Japan-China Symposium on Advances in Water and Sediment Research, July30-August1, 2012, Kyoto, JapanAN OVERVIEW OF MICROBIAL INTERACTIONS WITH
SEDIMENT DYNAMICS
Huiming ZHAO1*, Hongwei FANG2, Hajime NAKAGAWA3 and Hao ZHANG4
1Dr. of Eng., Postdoctor, State Key Laboratory of Hydro Science and Engineering, Dept. of Hydraulic Engineering ,Tsinghua University
2Dr. of Eng., Professor, State Key Laboratory of Hydro Science and Engineering, Dept. of Hydraulic Engineering ,Tsinghua University
3Dr. of Eng., Professor, Disaster Prevention Research Institute, Kyoto University
4Dr. of Eng., Assistant Professor, Disaster Prevention Research Institute, Kyoto University(Dept. of Hydraulic Engineering, Tsinghua University, Beijing 100084, China, E-mail:zhao-hm05@mails.tsinghua.edu.cn).

ABSTRACTIn aquatic environment, microorganisms such as bacteria and microalgae usually secrete a matrix of
mucilaginous extracellular polymeric substances (EPS) to form a “microbial biofilm” when they areassociated with solid surfaces (e.g., sediment particles, plant surfaces). Biofilms and the associatedmucilaginous secretions form a cohesive matrix surrounding sediment particles, modifying the sediment
properties, changing the sediment stability, and influencing the sediment dynamics. The purpose of thisoverview is to examine recent information concerning the roles of microbial interactions with sediment
dynamics. The microbial biofilm affects a number of changes on the physico-chemical and biologicalproperties of sediment. These range from the macro-scale stabilization of sediment to the micro-scale
bioflocculation of sediment particles. Also microbial biofilms are associated with considerable variability
in the properties of natural sediments. Sedimentological factors and biological factors interact in acomplex manner within the hydrodynamic regime both on a temporal as well as on a spatial scale.

Keywords: sediment; biofilm; biostabilization; biological and sedimentological factors; bioflocculation2008). The physico-chemical sediment properties,
such as bulk density, particle size, mineralogy andorganic carbon content, have become the main
considerations in most studies aiming to elucidate
the mechanisms governing the stability of cohesive
sediments (Jepsen et al., 1997; McNeil & Lick,
2004). However, sediment is not composed ofmineral particles alone. Great varieties of
microorganisms colonize the sediment and exert
influences on the sedimentary dynamics. The
microbiota that colonize the sediments come into
play, interacting with physical and chemicalparameters.
Whereastheinteractionofmicroorganisms with sediment dynamics has
become a main focus of many studies (Noffke N &Paterson D, 2008). In recent years, the importanceof biogenic influence on sediment dynamics,
especially by the mucilaginous matrix ofextracellular polymeric substances (EPS) producedby bacteria, microalgae and macrofauna, hasreceived a more and more increasing attention(Paterson, 1997; de Brouwer et al., 2000; Decho,
2000; de Deckere et al., 2001). Studies showed that
biological processes even seem to be the major

1. INTRODUCTION
Sedimentary systems are governed by a series ofdynamic processes such as erosion, transport,
deposition and deformation, which create numerous
sedimentary structures, including ripple marks ofdifferent morphologies and dimensions, current
laminations, ball and pillow structures, convolutebedding, bubble sand, and so on (Noffke N &Paterson D, 2008). Physical sediment dynamics,
usually accompanied by the associated release andrelocation of contaminants in aquatic environment,
is an important element that must be considered in
the plans development of modern integrated
management of rivers and coastal areas (Paterson etal., 2000; Foerstner et al., 2004). The possibility of
sediment erosion occurrence and the degree in termsof erosion rates and depth are determined by theinterplay of two kinds of forces imposed on
sediments with different effects, one is thehydrodynamic forcing (e.g. river flow, tidal flow,
density driven circulation and wind waves) and theother is the resisting forces (e.g. sediment cohesion,
gravity, biogenic stabilization) (Gerbersdorf et al.,93

impact factor of sediment cohesiveness in someintertidal areas (Black et al., 2002). Therefore, withrespect to the physico-chemical sediment properties,
many detailed field-studies have also been carriedout in order to evaluate and sometimes quantify theeffect of biological factors on sediment dynamics.
These studies have all shown that biological factors,
such as the microbial activities and their metabolic
products, may have a significant influence on thesediment dynamics. Sediment dynamics has beenwell-documented by microorganisms (Yallop et al.,
1994; Riethmüller et al., 2000) which secrete EPS
during their metabolic activities.

Biofilm exists in aquatic environments, especially
with
more
obviousperformanceinthe polluted waters. Biofilm not only plays animportant role on the absorption and degradation ofthepollutantsinwatersystem, butalso strongly changes
thecharacteristics
ofsediment particles, such as the morphology, bulk
density, water content, plasticity, mechanicalproperties, and so on. Because of the frequentexchange of materials, rich nutrients and severe life
events in the border zones of brackish/fresh waterand the junctions of land and sea, the effect of
biofilm in these areas is particularly significant. So
nowadays most related studies are focused on
marine-related systems and only a few on
freshwater systems. As the effect of biofilm on the
bed stability is mostly concentrated in the junctionsof land and sea or the estuary areas, the study object
is mainly fine sediment. It is generally believed that
why biofilm could strengthen the stability of bed
sediment especially the fine sediment, on one handis because the biofilm growth can form a relatively
smooth and stable surface, and on the other isbecause the EPS secreted by the microorganisms
can adhesion the sediment particles together. So theflow shear stress should overcome not only thecohesion between the particles but also the adhesive
force between the particles established by thebiofilm. Andersen (2001) examined the erodibilityof two microtidal mudflats and found that theseasonal variation of the erodibility at the two sites
is actually opposite to each other with higherodibility in the summer period at the site
dominated by macrofauna and low erodibility at thesite with a scarce macrofaunal population. Thisshows that complex interactions exist between
benthic diatoms (which stabilizes the surface) andmacrofauna (which often destabilizes the surface).
Such interactions will have to be further evaluatedand included in modeling tools when predictions of
the sediment dynamics at fine-grained deposits areneeded. Tolhurst (2008) investigated thedevelopment of a microphytobenthic biofilm andassociated changes in the sediment over 45 days andfound that biofilm developed rapidly and graduallyformed a multi-level structure with a certain
thickness. But there is also some researches (Stal,
2003) believe that the correlation between bed anti
erodibility and biofilm is not so significant. So there
are still controversies about the mechanism of bed
stability enhanced by the microbial biofilm, whichneeds further study. It is noteworthy that the water
environments of freshwater and seawater as well as
their biocoenosis are completely different. Therefore
the formed biofilms are unequal. The effect of
biofilm on the sediment particles in the marine

2. MICROBIAL BIOFILM IN AQUATICENVIRONMENT
When microorganisms such as bacteria andmicroalgae are associated with solid surfaces (e.g.,
sediment particles, plant surfaces), they secrete amatrix of mucilaginous extracellular polymeric
substances (EPS) to form a “microbial biofilm” (Fig.
1). EPS are the primary structuring agent for
microbial microenvironments, which control thephysical properties of biofilms. In aquatic
environment,
biofilm
andtheassociatedmucilaginous secretions form a cohesive matrix
surrounding the sediment particles and produce asignificant impact on the sediment dynamics, whichmake microbial biofilm become a focus studied
solely of its influence on sediment dynamics inrecent years.

Fig. 1 Conceptual diagram of a microbial biofilm within a solid
surface. The biofilm consists of microbial cells such as diatoms,
cyanobacteria, heterotrophic bacteria embedded within a matrix
of extracellular polymeric secretions (EPS) which closely
surround the solid.

94bioturbation (Rhoads et al., 1978). When coming to
the sediment stabilizing effect of biofilm, theadhesivemucilaginous
EPS
secretedbymicroorganisms is well understood. Some
researches demonstrated that EPS plays animportant role in the stabilization and deposition of
sediment. EPS probably exerts its effect by binding
sediment grains (Paterson, 1997; Wustman et al.,1998), decreasing drag (Paterson, 1999; Deckere etal., 2001), or by inclusion of particles in reinforced
EPS networks such as tube-like structures (deBrouwer et al., 2005). Therefore EPS would
increase the sediment stability, especially on thesurface of intertidal muddy sediments (Underwood& Paterson, 1993; Kornman et al., 1998) andenhance the deposition of sediment particles (deBrouwer et al., 2000; Herman et al., 2001). And
although frequent resuspension of intensively
bioturbated sediment by wind-driven waves andtidal currents may be resulted because
microorganisms change the characteristics andplacement of individual sediment particles as wellas the bulk characteristics and the boundary
properties of the sediment surface (Nowell &Jumars, 1984), the excretion of EPS especially by
microorganisms binds sediment particles thereby
reducing sediment resuspension (Grant et al., 1986;
Paterson, 1989). The growth of biofilms, referring tocells within a matrix of extracellular polymeric
substances secreted by microorganism, has beenshown to be important in mediating the properties ofand the processes in muddy sediments (Paterson,
1997; Black et al., 2002). The net effect of biofilm
growth is usually considered to be stabilising,
however, microorganisms such as diatoms candestabilise sediments (de Jonge&van der Bergs,
1987; Sutherland, 1998) and natural biofilms exhibit
a wide range of erosion thresholds (Defew et al.,2002). The stabilising effect of biota is usually
attributed to the secretion of EPS; however, recent
work indicates that the relationship may be more
complex, with the microorganisms themselves being
important in structuring or stabilising the EPS andsediment (de Brouwer et al., 2002; Tolhurst et al.,
2003; de Brouwer et al., 2005). On the other hand, a
lot of laboratory flume studies indicated that the net
effect of microorganisms appeared to bedestabilizing (Luckenbach, 1986; Grant & Daborn,1994). Result of the experiment in situ flume studies
at Skeffling mudflat in Humber estuary combinedwith laboratory studies showed an increasing
erodibility when bioturbation activity by Macoma
balthica increased (Widdows et al., 1998ab). Similar
results were found for Cerastoderma edule, but there
was also a positive correlation between the
Cerastoderma density and biodeposition. In someenvironment is different from that in the freshwater
system. It is generally believed that the
microorganisms in the water stick the sedimentparticles together through biofilm, inducing thechanges of sediment characteristics (Vignag, 2009).
Biofilm packs sediment, fills the gap between theparticles and provides more ion adsorption sites. It
is found that the critical drag force of surface
particles is related with the biomass and biofilm.
Under the biofilm influence, the critical drag force
fluctuated over time. Although the biofilm could
still enhance the particle stability with time after the
emergence of the largest critical drag forces, thedegree of enhancement declines. With the deep
study on various characteristics of biofilm, theknowledge of biofilm formation, composition,
structure and function has made considerable
progress. However, in many researches thealternative substrates are used to culture biofilm
under some specific conditions in the laboratory, so
the understanding about the role of biofilm in
the natural water environment and its effect on
sediment dynamics also subject to a certain degreeof restriction. In the study subjects, the researchof biofilm in water environment present a tendency
from that in sea water to that in fresh water. The key
research questions, including the difference of effecton biofilm between the seawater and freshwater
environment, the mechanism of biofilm on
the sediment dynamics,
etc., needtobefurther explored. Further study on biofilm would beof broad and important significance for thedevelopment of sediment dynamics.

3. EFFECT OF MICROORGANISMS ON
SEDIMENT STABILIZATION
Sediment stability is very important for cohesive
sediment dynamics. In the traditional study,
researchers
regardedthephysico-chemical
conditions as the most important drivers of sedimentstability. However, the sediment stabilization
mainly induced by biological activities, especiallythe influence of highly hydrated matrices of biofim,
has gradually been given an increasing attention in
the last decades. With an increasing amount ofreports of biological effects on erodibility offine-grained sediments, ‘biostabilization’ (Paterson,1994), which refers to the fixation of sediment by
the influence of microorganisms, has become afocus of many studies. Yet the effect of
microorganisms on sediment (de)stabilization iscomplex. On the whole, the influence can be
categorized
intotwogroups:thestabilization/deposition of sediment by binding andthe destabilization/erosion of sediment by95

Gerbersdorf et al., 2005, 2008). It has been wellknown that biological and sedimentologicalvariables sometimes show patterns of covariance (deBrouwer et al., 2003). Referred researches(Brouwer, 2000; Sabine et al., 2008) usually study
the mutual interrelations between biological activity
and physico-chemical properties from themacroscopic view, and nowadays most are limited
to field sampling, data extracting, and then building
the attachment of corresponding factors by somedirect correlation analysis. By using multiple
regression analysis researchers discovered that
sediment stability in their laboratory mesocosms
was best predicted by using a combination ofbiogeochemical properties of sediment particles,
including many biological and sedimentologicalfactors, such as bulk density, water content,
mineralogy, plasticity, cation exchange capacity, theconcentration of chlorophyll a, the concentration ofpheophytin, the concentration of colloidal
carbohydrate, and so on (de Brouwer et al., 2005;
Gerbersdorf et al., 2005; Tolhurst et al., 2008;
Gerbersdorf et al., 2008). The studies indicated that
sedimentological factors and biological factors
interact in a complex manner within thehydrodynamic regime both on a temporal as well as
on a spatial scale. Nowadays it is believed thatmicroorganisms and their metabolic activities wouldinteract with the sedimentological factors to
influence sediment dynamics. There are many
affecting ways, such as binding fine-grained
sediment, changing the water content, enhancing theorganic content through the secretion products, andso on. Furthert studies should be undertaken
addressing on both a biological and a physicalperspective, which could better assess the optimal
predictors of sediment stability and makecontribution on the risk assessment improvement ofcontaminated riverine sites along with a focus on
biofilm production and distribution.

cases, both stabilization and destabilization of thesediment by a single species was observed. For
instance, Gerdol and Hughes (1994) found that theamphipod
Corophium
volutator
causeddestabilization of the sediment bed due to grazingon microphytobenthos and reworking of thesediment by burrowing and tube formation. In
contrast, Mouritsen et al. (1998) attributed thestabilization of well-defined bed structures to thepresence of Corophium volutator. They suggested
that the coating of the walls of burrowing holes by
EPS was responsible for the observed stabilization(see also Meadows et al., 1990).

4. INTERPLAY BETWEEN BIOLOGICALAND SEDIMENTOLOGICAL FACTORS
There are many key-parameters for the transportof cohesive sediment, including the critical bed
shear stress for erosion (the erosion threshold), theerosion rate, the settling velocity of the material, andso on (Andersen, 2005). These parameters mainly
depend on the physical and chemical characteristicsof the sediment, such as water content, bulk density,
mineralogy, plasticity, salinity, and the adsorption
and cation exchange capacity (de Deckere et al.,2001). None of these parameters could easily be
predicted based on the distributions of grain sizes,
both due to the cohesive nature of the sediment andthe generally strong biological interaction in theimportant processes (Widdows and Brinsley, 2002).
The physical and chemical characteristics of thesediment are modified by the microbial activities(Paterson et al., 1999). Researchers (Yallop et al.,
2000; de Brouwer et al., 2005) found that sedimentstability correlated with a range of biologicalvariables, including the concentration of chlorophylla, the extracellular carbohydrate and EPS fractions,water content, bacterial biomass, and so on. Overthe last decades, biological factors of sedimentstabilisation have been given increasing attention in
many studies. Meanwhile microbial biofilms are
believed to be associated with considerable
variability in the properties of natural sediments.
EPS binding capacity is clearly affected not only by
the local physico-chemical environment, but also by
the characteristics of sediments in aquatic systems(Shin et al., 2001). Many biological factors, such as
the taxonomic composition of benthic communities,
their physiological state and bacterial action, which
in turn depend on the abiotic conditions, would
exert significant influence on the biofilm nature (deBrouwer & Stal, 2001). Therefore, some studies
have addressed the reciprocal influence of biology
and sedimentology, especially with regard to
sediment stabilization (de Brouwer et al., 2000;

5. BIOLOGICAL FLOCCULATION OF
SUSPENDED PARTICLES
Sediment flocculation is a critical component for
the understanding of cohesive sediment dynamics. It
is a non-negligible phenomenon in nature, which
has been paid much attention in many fields(Rojas-Reyna et al., 2010; Son and Hsu 2011). Fromthe macroscopic view, it is classified into the twoclassesoforganic-flocculation
andinorganic-flocculation.
Biological-flocculation
couldberegarded
as
one
form
of
organic-flocculation. Traditionally, the referredstudy has largely been devoted to the
inorganic-flocculation. However, over the last96

biofilm and appeared to be of complicated physicalfloc structures. The EPS was found to embedparticles and permeate the void space, representing
the dominant physical bridging mechanism of theflocs and contributed to the extensive surface area,architecture
characteristics
andmechanicalproperties of bioflocculation sediment (Steven N.
Liss, 1996; Huiming Zhao, 2011). But nowadays
most referred conclusions are qualitative
illustrations. Mechanistic models to describe theinteraction between mineral particles andmicroorganisms are an instrumental aid tointerpreting biofloccultion sediment dynamics. Yet,
nowadays little work (Federico Maggi, 2009)
explicitly coupled mineral and biomass dynamics at
length scales comparable to the floc size, thus
leaving a serious gap in our understanding of the
feedback
betweenmineralparticles
andmicroorganisms.
Coupling
mineralandmicroorganism dynamics represents therefore thebest target to understand the implication and fate ofbiomass-affectedsuspended
sediment
that
commonly occur in natural conditions.

decades, the bioflocculation of sediment by
biological activity has been given increasing
attention. Bioflocculation is different fromconventional inorganic-flocculation, in whichmicroorganisms plays a key role. As a livingorganism, it has a great difference with the generalinert material because of the association of life
activities. There have been many mechanisms ofbioflocculation, such as charge-neutralization
theory, capsula theory, cellulose fibrils outside thecell theory, EPS bridging theory, and so on (Smithet al,. 1992). Nowadays the most generally accepted
theory is EPS bridging theory, which believes thatthe material basis of bioflocculation is EPS and EPS
acts in the manner of “bridge” on the particle
surfaces resulting in the generation of flocculation.
The process of biological flocculation alters thehydrodynamic characteristics of sediment bychanging the density, porosity, settling velocity andsurface area of flocs (Droppo, 2001). Natural
bioflocculation sediment comprises many different
substances with concentrations that are generallysite specific and time varying. Although an accurate
taxonomy is currently lacking, the biological-flocsof sediment can generally be divided by inorganicand organic fractions. The inorganic fraction mainly
consists of various fine cohesive minerals, such as
kaolinite, illite, montmorillonite, carbonate, and soon (Van Leussen, 1994; McAnally, 1999). The
organic fraction is prevalently made of numerous
microorganisms, their metabolic products (EPS),
and residuals from dead organisms (Crump andBaross, 2000; Simon et al., 2002; Bhaskar et al.,2005). These two fractions are intimately related byphysical, chemical and biological processes, making
the biological-flocs of sediment a complex, reactive
biomaterial distributed in the aquatic environment.
Flocculation of biological forms aggregates that
increase in size by collecting suspended sediment,
organic particles, and microorganisms (Federico
Maggi, 2009). There is a general consensus that theinteraction between suspended sediment particles
and microorganisms may exert manifold impacts on
chemical and mechanical floc responses.
Experiments in controlled conditions and fieldobservations have given evidence that the organic
matter (especially the EPS) had substantial effects
on flocculation time, floc size, density, and settling
velocity (Guenther and Bozelli, 2004; Passow and
De La Rocha, 2006; Bowers et al., 2007).
Furthermore, it is generally accepted that EPS
increase the aggregation efficiency (Kiorboe et al.,1990), while relatively little is known about theeffect on floc breakup (Alldredge et al., 1990).
Researches have demonstrated that bioflocculation
sediment was composed of complex networks of

6. SUMMARY
Microbial factors play critical roles in thesediment dynamics. Many of the geochemical andbiological processes which are mediated by
microorganisms as well as their secretions biofilm
occur in a complex manner within thehydrodynamic regime. The microbial biofilm
represents an important element for consideration
during the investigation and the interpretation of
biological, chemical, and sedimentological data inaquatic systems. While the biofilm is a common
microbial adaptation in aquatic systems, thecomplexity of biofilms and the resulting effects on
sediment dynamics are still not well understood.
Nowadays most relevant researches are qualitative
illustrations, as not much work has been done on thequantitative researches and mathematical modelingof influence from biofilm on sediment dynamics.
Researchers are yet to carry out much intensive
theoretical studies of influence of biofilm on
physico-chemical properties of sediments withspecial focus on sediment dynamics.
ACKNOWLEDGMENT: This investigation was
supported by the National Science Foundation ofChina No. 51109113 and No. 50909095, thePostdoctor Science Foundation of China No.
20110490413 and the JSPS Asia-Africa Science
Platform Program, MEXT, Japan.

97

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