventfluids typically exhibit H2 concentrations of <1 mmol/
kg, whereas >10 mmol/kg H2 has frequently been reported for ultramafic rock-associated fluids (Additional
file 1). The potential for even higher H2 concentrations(>100 mmol/kg) has been suggested by both petrological (Frost 1985; Alt and Shanks 1998) and experimental(Berndt et al. 1996; McCollom and Seewald 2001)
studies.

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In addition, ultramafic rock-associated hydrothermal
fluids are often characterized by CH4 enrichment(Figure 2). Although the origin of CH4 in these fluids iscontroversial, it is generally thought to be derived fromreduction of CO2 by high concentrations of H2 throughabiotic methanogenesis (Nakamura et al. 2009). However, the hydrothermal fluid CH4 concentrations are always disequilibrated with the concomitant H2 and CO2
concentrations, suggesting that the subseafloor hydrothermal circulation system is an open system with respect to CH4 content. Enriched CH4 (>0.5 mmol/kg) has
also been observed in hydrothermal fluids from certain
basalt-hosted systems at the MOR (Figure 2; Lucky
Strike and Menez Gwen hydrothermal fields) (Additional
file 1). Both of these fields are located in the northern
Mid-Atlantic Ridge, where several ultramafic rockassociated hydrothermal systems have been discovered.
Based on geological and geochemical lines of evidence, it
has been suggested that the high CH4 concentrations inthese basalt-hosted hydrothermal fluids were caused byserpentinization of ultramafic rocks somewhere in thesubseafloor (Charlou et al. 2000).

felsic rocks are lower than those in basaltic rocks. The
Fe and Mn concentrations in deep-sea hydrothermal
fluids are correlated not only with Cl concentrations but
also with pH (Figure 4). Moreover, the Fe/Cl and Mn/Cl
ratios for hydrothermal fluids exhibit strong correlations
with pH (Figure 4). This clearly shows that the concentrations of heavy metals in deep-sea hydrothermal fluids
are mainly controlled by the pH of the hydrothermal
fluids.

Felsic rocks Hydrothermal systems hosted by felsic rocks
have been identified only in ABA settings (Figure 1). Felsicrock-hosted hydrothermal fluids are characterized by relatively low pH and enrichment in H2S, CO2, K, Mn, and Fe
compared to mafic rock-hosted fluids (Figure 2). The
chemical characteristics of felsic rock-hosted hydrothermal fluids are generally consistent with experimental results for seawater-felsic rock interactions (e.g., Hajash andChandler 1981). For example, felsic rocks contain highconcentrations of incompatible elements such as K. Enrichment of K in felsic rock-hosted fluids originates fromthe bulk rock composition. In addition, the lower pH is attributed to the low ability of felsic rocks to consume H+ in
solution. The pH of a hydrothermal solution is lowered byremoval of Mg2+ via precipitation of Mg-hydroxysulfate
during heating of the seawater (Bischoff and Seyfried1978) and by formation of Mg-bearing alteration minerals(e.g., smectite and chlorite) during seawater-rock interactions (Mottl 1983). In a basalt–seawater system, the H+
generated in the fluid is consumed by dissolution of Ca
from the reacted rocks (Seyfried and Mottl 1982; Mottl
1983). Mg-Ca exchange reactions control the fluid pH toapproximately neutral under in situ conditions (Seyfried
and Mottl 1982; Wetzel and Shock 2000). However, because felsic rocks are relatively depleted in Ca, their ability
to buffer pH changes is significantly lower than that of
their mafic counterparts.
Low pH in hydrothermal fluids promotes leaching ofheavy metals through water-rock interactions. This ultimately results in high concentrations of heavy metals,
although the initial concentrations of heavy metals in

Inputs of magmatic volatiles

Enrichment of H2S and CO2 in felsic rock-hosted hydrothermal fluids cannot be explained only by water-rockinteractions. Instead, enrichment in these volatiles canbe caused by inputs of magmatic volatiles into hydrothermal systems. ABA magmas (particularly those thatare felsic in composition) have very high concentrationsof volatile elements and molecules, and hydrothermal
fluids that are highly enriched in sulfur and/or CO2 havebeen observed in ABA hydrothermal systems, mainly
hosted by more siliceous rocks, e.g., andesite, calcite,
and rhyolite rather than by basalt (Gamo et al. 1997;
Sakai et al. 1990; Inagaki et al. 2006; Lupton et al. 2006,2008). Therefore, enrichment in CO2 and H2S of felsicrock-hosted hydrothermal fluids is likely due to significant inputs of magmatic volatiles into these hydrothermal systems.
Dissolution of CO2 gas into a hydrothermal fluid results in production of H+ in the fluid via the following
reaction:
CO2 þ H2 O ¼ HCO3 − þ Hþ :

ð2ÞCompared to that for SO2 (see below), the dissociation
constant of this reaction is much smaller, particularly
under high-temperature conditions. It is therefore believed that the effect of CO2 on the fluid pH is not verysignificant. However, segregation of CO2 from upwellinghydrothermal fluids in the subseafloor can result in consumption of H+ in the fluid, increasing the pH. Even asmall pH increase during ascent of the hydrothermal
fluid can cause subseafloor precipitation of metal-sulfide
minerals, resulting in low heavy metal concentrations in
the hydrothermal fluids. This process would be expectedin hydrothermal systems with significant inputs of CO2
but not SO2 from magma, such as hot spot-influenced
MOR hydrothermal systems and basalt-hosted arcbackarc hydrothermal systems.
Volatile sulfur species in the magma have a more significant effect on deep-sea hydrothermal systems. The
predominant gaseous sulfur species in magma are SO2and H2S (Wallace and Edmonds, 2011). Although dissolution of H2S does not significantly affect hydrothermal
fluid chemistry, that of SO2 into hydrothermal fluids

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100

10

10
1

Mn (mM)Fe (mM)

1

0.1

0.1

0.01

0.01

(B)

(A)
0.001

0.001

1

0.1

MOR-B
MOR-U
ABA-M
ABA-F

0.1
0.01

SED-MORSED-ABA

Mn/Cl

Fe/Cl

0.01
0.001

0.001

0.00010.00010.00001(C)(D)

0.000001

0.00001
2

3

4

5

6

7

8

2

3

4

5

6

7

8

pH

pH

Figure 4 Plots of (A) Fe, (B) Mn, (C) Fe/Cl, and (D) Mn/Cl versus pH for hydrothermal vent fluids. These plots clearly show that concentrationsof Fe and Mn in hydrothermal vent fluids are mainly controlled by pH.

increases the f O2 and sulfuric acid in the fluids via thefollowing reactions:
2SO2 þ 2H2 O ¼ 2H2 S0 þ 3O2

ð3Þ

2SO2 þ O2 þ 2H2 O ¼ 2HSO4 − þ 2Hþ :ð4Þ

Nevertheless, felsic rock-hosted hydrothermal systems
affected by magmatic volatile inputs clearly exhibit highconcentrations of base metals and low pH (Figure 4).
Phase separation

Once the f O2 of the hydrothermal fluid reaches thesulfate-sulfide boundary via reaction (3), sulfuric acid is
produced by reaction (4). The presence of sulfuric acidcan cause a significant decrease in pH. Because the solubility of heavy metals is quite sensitive to pH, the pH decrease caused by SO2 promotes dissolution of heavy
metals from the reacted rocks. Volatile inputs frommagmas occur intermittently, and even during such activity, the chemistry of hydrothermal fluids is controlled
by reactions induced by both volatile inputs and waterrock interactions. Therefore, it is likely that the chemicalcomposition of the fluids, as is typical of open and dynamic systems, significantly varies with space and time.

As described above, the concentrations of all components in hydrothermal fluids exhibited positive or negative correlations with Cl, except for H2, CO2, and CH4
in several samples affected by serpentinization of ultramafic rocks, CO2 inputs from magma, and CH4 inputs
from sedimentary organic matter and/or microbial processes (Figure 2). Deep-sea hydrothermal fluids often
reach temperatures high enough that they separate into
vapor and brine phases. The phase separation temperature depends primarily on the pressure conditions(i.e., water depth) of the hydrothermal system. The observed temperatures of hydrothermal fluids from various
vent sites were clearly limited by the two-phase boundary of seawater (Bischoff and Pitzer 1989) (Figure 3).
Phase separation and subsequent remixing of the vapor

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and brine phases produce hydrothermal fluids with awide range of salinities, from 1 order of magnitude lower
to several times higher than that of seawater (Figure 2).
The chemical properties of the vapor and brine phases
are quite different from each other and from their parent
fluid, because each of the chemical species in the parent
fluid is distributed preferentially into the vapor and liquid phases according to their physical and chemical
properties during phase separation (Butterfield et al.
2003; Foustoukos and Seyfried 2007). The concentrations of gaseous species greatly increased with decreasing Cl concentration, indicating the strong affinity ofthese volatile components for the vapor phase (Figure 2).
In contrast, the positive correlations between the Cl concentration and other dissolved species that are primarily
ionic (e.g., Na+ and Cl−) indicate the strong affinity ofthese species for the liquid phase. In addition, the relationships between the Cl concentration and the ratios ofelements to chloride clearly showed a strong increase in
the ratios of gaseous species to chloride with decreasing
Cl concentration (Figure 5). The Si/Cl ratio also slightly
increased with decreasing Cl concentration. This indicates that, in addition to gaseous species, neutral species
such as SiO02 have some affinity for the vapor phase. On
the other hand, there was little change in the ratios ofionic species with Cl concentration as a result of phaseseparation, indicating that they all partition strictly into
the brine phase. These chemical behaviors of the
dissolved species during the phase separation and partitioning into hydrothermal fluids result in formation of
low-Cl, vapor-dominated fluids enriched in gases and ofresidual brines enriched in ionic species and depleted ingases.

and Von Damm, 2004). This greatly decreases the solubility of metal-sulfide minerals, leading to low heavy
metal concentrations in the hydrothermal-vent fluids.

Presence of sediments

SED hydrothermal systems have chemical compositions
distinct from those of other hydrothermal fluids. Compared to those of sediment-starved MOR and ABAhydrothermal systems, SED hydrothermal fluids generally have relatively high pH, lower heavy metal contents,and higher CH4 and NH+4 concentrations (Figure 2)(German and Von Damm, 2004). The very high CH4
concentrations of hydrothermal fluids in SED systems
are attributed to thermal decomposition of organic matter at high temperatures during hydrothermal reactions
at discharge zones and/or microbial methanogenesis at
relatively low temperatures at sedimentary rechargezones (Lilley et al. 1993; Kawagucci et al. 2011, 2013).
Likewise, the source of NH+4 in SED hydrothermal systems is considered to be thermal decomposition and microbial ammonification of organic matter (Kawagucci
et al. 2011, 2013). High concentrations of NH+4 in thesehydrothermal fluids provide an NH3/NH+4 buffer thatmaintains the relatively high pH of the fluid (German

Effects of hydrothermal fluid chemistry on thebioavailable energy yield

The chemosynthetic primary producers that sustain
deep-sea hydrothermal vent ecosystems utilize inorganic
substances (e.g., H2S, CO2, H2, and CH4) derived fromhydrothermal vent fluids as energy and carbon sources.
Thus, deep-sea hydrothermal vent ecosystems should be
at least partially controlled by the chemical compositionof the hydrothermal fluids. The effects of hydrothermal
fluid compositions on deep-sea hydrothermal vent ecosystems based on the energy yields available to various
chemolithotrophic metabolisms are described below.
Hydrogen sulfide (H2S)

In all of the deep-sea hydrothermal systems in all settings, the potential energy yields for sulfur-oxidizing
chemolithotrophy (thiotrophy) using H2S in the hydrothermal fluids were uniformly high at >10 J/kg mixed
fluid (Figure 6A). Even in ultramafic rock-associatedhydrothermal systems with relatively low H2S concentrations, the metabolic energy of sulfur oxidation (H2S oxidation) was nearly identical to that in other types ofhydrothermal systems, some of which had 2 orders ofmagnitude higher H2S concentrations (Figure 6A). This
uniformity is attributed to the relatively high concentrations of H2S (mostly >1 mmol/kg) present in hydrothermal fluids in all of the hydrothermal systems. As aresult, the amount of H2S always exceeded the O2 concentration throughout the habitable temperature range
in the mixing zones, except at very low temperatures(several degrees Celsius). The potential energy yield of
sulfur-oxidizing chemolithotrophy is therefore solely
controlled by the dissolved O2 concentration in the seawater (which is globally similar in all deep-sea water).
Thus, concentrations of H2S in end-member hydrothermal fluids may not significantly affect the abundanceand composition of sulfur oxidizers.
The exception is in hydrothermal plumes, where muchhigher seawater mixing ratios (>1000) and low temperatures (up to several degrees Celsius) are found. In hydrothermal plume environments, the concentration of H2S
in the source hydrothermal fluid, rather than theseawater-dissolved O2, becomes the limiting factor forsulfur-oxidizing chemolithotrophic metabolism.
Hydrogen (H2)

In contrast to H2S, variations in the H2 concentration
directly affected the potential energy for the chemolithotrophic microbial population, not only for aerobic H2 oxidation but also for most anaerobic energy metabolisms

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Figure 5 Plots of major element to Cl ratios versus Cl for hydrothermal vent fluids.

other than anaerobic methane oxidation. This feature ispartially attributed to the wide range of H2 concentrations
in hydrothermal fluids. For example, typical basalt-hostedhydrothermal fluids had H2 concentrations of <1 mmol/kg (Figure 2). In contrast, ultramafic rock-hosted hydrothermal fluids had H2 concentrations 1 to 2 orders ofmagnitude higher, whereas hydrothermal fluids in ABA
settings had H2 concentrations 1 order of magnitude

lower (Figure 2). Thus, potential energy yields for aerobic
and anaerobic H2-oxidizing (H2-trophic) metabolisms
were directly correlated with H2 concentrations in theend-member hydrothermal fluids (Figure 6B, C, D).
For aerobic H2-oxidizing metabolism, nearly the sameamount of metabolic energy was available irrespectiveof the H2 concentration in the end-member hydrothermal
fluid (Figure 6B), when the H2 concentration exceeded

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100

100

10

10

1

0.1

(A) H2S oxidation

1
0.1

1

10

(B) H2 oxidation
100

0.01
0.001

0.01

Potential metabolic energy (J/kg mixed fluid)

H2S (mM)

1

10

100

H2 (mM)

1000

1000

100

100

10

10

1

1

0.1

0.1

0.01
0.001
0.001

0.1

0.01

(C) SO4 reduction
0.01

0.1

1

10

(D) Methanogenesis

100

0.001
0.001

0.01

H2 (mM)

0.1

1

10

100

H2 (mM)
1000

100

100
10
10
1

1

0.1
0.1

0.01
0.001

(E) Aerobic CH4oxidation
0.01

0.1

1

(F) Anaerobic CH4oxidation

0.01

10

100

CH4 (mM)

0.001
0.001

0.01

0.1

1

10

CH4 (mM)

100

MOR-B
MOR-U
ABA-M
ABA-F
SED-MORSED-ABA

10

1

0.1

0.01
0.01

(G) Fe2+ oxidation
0.1

1

Fe2+ (mM)
Figure 6 (See legend on next page.)

10

100

<25 °C
25–45 °C
45–80 °C
80–125 °C

100

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Page 13 of 24(See figure on previous page.)
Figure 6 Metabolic energy yields versus H2S, H2, CH4, and Fe2+ concentrations in hydrothermal fluids. Potential metabolic energy
available from (A) thiotrophic (H2S-oxidizing) O2 reduction as a function of the H2S concentration in the end-member hydrothermal fluid; (B)hydrogenotrophic O2 reduction, (C) hydrogenotrophic SO4 reduction, and (D) hydrogenotrophic methanogenesis as a function of the H2 concentrationin the end-member hydrothermal fluid; (E) aerobic methanotrophy and (F) anoxic methanotrophy as a function of the CH4 concentration in theend-member hydrothermal fluid; and (G) Fe2+-oxidizing O2 reduction as a function of the Fe2+ concentration in the end-member hydrothermal fluid
are plotted for each kilogram of mixing water for four temperature ranges. The temperature ranges of <25°C, 25°C to 45°C, 45°C to 80°C, and 80°C to
125°C generally correspond to psychrophilic, mesophilic, thermophilic, and hyperthermophilic microbial components, respectively.

approximately 1 mmol/kg (for hyperthermophiles at relatively high temperatures) to approximately 10 mmol/kg(for psychrophiles to hyperthermophiles at all temperature
ranges). As with H2S oxidation, this occurs because
seawater-dissolved O2 rather than H2 becomes the limiting factor for aerobic H2-oxidizing metabolism.
However, because most seafloor hydrothermal fluids
had H2 concentrations <1 mmol/kg, except for ultramafic rock-hosted and highly vapor phase-enrichedhydrothermal fluids (Figure 2), variations in the H2 concentration of the end-member hydrothermal fluid significantly affected the potential energy yields of nearly
all H2-trophic chemolithotrophs (Figure 6B, C, D). Thisvariation is expected to have a strong impact on biomass
production and the compositional structure of most H2trophic microbial populations as well as the entire microbial community. As described above, the abundanceof H2S in hydrothermal fluids is relatively constantamong most hydrothermal systems, tectonic settings,
and geological conditions. In addition, H2S is coupled
only to aerobic (both O2- and NO3-reducing) sulfuroxidizing metabolisms. In contrast, the abundance of H2
in end-member hydrothermal fluids is highly variable
and constrains various aerobic and anaerobic chemolithotrophic energy metabolisms for primary production.
Although ultramafic rock-associated hydrothermal
fluids are significantly enriched in H2 (Charlou et al.
2002), in several phase separation-influenced (vapor
phase-abundant) hydrothermal fluids hosted by MOR-B,
H2 can also be comparably enriched (Lilley et al. 2003)(Figure 2). In these hydrothermal systems, therefore, theenergy yield of H2-trophic metabolisms was similar tothat in ultramafic rock-hosted hydrothermal systems(Figure 6B, C, D). However, the abundant availability of
H2 (as well as other gaseous species) induced by phaseseparation in MOR-B-hosted hydrothermal fluids is generally transient and lasts several weeks to several months(Lilley et al. 2003). Thus, the effect of temporal enrichment of hydrothermal fluid H2 on biomass production
and compositional structure of the entire microbial community is likely transient and minor.
Methane (CH4)The CH4 concentration in seafloor hydrothermal fluids
was also variable, ranging from the nanomole perkilogram level in ABA hydrothermal fluids to the millimole per kilogram level in SED and ultramafic rockhosted fluids. Variations in the CH4 concentration inhydrothermal fluids could affect both aerobic and anaerobic methane oxidizers (Figure 6E, F).
The potential metabolic energy from anaerobic CH4 oxidation (methanotrophy) was directly correlated with theCH4 concentration in the hydrothermal fluid (Figure 6F),
suggesting that the anaerobic methanotrophic population is likely affected by CH4 concentrations in endmember hydrothermal fluids. This is attributable to thelarge amount of SO42− in seawater; these high levels ofSO42− are always present in seawater-hydrothermal fluid
mixing zones in all habitable temperature ranges. For
aerobic CH4 oxidation reactions, the potential energy
yield was also affected by the CH4 concentration in
end-member hydrothermal fluids, except for hydrothermal fluids with high CH4 concentrations (>0.2 mmol/kg
for hyperthermophiles to >2 mmol/kg for psychrophiles)(Figure 6E).
Iron (Fe)

Variation in the Fe2+ concentration of the hydrothermal
fluids was also large, from the nanomole per kilogramlevel to the millimole per kilogram level (comparable to
the ranges for H2 and CH4 concentrations). This variation in the Fe2+ concentration of the hydrothermal
fluids could affect aerobic iron-oxidizing chemolithotrophy. The potential energy yield from the aerobic Fe oxidation reaction was well correlated with the Fe2+
concentration in the hydrothermal fluid (Figure 6G).
However, for highly Fe2+-enriched hydrothermal fluids(>0.2 mmol/kg for hyperthermophiles to >2 mmol/kg
for psychrophiles), the amount of available metabolic energy was saturated with respect to the Fe2+ concentration in the end-member hydrothermal fluid (Figure 6G).
The metabolic energy yield potentially obtained fromaerobic oxidation of 1 mol of Fe2+ was several times
smaller than that from aerobic oxidation of 1 mol of
H2S, H2, or CH4 (Figure 6). This may affect the relative
abundance of aerobic Fe-oxidizer populations in deepsea hydrothermal vent ecosystems.
In contrast to aerobic Fe-oxidizing chemolithotrophy,
there was an essentially negligible energy yield predicted
for anaerobic Fe3+ reduction using H2 or CH4 for allNakamura and Takai Progress in Earth and Planetary Science 2014, 1:5
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Page 14 of 24

types of deep-sea hydrothermal fluids and systems. This
is attributed to an extremely low concentration of Fe3+
in both seawater and hydrothermal fluids.

may supply more abundant and diverse energy sources
for biological production.
In the SED setting, aerobic methanotrophy could becompetitive with aerobic sulfur oxidation in all temperature ranges (Figure 8A). Interestingly, among all
possible chemolithotrophic metabolisms, anaerobic (sulfate-reducing) methanotrophy was by far the mostfavorable energy-generating metabolism, particularly inhigh-temperature habitats (Figure 8B). The total amountof potentially bioavailable energy yield in the mixing
zones of habitats in the SED setting was also greaterthan in the typical MOR-B and ABA settings.

Effect of the geological setting of the hydrothermal
system on the bioavailable energy yieldIn the MOR-B and all ABA settings (comprising mostdeep-sea hydrothermal systems), almost all potentiallybioavailable energy can be obtained from aerobic metabolism (Figure 7). The end-member hydrothermal fluids inthese settings contain only small amounts of H2 and CH4(other than highly vapor-enriched hydrothermal fluids).
The most energetically favorable chemolithotrophic metabolism was aerobic sulfur oxidation (Figure 8A). Thus,
aerobic sulfur oxidizers are the chemolithoautotrophic
population most likely to sustain primary production inthese deep-sea hydrothermal vent ecosystems.
In the MOR-B and ABA-M settings, aerobic oxidationof H2 and CH4 were the second most available metabolic
reactions, particularly at higher temperatures (lower
mixing ratios). On the other hand, in the ABA-F setting,aerobic Fe2+ oxidation was the second most favorable
chemolithotrophic metabolism (Figure 8A). These differences are directly related to the different chemical compositions of the end-member hydrothermal fluids (e.g.,
H2, CH4, and Fe2+ concentrations) in these settings, ultimately derived from the oxidation state of the magmas
and/or volatile (particularly SO2) inputs into the hydrothermal fluids. Relatively little energy was predicted to
be available from anaerobic chemolithotrophic metabolisms for these settings, except for temporally andspatially limited habitats induced by phase separation ofhydrothermal fluids (Figure 8B).
In the MOR-U and SED settings, the potential energy
from aerobic oxidation of H2 or CH4 exceeded that fromaerobic sulfur oxidation at higher temperatures (lower
mixing ratios) (Figure 8A). More importantly, in thesesettings, considerable energy for primary production canbe obtained from anaerobic chemolithotrophic metabolisms and populations (Figure 8B). Particularly in hightemperature habitats, anaerobic chemolithotrophs are
expected to play a prominent role as primary producers(Figure 8A, B). This represents a marked difference inpotential chemolithotrophic microbial communities between the MOR-U and SED settings and the more common MOR-B and ABA settings.
In the MOR-U setting, because of the high H2 concentrations in end-member fluids, both aerobic and anaerobic H2-trophic population reducers were energeticallydominant primary producers (Figure 8A, B). In addition,
the total potentially bioavailable energy yields in the
mixing zones were greater in the MOR-U setting than in
the typical MOR-B and ABA settings (Figure 8A, B).
Thus, the MOR-U deep-sea hydrothermal environments

Comparison of existing chemolithotrophic microbialcommunities with the results of thermodynamic modeling

Above, we have provided the theoretical basis for relationships between the geological environments of hydrothermal activity (e.g., tectonic settings, basement-rockgeochemistry, abundance of sediments, magmatic volatile
input, and phase separation related to subseafloor hydrothermal processes), physical and chemical variations inhydrothermal fluids, and the compositional diversity ofpotentially bioavailable energy for various vent-endemic
chemolithotrophic metabolisms estimated using thermodynamic models. We have shown that the abundance andcomposition of chemolithotrophic energy metabolisms inhydrothermal vent biological communities is directly constrained by the physical and chemical characteristics ofthe hydrothermal mixing zones of habitats, which are subject to the physical and chemical properties of endmember hydrothermal fluids. Furthermore, the physicaland chemical characteristics of the end-member hydrothermal fluids are substantially controlled by the geological settings that host the hydrothermal systems. Thus,
it seems likely that the abundance and composition ofchemolithotrophic energy metabolisms in microbial communities located in a given deep-sea hydrothermal system
could be systematized in terms of geological backgrounds
based on the results of the thermodynamic models.
In typical mixing zones in deep-sea hydrothermal habitats, chemolithotrophic microbial communities consist oforganisms with three typical lifestyles: surface-attached or
biofilm-forming free-living entities, planktonic free-living
entities, and symbiotic entities. Here, we discuss potential
patterns in chemolithotrophic microbial community
development delineated by recent microbiological investigations (biogeochemical, ecological, and molecular approaches) for representative hydrothermal mixing zonesof habitats in which the predominant organisms have different lifestyles.
Hydrothermal plumes

Hydrothermal plumes are typical of mixing zone habitatsthat host planktonic free-living microbial communities

800

700

900

900

0

<25 ºCMAR

Aerobic reactions
Anaerobic reactions

Vienna Woods

CIR

ABA-M

CIR
Lau
Lau
PACMANUS

500

400

300

200

100

1000
0

900

25–45 ºC

800

700

600

500

400

300

200

100

1000
0

45–80 ºC

800

700

600

500

400

300

200

100

1000
0

80–125 ºC

800

700

600

500

400

300

200

100

Okinawa Trough600

Juan de Fuca
GuaymasOkinawa Trough Iheya North NBC
Okinawa Trough Izena HAKUREI
Okinawa Trough Izena JADE
Okinawa Trough Minami-Ensei

Kermadec

ABA-F

Guaymas basin
Escanaba TroughMEF at JdFR Hulk1999
MEF at JdFR Dante1999
MEF at JdFR Bastille1999
MEF at JdFR Cantilever1999
MEF at JdFR Sully1999
Middle Valley Site 856
Middle Valley Site 858

Lau Basin Mariner
Lau Basin Mariner-brine
Lau Basin Mariner-vapor
PACMANUS RMR1
PACMANUS RMR2
PACMANUS RMR3
PACMANUS RMR4
PACMANUS RGR1
PACMANUS RGR2
PACMANUS SM1
PACMANUS SM2PACMANUS SM3
PACMANUS F1PACMANUS F2PACMANUS F3PACMANUS F4
Kermadec #851-3A
Kermadec #852-2B

EPR

Vienna Woods VW1
Vienna Woods VW2Vienna Woods VW3
Lau Basin Kilo Moana
Lau Basin Tow Cam
Lau Basin ABE
Lau Basin Tui Malila

1000

MOR-U

MAR

MOR-B

Rainbow
Logatchev 1996
Kairei #4
Kairei #5
Kairei #6
Kairei KaliKairei Fugen

900

EPR 9º50'N Aa1
EPR 9º50'N Aa2
EPR 9º50'N Aa3
EPR 9º50'N Bio9
EPR 9º50'N Bio9
EPR 9º50'N Bio9
EPR 9º50'N Bio9
EPR 9º50'N Bio9’
EPR 9º50'N Bio9
EPR 9º50'N Bio9’
EPR 9º50'N Bio9’
EPR 13ºN
EPR 17º25'S Nadir 03-G
EPR 17º25'S Rehu-Marka 19-D
EPR 18º15'S Akorta 17-D
EPR 18º26'S Stockwork 08-G
EPR 18º26'S Fromveur 09-D
EPR 18º26'S Fromveur 13-G
EPR 21ºN OBSEPR 21ºN NGSEPR 21ºN SW
Lucky Strike Y3
Lucky Strike Eiffel
Lucky Strike Mrk US4
Lucky Strike Mrk US6
Lucky Strike Mrk US7
Lucky Strike Helene
Menez Gwen Menez flankMenez Gwen Mogued Gwen1
SnakePit MARK-1
SnakePit MARK-2
TAG 1993BS
Turtle Pit 2005 Two Boats
Comft. Cove 2006 Sisters Peak
Red Lion 2005 Mephisto
Edmond #2
Edmond #10
Edmond #12
Edmond A
Edmond Nura Nura
Edmond White Head

Potential metabolic energy (J/kg mixed fluid)

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SED-MORSED-ABA

Figure 7 Metabolic energies available from the aerobic and anaerobic reactions shown in Table 1. Calculations were performed for all the
89 hydrothermal vent sites in MOR-B, MOR-U, AMA-M, ABA-F, SED-MOR, and SED-ABA settings. Shaded areas represent hydrothermal vents
issuing highly vapor-rich (<100 mmol/kg Cl) fluids.

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Figure 8 Metabolic energies available from each (A) aerobic and (B) anaerobic reactions shown in Table 1. Calculations were performedfor H2 oxidation, H2S oxidation, methanotrophy, and Fe2+ oxidation (aerobic reactions) and hydrogenotrophic methanogenesis, hydrogenotrophic SO4
reduction, anoxic methanotrophy, and anaerobic Fe3+ reduction (anaerobic reactions) at the 89 hydrothermal vent sites in MOR-B, MOR-U, AMA-M,
ABA-F, SED-MOR, and SED-ABA settings. Shaded areas represent hydrothermal vents issuing highly vapor-rich (<100 mmol/kg Cl) fluids.

and are characterized by low temperatures and quite low
mixing ratios of hydrothermal fluids (<0.1%). In hydrothermal plumes, the SUP05 group of Gammaproteobacteria is the most abundant and geographicallywidespread microbial component (Sunamura et al. 2004;
Dick and Tebo 2010; German et al. 2010). The deepsea vent Epsilonproteobacteria (Sunamura et al. 2004;
Nakagawa et al. 2005a; German et al. 2010), methanotrophic
Gammaproteobacteria (Lam et al. 2008), and ammoniaoxidizing Betaproteobacteria and Thaumarchaeota (Lamet al. 2008; Takai et al. 2004b) have been identified asother dominant microbial populations.
Although microbial communities in hydrothermal
plumes have variable abundances and compositions ofchemolithotrophic metabolisms, there have been few
quantitative studies or functional characterizations ofthese communities. Thus, we still do not know muchabout how these microbial communities and their metabolisms respond to the varying physical and chemical
states of hydrothermal plume habitats or how they are
related to the geological backgrounds that produce thesource hydrothermal fluids. Nevertheless, the generallandscape of metabolic abundance and composition inhydrothermal plume microbial communities has been
established via biogeochemical (Cowen et al. 1986; deAngelis et al. 1993; Mandernack and Tebo, 1993; Dicket al. 2009) and microbial ecology (Sunamura et al. 2004;
Takai et al. 2004b; Nakagawa et al. 2005a; Lam et al.
2008; Dick and Tebo 2010; Lesniewski et al. 2012) investigations. For example, dominance of the sulfuroxidizing SUP05 group of Gammaproteobacteria and the
deep-sea vent Epsilonproteobacteria is commonly observed in geographically and geologically diverse deepsea hydrothermal systems. These organisms primarily
sustain themselves via aerobic sulfur oxidation; considerable populations occasionally utilize aerobic H2 oxidation
for additional energy conversion if metabolically available
H2 is present. In addition, much smaller but ubiquitous
populations of phylogenetically diverse bacteria also utilize
Fe2+ and Mn2+ oxidation for biomass production. In contrast, in hydrothermal plumes highly enriched in CH4 andNH+4 , particularly in SED hydrothermal systems, theNakamura and Takai Progress in Earth and Planetary Science 2014, 1:5
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methanotrophic Gammaproteobacteria and ammoniaoxidizing Betaproteobacteria and Thaumarchaeota dominate the microbial communities in spatially and temporally
varying hydrothermal plume habitats.
An increasing number of recent observations appear
consistent with our conclusions based on thermodynamic estimates of bioavailable energy yields in lowtemperature mixing zones: (1) aerobic sulfur oxidation is
the most common and basic chemolithotrophic energy
metabolism in global deep-sea hydrothermal systems, (2)aerobic Fe2+ and Mn2+ oxidation are less abundant but
widespread metabolisms, and (3) aerobic methanotrophy
and ammonia oxidizer are dominant in SED systems,
respectively.

analyses, has indicated that even in H2-poor hydrothermal fluids in MOR-B settings, H2 oxidation-based primary production is highly attractive despite the low H2content (Perner et al. 2013b). This leads us to consider
that low-temperature diffusing flow is the product ofcomplex subseafloor processes (including seawaterhydrothermal fluid mixing, conductive cooling, various
redox reactions, and mineral precipitation), and thus,
the simple batch-mixing model employed in this study
may not be able to accurately reproduce all of theseprocesses.
Geochemical data sets for low-temperature diffusing
flows remain scarce. Thus, further quantitative estimatescombined with in situ or detailed chemical measurements will be needed to more accurately describe interactions among the physical and chemical processes,
bioavailable energy yields from chemolithotrophic metabolisms, and community development in diffusinghydrothermal fluids.

Diffusing hydrothermal fluids

Microbial communities in relatively low-temperature diffusing hydrothermal fluids have been investigated in awide variety of geographically diverse hydrothermal systems (Huber and Holden 2008; Huber et al. 2009; Perner
et al. 2011, 2013a, 2013b; Akerman et al. 2013; Campbell
et al. 2013). These are mainly planktonic free-living
communities under conditions in which the endmember fluids have already mixed with infiltrated seawater in relatively shallow subseafloor environments in
the recharge and discharge regions of hydrothermal
fluids (Bemis et al. 2012). In addition to planktonic freeliving populations, these microbial communities also
include detached epilithic and biofilm-forming components entrained by the fluid flows.
Hydrothermal fluids diffusing at the seafloor would be
expected to combine all growing, living, and dead populations and components within the entire subseafloor
fluid flow path in the discharge. This differs from microbial communities in hydrothermal plume habitats inwhich most microbial populations are indigenously growing from planktonic origins in deep-sea water (Lesniewski
et al. 2012). Thus, it is challenging to clearly understandthe relationships between the diversity and compositionof the observed microbial populations and hydrothermal fluid chemistry based on existing biological andgeochemical data for diffusing fluid habitats. However,
several studies have recently suggested the dominanceof sulfur oxidizers in typical MOR-B settings and thepresence of hydrogen oxidizers in MOR-U settings(Perner et al. 2011, 2013a; Akerman et al. 2013). These
results are generally consistent with our thermodynamic
predictions of relationships among microbial metabolisms and functions, hydrothermal fluid chemistry, andgeological background.
On the other hand, a very recent study producing
function-focused quantitative estimates, based on H2
and sulfide consumption and CO2 assimilation activities
as well as metagenomic 16S rRNA and functional geneChemosynthetic invertebrates

Chemolithotrophic symbionts hosted by deep-sea ventendemic chemosynthetic invertebrates represent important primary producers in global deep-sea hydrothermal
ecosystems. Their biomass production and functions
may be constrained by the energy states of the habitatsof both the symbionts and the host animals (Dubilier
et al. 2008), as productivity and energy metabolism in atight symbiotic association are strongly regulated by theinteraction of the symbiont with the physiology andecology of the host animal (Dubilier et al. 2008). There
have been numerous studies of the basic relationships
between the in situ physical and chemical conditions ofhabitats and the abundance and composition of energy
metabolisms in deep-sea hydrothermal chemosynthetic
symbioses (Beinart et al. 2012; Petersen et al. 2011;
Suzuki et al. 2006; Watsuji et al. 2010, 2014). However,
the energy conversion yield of the primary production ofchemolithotrophic symbionts is likely one of the mostimportant factors in the establishment of chemosynthetic symbioses, affecting the selection, acquisition, andbreeding of specific bacterial counterparts. In particular,
episymbioses and horizontally transmitted endosymbioses, in which symbionts are acquired from the proximal
environments of habitats in their larval and adult stages
in each generation, would be expected to be morestrongly affected by the energy states of chemolithotrophic symbiont metabolisms than vertically transmitted endosymbioses.
Recently, several studies have been conducted of therelationship between the activity of chemolithotrophic
symbionts and hydrothermal fluid chemistry, e.g., aseries of studies on epibiotic microbial communities in
the galatheid crab Shinkaia crosnieri in Okinawa TroughNakamura and Takai Progress in Earth and Planetary Science 2014, 1:5
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Page 18 of 24(Watsuji et al. 2010, 2012, 2014). The epibiotic microbialcommunities of S. crosnieri abdominal setae consist primarily of the sulfur-oxidizing Epsilonproteobacteria andGammaproteobacteria and methanotrophic Gammaproteobacteria (Watsuji et al. 2010, 2012, 2014). These results are generally consistent with the results of ourthermodynamic modeling, indicating high bioavailable
energy yields from both sulfur- and CH4-oxidizing reactions at low temperatures (high seawater mixing ratios)in the Okinawa Trough (Figure 8). The abundance of
epibiotic methanotrophic gammaproteobacterial populations and methanotrophic activity vary among the S.
crosnieri populations recovered from different hydrothermal fields (Iheya North and Hatoma Knoll fields)(Watsuji et al. 2010). As suggested by our model calculations, these variations are likely correlated with the insitu CH4 concentrations in the S. crosnieri colonies. Thismay, in turn, be associated with the CH4 concentrationsin the end-member hydrothermal fluids, although CH4
concentrations in the Hatoma fluids have not yet been
published.
Another notable example is the dual endosymbiotic(thiotrophic and methanotrophic) populations of ventmussels living in different geological settings of deep-sea
hydrothermal vent sites in the MAR and the Eastern
Pacific (Petersen et al. 2011). Based on thermodynamic
modeling of preferred H2-trophic energy metabolism,
genetic characterization of a key enzyme gene for H2trophic energy metabolism, and functional analyses of
H2 consumption and CO2 fixation of endosymbionts inBathymodiolus puteoserpentis in a typical MOR-U
hydrothermal system (Logatchev field), Peterson et al.
(2011) clearly demonstrated that the thiotrophic population in dual endosymbiosis of the Logatchev B. puteoserpentis use H2 and H2S comparably as energy sources forprimary production. This was the first reported example
of chemosynthetic symbiosis sustained by an inorganic
energy source (H2) other than H2S (reduced sulfur species) or CH4. In other words, this study first revealed
that compositional variations in H2, H2S, and CH4 in the
mixing zones of chemosynthetic macrofaunal habitats
affect the patterns and functions of episymbioses andendosymbioses in chemosynthetic microbial-faunal associations. Peterson et al. (2011) also showed that thethio- and H2-trophic endosymbionts hosted by different Bathymodiolus populations living in geographicallyand geologically distinct hydrothermal systems of the
MAR and Pacific (all H2-starved MOR-B hydrothermal
systems) had much lower specific H2 consumption activities than the endosymbiotic population from theH2-abundant MOR-U hydrothermal system (Logatchev
field). Although not fully quantitative, these results provide strong evidence that the metabolic activity of chemolithotrophic symbionts is controlled by hydrothermal fluid

chemistry and is related to the geological backgroundof the hydrothermal system, as suggested by our model
calculations.
Recently, metagenomic and metatranscriptomic approaches have also been used to study possible biogeochemical associations with Alviniconcha (deep-sea
hydrothermal-vent snail) holobionts (host/symbiont associations) that dwell in a broad region of the Eastern
Lau Spreading Center (ELSC) (Beinart et al. 2012; Sanders
et al. 2013). Different holobiont patterns have been foundin the Alviniconcha populations obtained from the mixing
zones of colonies in four different hydrothermal systems
in the ELSC. The endosymbionts were classified into threegroups: Sulfurimonas-type Epsilonproteobacteria, gamma1-type Gammaproteobacteria, and gamma-Lau-type Gammaproteobacteria (Beinart et al. 2012), all of which are
known to be typical sulfur (and H2) oxidizers. The Alviniconcha holobiont and endosymbiont distributions varied
from the northern to the southern region of the ELSC,
which have somewhat different geological settings (Beinart
et al. 2012). The ELSC has been well characterized from
north to south in terms of geological properties (such as
the spreading stage and rate, magmatic productivity, geochemistry, and host-rock geochemistry) (Tivey et al.
2012). Reflecting the change in geological setting, thechemical compositions of the end-member hydrothermal
fluids also change from relatively reduced and H2- andH2S-enriched (approximately 500 μM and approximately
5 mM, respectively) in the north to relatively oxidized andH2- and H2S-depleted (approximately 30 μM and approximately 3 mM, respectively) in the south (Beinart et al.
2012). The endosymbiont species shift from predominantly Sulfurimonas-type Epsilonproteobacteria in thenorth to predominantly gamma-1-type Gammaproteobacteria and finally to both types of Gammaproteobacteria inthe south (Beinart et al. 2012). Interestingly, the compositional abundance of both the endosymbiotic microbial
components and the expressed key gene transcripts forvarious energy metabolisms vary with the regional geochemical gradient (Sanders et al. 2013). Under relatively
reduced and H2- and H2S-enriched conditions, the compositional abundance of mRNAs related to H2- andsulfur-oxidizing metabolisms throughout the entire endosymbiont transcriptome is highly elevated (Sanders et al.
2013). The compositional abundances of the mRNAs ofthese energy metabolisms throughout the entire endosymbiont transcriptome are likely associated with the activitiesof these energy metabolisms in the endosymbiotic populations of the Alviniconcha host individuals.
Our geochemical modeling suggests that changes inthe H2S concentration from north to south in the ELSC
(approximately 5 mM to approximately 3 mM) should
not significantly affect sulfur-oxidizing metabolisms,
whereas H2-oxidizing metabolisms could be affected by

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the change in H2 concentration (approximately 500 μM
to approximately 30 μM) (Figure 6). Indeed, based on
differences in the expression of hydrogenases between
Epsilonproteobacteria and Gammaproteobacteria individuals, Sanders et al. (2013) suggested that H2 oxidation
may play a larger role in the energy metabolism of holobionts with Epsilonproteobacteria. Thus, the change in
H2 concentration, rather than the H2S concentration,
may account for differences in the holobiont patterns
found in the Alviniconcha populations in the ELSC. Although future studies are needed to elucidate the degree
to which Epsilonproteobacteria endosymbionts rely on
H2 for energy production, this may be additional evidence supporting the relationship between geologicalconstraints on hydrothermal fluid chemistry and thecompositions and functions of chemosynthetic microbial
symbionts in deep-sea hydrothermal environments.

hydrothermal fluid H2 concentrations, particularly in
MOR-U hydrothermal systems (Flores et al. 2011; Roussel
et al. 2011). Our geochemical model provides consistent
explanations for the results of these studies. Specifically,
the energy yields of anaerobic (and aerobic, in most cases)
H2-trophic reactions were well correlated with the H2concentrations of hydrothermal fluids (Figure 6). In
addition, thermophilic H2-trophic methanogens and sulfate/sulfur reducers are predominantly found in H2enriched deep-sea hydrothermal systems in the MOR-U
setting (Figure 8). It is thus very likely that serpentinizationdriven H2 enrichment in hydrothermal fluids is an
important geochemical factor that directly controls thethermodynamic energy potential, biomass, and productivity of H2-trophic chemolithotrophs.
Similar to the apparent relationship between H2 concentrations in hydrothermal fluids and the abundance ofH2-trophic chemolithotroph populations, our thermodynamic calculations also identified a possible relationshipbetween CH4 enrichment and the abundance of anaerobic methanotroph populations (particularly thermophilic
methanotrophic sulfate reducers) in SED hydrothermal
systems (Figure 8). In low-temperature habitats (e.g.,hydrothermal plumes, diffusing fluids, and chemosynthetic animal symbioses), many molecular signals andmetabolic activities of aerobic methanotrophy have been
observed. However, the existence of anaerobic thermophilic methanotrophic sulfate reducers has been inferred
only from lipid biomarker signals (Schouten et al. 2003).
Recently, thermophilic anoxic CH4-oxidizing SO4-reducing
activities have been directly verified at up to 70°C in
the sediments of the Guaymas Basin hydrothermal field(Holler et al. 2011). In addition, possible microbial components of thermophilic anaerobic methane oxidizers, consortia of ANME-1a Archaea and HotSeep-1 cluster
Deltaproteobacteria, have been identified via FISH analysis(Holler et al. 2011). Similar phylotypes of potentiallythermophilic ANME-1a Archaea have also been found inhydrothermal sediments and diffusing fluids of SED
hydrothermal systems such as the Axial Seamount andEndeavour Segment fields in the Juan de Fuca Ridge andthe Yonaguni Knoll IV field in the Okinawa Trough(Nunoura et al. 2010; Merkel et al. 2013). Because these
phylotypes of thermophilic anaerobic methanotrophic Archaea remain resistant to cultivation, quantitative cultivation methods are not feasible. However, other quantitativetechniques targeting 16S rRNA and functional gene transcripts together with direct metabolic activity measurements are now available (e.g., Beal et al. 2009; Watsuji
et al. 2012, 2014). Such quantitative estimates will provide
multiple lines of evidence for the relationship between
CH4 enrichment in SED hydrothermal systems and theabundance of thermophilic methanotrophic sulfate reducers in mixing zone habitats.

Chimney structures and sediments

The compositional and functional diversity of microbialcommunities has been most extensively explored in deepsea vent chimney structures that host high-temperaturehydrothermal fluid emissions (Nakagawa and Takai 2008;
Takai and Nakamura 2010, 2011; Takai et al. 2006b).
These microbial communities consist of typical epilithic(mineral surface-attached) and/or biofilm-forming populations and are sustained by the redox disequilibria formedin the chimney wall via diffusive mixing between the internal hydrothermal fluid and external seawater. Thus, theabundance and composition of chemolithotrophic energy
metabolisms in the chimney microbial communities are
directly controlled by the energy states of the chimney
habitats, resulting in good approximations by the thermodynamic calculations of the simple batch-mixing model.
Using data for both end-member hydrothermal fluids
and chimney microbial communities obtained from six
deep-sea hydrothermal systems with different geologicalsettings, Takai and Nakamura (2010, 2011) constructed
intra-field and inter-field comparisons between theabundance and composition of chemolithotrophic energy metabolisms predicted by thermodynamic modelingand the microbial community composition determinedthrough quantitative cultivation methods. Based on boththe thermodynamic modeling and microbiological characterization, statistically significant correlations between
the H2 concentration in the hydrothermal fluid or theestimated potential energy yield of H2-trophic methanogenesis and the cultivatable population size of hydrogenotrophic methanogens were found. More recently, in
addition to quantitative cultivation methods, statistical
phylotype compositional analyses of 16S rRNA andother functional genes have also been used to demonstrate significant correlations between H2-trophic chemolithotrophy in chimney microbial communities andNakamura and Takai Progress in Earth and Planetary Science 2014, 1:5
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Takai and Nakamura (2010) have also noted that phaseseparation has a considerable impact on intra-field variations in hydrothermal fluid chemistry. In microbiologicalstudies of the Iheya North field in the middle Okinawa
Trough and the Mariner field in the Lau Basin, increased populations of anaerobic and aerobic H2-trophic
chemolithotrophs (e.g., Methanococcales and Aquificales) were observed, potentially due to phase separationof hydrothermal fluids (Nakagawa et al. 2005b; Takai
et al. 2008). However, in studies of the Yonaguni Knoll
IV field in the Southern Okinawa Trough, H2-trophic(and thiotrophic) chemolithotrophs (e.g., Methanococcales, Desulfurococcales, Nautiliaceae, and Thioreductoraceae) were the dominant microbial components
in both vapor- and brine-rich hydrothermal fluids(Nunoura and Takai 2009). Although H2S concentration
data for the Yonaguni Knoll IV fluid have not yet beenreported, our geochemical model calculations indicatethat if the H2 concentrations of the end-member hydrothermal fluids were well below approximately 1 mmol/kg,
the metabolic energy available from both aerobic andanaerobic H2-trophic reactions would be directly correlated with the H2 concentration of the fluids (Figure 6).
The H2 concentrations in the vapor- and brine-richhydrothermal fluids venting at the Iheya North field(0.045 and 0.096 mmol/kg, respectively) and the Mariner
field (0.012 and 0.13 mmol/kg, respectively) are well below
approximately 1 mmol/kg and thus, phase separationinduced H2 variations may directly affect the available
energy yields from aerobic and anaerobic H2-trophic reactions. In contrast, the H2 concentrations in the fluids
at the Yonaguni Knoll IV field (0.8 to 3.6 mmol/kg) aremostly above approximately 1 mmol/kg, resulting insaturation of the metabolic energy available from aerobic hydrogenotrophic reactions, particularly at higher
temperatures (Figure 6). In addition, the bioavailable
energy yield from hyperthermophilic anaerobic reactions is nearly comparable to that from aerobic thiotrophic reactions, even in brine-rich hydrothermal
fluids (Figure 6). This may explain why there are no
major differences in abundance or composition of microbial communities between the vapor- and brine-richhydrothermal fluids in the Yonaguni Knoll IV field(Nunoura and Takai, 2009).

physical and chemical variations in hydrothermal fluids,
and compositional diversity of potentially bioavailable
energy for various vent-endemic chemolithotrophic metabolisms have been elucidated through thermodynamic
modeling of redox states in hydrothermal mixing zone
habitats. In addition, these relationships have been empirically substantiated by recent multidisciplinary biogeochemical and microbiological studies of existing
microbial communities and their metabolic functions in
representative deep-sea hydrothermal systems in different geographic locations and geological settings.
However, thermodynamic estimates of potential energy
for possible chemolithotrophic metabolisms are basedon certain simplifications, particularly with respect toquantitative representations of mixing of source hydrothermal fluids and seawater and the kinetic effects ofabiotic reactions, cellular uptake and excretion of energy
sources, and enzymatic functions on energy metabolism.
These shortcomings may result in differences between
the theoretical predictions and actual configurations andpatterns in some cases. To characterize the in situ physicaland chemical characteristics of hydrothermal mixing zone
habitats at high spatial and temporal resolution, several
electrochemical sensors have been developed and applied
to various habitats such as diffusing hydrothermal fluids
and chemosynthetic animal colonies. However, these sensors have some technical challenges, including multiple
chemical interferences, relatively narrow dynamic ranges,
and the need for in situ calibration (Luther et al. 2012). A
deep-sea in situ membrane inlet mass spectrometry(MIMS) method has also been developed and used for insitu measurement of volatile and time-sensitive chemical
species (Wankel et al. 2010). These newly developed insitu measurement tools will enable more precise estimatesof the energy states of habitats of chemolithotrophic microbial communities. Improvement and development ofbiogeochemical and microbiological characterization techniques are also necessary to understand the functionaland metabolic abundance and composition of microbialcommunities in deep-sea hydrothermal environments. It isa significant challenge to quantify the biomass, productivity, and functions of dominant microbial components indeep-sea vents. Comprehensive characterizations of in situ
mRNA assemblages using such tools as GeoChip technology (Wang et al. 2009) and the metatranscriptomic approach (Dahle et al. 2013) will likely prove more objective,
quantitative, and effective than employing elaborate quantitative cultivations using numerous media for intra-field
and inter-field comparisons of microbial communities andtheir functions. Successfully overcoming these challenges
is essential for clarifying the relationships between geology,
geochemistry, microbial energy metabolisms, and community development associated with global deep-sea
hydrothermal activities.

Conclusions
We have provided an overview of variations in the geology, geochemistry, microbial energy metabolisms, andcommunity development associated with global deep-sea
hydrothermal systems. Relationships among the geological backgrounds of hydrothermal activities (e.g., tectonic settings, basement rock geochemistry, abundanceof sediments, magmatic volatile inputs, and phase separation related to subseafloor hydrothermal processes),Nakamura and Takai Progress in Earth and Planetary Science 2014, 1:5
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Additional file
Additional file 1: Chemical compositions of end-memberhydrothermal fluids and seawater used in this study. Data are from89 hydrothermal vent sites in MOR-B, MOR-U, AMA-M, ABA-F, SED-MOR,
and SED-ABA settings.

Abbreviations
ABA: arc-backarc; ABA-F: felsic rock-hosted hydrothermal system in an
arc-backarc setting; ABA-M: mafic rock-hosted hydrothermal system in an
arc-backarc setting; MOR: mid-ocean ridge; MOR-B: basalt-hostedhydrothermal system in a mid-ocean ridge setting; MOR-U: ultramafic
rock-hosted hydrothermal system in a mid-ocean ridge setting;
SED: sediment-associated; SED-ABA: sediment-associated hydrothermal
system in an arc-backarc setting; SED-MOR: sediment-associatedhydrothermal system in a mid-ocean ridge setting.
Competing interests
The authors declare that they have no competing interests.
Authors’ contributions
Both KN and KT proposed the topic, conceived of and designed the study,
compiled and processed the data, and wrote the paper. Both authors readand approved the final manuscript.
Acknowledgements
We would like to thank the two anonymous reviewers for their constructive
and helpful comments, which have significantly improved the manuscript.
This research was financially supported by the Ministry of Education, Culture,
Science, and Technology (MEXT) of Japan through the special coordination
fund Project TAIGA: Trans-crustal Advection and In situ Biogeochemical
Processes of Global Subseafloor Aquifer.
Author details
1
Precambrian Ecosystem Laboratory (PEL), Japan Agency for Marine-Earth
Science and Technology (JAMSTEC), 2-15 Natsushima-cho, Yokosuka,
Kanagawa 237-0061, Japan. 2Current address: Department of Systems
Innovation, School of Engineering, The University of Tokyo, 7-3-1 Hongo,
Bunkyo-ku, Tokyo 113-8656, Japan. 3Subsurface Geobiology Advanced
Research (SUGAR) Project, Japan Agency for Marine-Earth Science andTechnology (JAMSTEC), 2-15 Natsushima-cho, Yokosuka, Kanagawa 237-0061,
Japan.
Received: 8 November 2013 Accepted: 15 March 2014
Published: 22 April 2014
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Cite this article as: Nakamura and Takai: Theoretical constraints ofphysical and chemical properties of hydrothermal fluids on variations inchemolithotrophic microbial communities in seafloor hydrothermal
systems. Progress in Earth and Planetary Science 2014 1:5.

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