Journal of Nuclear and Radiochemical Sciences, Vol. 6, No. 1, pp. 11-15, 2005

Accepted
Microorganisms and Their Influence on Radionuclide Migration in Igneous RockEnvironments
Karsten Pedersen*
Göteborg University, Department of Cell and Molecular Biology, Microbiology, Box 462, 405 30 Göteborg, Sweden
Received: November 15, 2004; In Final Form: November 15, 2004
Microorganisms interact with their surroundings and in some cases they greatly modify the characteristics of theirenvironment. Several such interactions may have a significant influence on the behaviour of radionuclides
possibly escaping from underground radioactive waste repositories. Microbes can mobilise trace elements.
Unattached microbes may act as large colloids, transporting radionuclides on their cell surfaces with the groundwater flow. Many microbes produce ligands that can mobilise trace elements from solid phases and that caninhibit trace element sorption to solid phases. Bacterial species from the deep subsurface have demonstrated asignificant effect on the mobilization of 59Fe(III), 147Pm(III), 234Th(IV) and 241Am(III) under varying redox conditions. The extent of bacterial immobilisation of radionuclides has been investigated under in situ conditions.
Experiments have demonstrated this effect with 60Co, 147Pm, 234Th, 237Np, and 232U. A large group of microbes
catalyse the formation of iron oxides from dissolved ferrous iron in groundwater that reaches an oxidising environment. Such biological iron oxide systems (BIOS) will have a retardation effect on many radionuclides.
Microorganisms execute an important influence on the chemical situation in groundwater. Especially, they may
catalyse reactions that stabilise the redox potential in groundwater at a low and, therefore, beneficial level for aradioactive waste repository.

every single, constructive combination of those laws formaking a good living of all or almost nothing.

1. Introduction
A microbe is an organism that has all it needs for a complete
life cycle in one single cell. Many microbial species may
under appropriate circumstances form multi-cellular structures,
sometimes with morphological and metabolic differentiations
between the different cells making up a bio-structure. Growthby cell division is the most common way of microbe propagation. The microbes outnumber multi-cellular organisms on ourplanet. They are characterised by their almost infinite ability
to bio-degrade and bio-synthesize naturally occurring
compounds in the environment. Microbial reactions control,
partly or fully, the chemical composition of many, very
different environments such as sediments, soils, lakes andgroundwater. They also have the ability to adapt to extreme
environments such as alkaline and acidic groundwater.1, 2
Microbes occur either as unattached, planktonic cells
passively floating or actively swimming in the free waterphase, or are attached to solid surfaces. Any solid surface,living or dead, immersed in a water phase with living microbes
is predestined to develop biofilms i.e. films of life that cover
the surface. Microbes from the water phase become attachedto the surface and, if growth conditions are appropriate, they
start to grow and divide, in an attached mode.
All microbial life is based on metabolic processes driven bychemical energy extracted from the oxidation of inorganic ororganic compounds. The oxidative harvesting of energy
requires an electron acceptor that is concomitantly reduced.
This process is called respiration when a reducible external
electron acceptor is used (e.g. oxygen, nitrogen, sulphur, ironor manganese), and fermentation when the electrons are shuffled around between the degradation products of the original
energy source (e.g. sugar to alcohol and carbon dioxide). The
microbes certainly must obey the laws of thermodynamics, butthey are utterly sophisticated lawyers that understand to use*Corresponding author. E-mail: karsten.pedersen@gmm.gu.se.
FAX: +46-31-773-2578.

2. Microbial Processes and Radionuclides
Microbial processes can significantly alter the mobility ofradionuclides in the environment. Multi-disciplinary researchcombining microbial physiology, ecology and molecularbiology with nuclear chemistry, geochemistry and geology
plays an important role in the exploration of the processes
described in this paper.
Figure 1 summarises microbial processes that can influence
radionuclide speciation and thereby their migration behaviour.
Microbial processes will act immobilising or mobilising,depending on the type of process and the state of the microbes.
Microbes in biofilms will, with exception for those who
produce complexing agents, be immobilising. Planktonic
cells, that bio-sorb or bio-accumulate radionuclides, will act
mobilising on radionuclides. The processes can have a direct
or indirect action on radionuclide transport in the geosphere.
A direct action involves contact between a microbe and the
Accumulation

Red-ox-reactions

Sorption

Mobilisation

Complexing
agentsSorption

Immobilisation

Red-ox-reactions

Transformation

Accumulation

Mineralisation

Figure 1. Schematic view over how microorganisms interact with
their surroundings and how they may influence the behaviour ofradionuclides possibly escaping from underground radioactive waste
repositories.

© 2005 The Japan Society of Nuclear and Radiochemical Sciences
Published on Web 07/31/2005

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J. Nucl. Radiochem. Sci., Vol. 6, No. 1, 2005

Pedersenradionuclide with a resulting change in its speciation. Indirect
action is caused by changes in the environment generated by
microbial metabolism, which in turn influences radionuclide
behaviour. Finally, all microbial processes except bio-sorption
require an active, energy driven metabolism. The modelling of
microbial processes, therefore, must include a proper understanding of microbial energy turnover rates in deep rockaquifers. The processes in Figure 1 are discussed in somedetail below, with emphasis on their importance for understanding geosphere retention phenomena in the safety assessments of radioactive waste disposal. Table 1 outlines some
important features of the discussed processes.
TABLE 1: Microbial Processes Can Influence Retention ofRadionuclides Directly or Indirectly in Several Different
Ways
Microbial
processes that
influence
radionuclide
migration

Microbes in thisprocess are in
the following
state(s):This action ofthis microbial
process onradionuclides
is:planktonic biofilm direct Indirect

Immobilisation processes
Bio-sorption
Bio-accumulation
Bio-transformation
×
Bio-mineralisation
×Metabolic red-ox×reactions
Mobilisation processes
Bio-sorption
Bio-accumulation
Production ofcomplexing agents

×
×
×

×
×
×
×
×

×

×
×
×

×

×
×

×
×
×

This process
requires anactive microbial
energy driven
metabolism:
yes
no

×
×
×
×

×
×
×

The most important variables for such processes are the state of attachment,
are the microbes attached or unattached, and whether the microbes are activewith a metabolism that turns over energy, or dormant and inactive.

3. Bio-Sorption
The term bio-sorption is used to describe the metabolismindependent sorption of heavy metals and radionuclides tobiomass, i.e. microbial cells. Bio-sorption can be summarized
as the sorption and accumulation of trace elements to thesurface of microbial cells. Both living and dead biomass arecapable of bio-sorption and ligands involved in metal binding
include carboxyl, amine, hydroxyl, phosphate and sulfhydryl
reactive groups on the cell wall.3
Microbes have the largest surface area to volume ratio of
any independent life form due to their extremely small size,
typically centring around 1 µm3. Fitting of experimental datato Langmuir sorption isotherms gives information on the sorption capacity of microbes that can be cultured on the laboratory. Values for equilibrium sorption constants and sorption
capacity have been established for the two major types ofbacterial cells, those with Gram-positive and Gram-negativecell walls.4 Distribution ratios at varying pH, cell number andconcentration of the lanthanide Promethium have also been
determined.5
The typical volume of a groundwater bacterium is in therange of a part of 1 µm3 up to a couple of µm3. Numbers ofplanktonic microbes in deep groundwater vary in the range of
106 to 109 cells L−1 of groundwater.6−8 Bio-sorbing planktonic
microbes can be regarded as large colloidal particles and aredealt with elsewhere in this paper. However, microbes inbiofilms are different. They have been reported to reach 1011
cells m2 in Fennoscandian shield rock groundwater.7, 8 Biofilm
microorganisms commonly excrete extra-cellular material
supporting attachment and also the three dimensional shape ofa growing biofilm. As this extra-cellular material is organic in
its nature, it will add a bio-sorption capacity to the cell’ssurfaces. In conclusion, bio-sorption to planktonic microbes
will act mobilising on radionuclides, while bio-sorption tobiofilms will act immobilising (Table 1).
Host rocks surrounding hydraulically conductive fractures
are considered important barriers to the migration of radionuclides in the far-field. Fluid-rock interfaces can be isolated
from one another by the growth of microbial biofilms. In an
ongoing study of the adsorptive capacity of in situ anaerobic
biofilms grown 500 m underground in ‘repository’ conditions
was compared to the capacity of host granite from the sameenvironment. Surfaces were exposed to 60Co(II), 234Th(IV),237
Np(V), 147Pm(III), and U(VI) over the period of 6 weeks in a
pH neutral anaerobic synthetic groundwater. Adsorption wasinvestigated using radioactive tracers and autoradiography.
Results indicate that the trivalent elements did attach better
than the other tested elements. Anaerobic biofilms and rocksurfaces were found to share similar adsorption capacities but
probably have dissimilar complex stability due to the surfacefunctional groups available and competition for those groups.
The high ionic strength of the groundwater and the chemical
properties of the radionuclide species used potentially reduced
the effectiveness of biofilm surfaces as a sorbant. The effectof fracture biofilm coverage on radionuclide adsorption andmigration in subsurface environments cannot be ignored.
Potential suppression of adsorption by biofilms should be
accounted for in performance safety assessment models.
4. Bio-Accumulation
Metals catalyse many metabolic reactions in the microbial
cell. Microbes, therefore, have evolved energy dependent
uptake systems for physiologically important metals. The
import mechanisms of metals and other elements into the cells
relate to size and charge of the element in focus. For example,
the close similarity of the Cs+ and K+ cations dictates that thebroad-specificity alkali metal uptake transporters take up boththose cations in all microbial groups. The specific mechanisms by which Cs + is transported into the cell have beenreviewed by Lloyd and Macaskie.9
As concluded for bio-sorption, bio-accumulation will have avery different effect on radionuclide retention in planktonic
versus biofilm microbes (Table 1). In the planktonic state, themicrobe can be regards as a large, living colloid, while thebiofilm microbes relate to solid phase retention models. Althoughsome microbes may alter between unattached and attachedmodes, many may become trapped and fossilised over time.10
As bio-accumulation is a process that requires energy, it can be
expected that this process is biased towards biofilm microbes,
because microbial biofilm populations have been found much
more metabolically active relative to planktonic microbes.7
Up to date, in situ experimental data does not exist on theimportance of bio-accumulation processes for understanding
geosphere retention phenomena in the safety assessments ofradioactive waste disposal. The potential of this process islinked to metabolism, and therefore also to the availability ofsources of energy for microbial metabolic reactions in deep
groundwater, further discussed below.
5. Metabolic Red-Ox Reactions
Microbial energy metabolism requires a reduced electron
and energy donor and an oxidised electron acceptor (Table 2).
The energy donor can be an organic or an inorganic
compound. The electron acceptor is generally an inorganic
compound, with exception for fermentation, where the electron
donor and electron acceptor is the same organic compound.
Electron donors and acceptors can be combined in redox

Microorganisms and Their Influence on Radionuclide Migration

TABLE 2: The Most Common Energy and Electron Donors
and Electron Acceptors in Microbial Metabolism
Organic energy sourcesand electron donors

Inorganic energy
sources and electron
donorsElectron acceptors

Reduced

Reduced Oxidised

Oxidised

Reduced

Oxidised

Carbohydrates

CO2

O2

H2O

Amino acids

CO2

NH4+

NO3

NO3

N2

Organic acids

CO2

Mn2+

Mn4+

Mn4+

Mn2+

CO2

2+

3+

3+

Fe2+

Fat

Fe

Fe

2−

Fe

2−

H2S

SO4

SO4

H2S

CH4

CO2

S0

H2S

6+

CO

CO2

U

U4+

H2

H2O

CO2

CH4

The respective atom that donates or accepts one or several electrons is underlined.

couples according to the difference in free energy. Any redox
couple that releases energy via a reaction is a possible sourceof energy for microbes. The result from microbial harvestingof energy from redox couples is an oxidised donor and areduced acceptor. Important to notice here is that microbial
metabolism generally lowers the redox potential in the environment. Further, some of the reduced electron acceptors (e.g.
sulphide), may result in bio-mineralization processes, as
discussed next.
A case of special importance is the reduction of oxygen in
microbial metabolism. Oxygen is the preferred electron
acceptor by many microorganisms, because the free energy
available in oxidation of an electron/energy donor is largest
when oxygen is used, compared to other acceptors (Table 2).
A first indication that microbial oxygen reduction may be of
considerable proportions in granitic environments was
published after a series of full scale oxygen intrusion experiments into a 70 m deep vertical fracture zone at the Äspö Hard
Rock Laboratory (HRL), Sweden. 11 Later, the MichaelesMenten kinetics was successfully used to model oxygen reduction during a series of field (also at Äspö HRL) and replica
laboratory experiments in a detailed scale called REX aiming
at the study of O2 depletion in granitic media.12 This model
describes the effect of the initial oxygen concentration on theoxygen reduction rate. Over a wide range of O2 concentrations
tested in situ, the variation of (v) with respect to [O2] followed
the empirical Monod equation (Michaelis-Menten kinetic used
for microbial growth):v = Vmax[O2 ]Km0 + [O2 ]where v is O2 reduction velocity at a specific O2 concentration,
Vmax is the maximum rate when the organism is O2 saturated
and Km0 is the O2 concentration when the O2 reduction rate is
1/2 of the maximum. This model was further developed andadapted to experimental data during the REX-project.12, 13
The most important conclusions from the REX experiments
were:12• Microbes play a substantial role in O2 reduction in granitic
media, and microbial processes implicate a significant
added reducing capacity in a repository environment.
• When a surface water containing O 2 encounters the“stationary” groundwater system at depth, there is an
important increase in microbiological activities, resulting
in O2 depletion, transformation of organic material to CO2
and formation of biofilms.
• The time scale for microbial oxygen reduction to noughtin typical fractures was estimated to be in the order of afew days.

J. Nucl. Radiochem. Sci., Vol. 6, No. 1, 2005

13

6. Bio-Mineralisation
Radionuclides can precipitate with microbially generated
ligands, e.g. phosphate, sulphide or carbonate. The concentration of free radionuclide (metals) at equilibrium is governed by
the solubility product of the metal complex (typically 10−20 to10−30). Most of the metal or radionuclide should therefore be
removed from solution if an excess of ligand is supplied.
Phosphate concentration in deep groundwater is very low, andthis compound is an indispensable and central metabolicenergy transport entity. Therefore, it is not likely thatmicrobes excrete phosphate to the environment. Sulphide is
the respiration waste product from sulphate reduction, and iscommonly found in deep groundwater. With exception forvolcanic and hydrothermal areas, it can be safely assumed that
dissolved sulphide to a large part is the result of microbialsulphate reduction. Sulphate reducers have been demonstrated
common in Fennoscandian groundwater,7 which support theassumption that sulphate reduction is an important retention
factor for radionuclides prone to form solid sulphidecompounds. Microbial metabolism results in the production ofcarbon dioxide from degradation of organic carbon. Locally,such production may give rise to carbonate precipitates, e.g.
calcite, with a concomitant co-precipitation of radionuclides.14
Organic surfaces and iron oxides have been identified asimportant factors in radionuclide transport modelling. Several
microorganisms oxidise ferrous iron to ferric iron resulting in a
mix of organic material (microbes) and iron oxides, here
denoted BIOS (Biological Iron Oxides). Such biological ironoxide will have a retardation effect on many radionuclides.
Typically, the microbes form stalks and sheaths that increase
the volume of the iron oxides from densely packed inorganicoxides to a fluffy rust-like material with water contents of up
to 99% or more. The microbes contribute to the exposure of alarge oxide area to trace elements flowing by and the organic
biological material adds a strong retention capacity in addition
to iron oxides. BIOS can be found everywhere along the ÄspöHRL tunnel system. This BIOS is mainly produced by the
stalk-forming bacterium Gallionella ferruginea.15, 16 BIOS
from different sites and with varying age were analysed for thecontent of rare earth elements (REE).17 The results showedthat the REE concentration analysed in the inflow and outflow
of the experimental artificial ditches were more than 1000
times lower compared to a chondrite standard. Ten to twelve
weeks old BIOS that had developed in artificial ditches attunnel length 2200 m adsorbed three orders of magnitude more
REE compared to the groundwater. Very old BIOS (4 – 6
years), collected at 1127B m tunnel length had a REE concentration that were about one million times higher compared to thegroundwater and 10 to 100 times higher than what is found in
typical Äspö/Ävrö rock material. The obtained data clearly
demonstrates the excellent REE sorption capacity of BIOS, asfirst suggested by Ferris et al.18, 19
Microbial BIOS and carbonate mineralization processes will
have the largest retention impact on radionuclides at sites
where there is an outflow of anoxic groundwater to an aerobic
environment. This is because the gradients formed when theanoxic groundwater is oxygenised offer an excellent environment for microbial proliferation resulting in development of
BIOS and carbonates that co-precipitate and sorb radionuclides. In opposite, sulphide bio-mineralization will occur
along the transport routes up to the ground surface.
7. Bio-Transformation
Microbes can catalyse the direct transformation of someradionuclides to less soluble forms via metabolic processes.
The most studied process is how sulphate and iron reducing
bacteria can use U6+ as a surrogate for sulphate20 and Fe3+, 21

14Pedersen

J. Nucl. Radiochem. Sci., Vol. 6, No. 1, 2005

respectively, as electron acceptors (Table 2). It is not known if
this process is of significant importance for the safety inradioactive waste. The concentrations of SO42− and solid Fe3+phases in most repository environments will be much higher
than that of possibly occurring U6+. Therefore, bio-transformation of radionuclides escaping from a waste repository may not
be significant, but this remains to be demonstrated under insitu conditions.
8. Production of Chelating Compounds
Microbes need metals for their metabolism, just as all multicellular living organisms. Such metals are often available onlyin small quantities or, as in the case of iron in surface waters,
are not bio-available at all due to low solubility under aerobic
conditions. Therefore microbes produce various kinds ofchelating compounds to increase the bioavailability of essential
elements, needed for metabolism. These ligands are notalways highly specific, and several of them will also mobilize
other elements such as heavy metals and radionuclides. In theprocess of capturing the metal-ligand complex, microbes sort
toxic metals from essential ones and expel the toxic elementsback to the environment. The potential for mobilization ofradionuclides from repository environments by bacterially
produced ligands is unknown and, therefore, a concerning
possibility in the safety analysis that should be explored.
In a first study, the action of the chelating compounds introduced above on solid phase material was investigated.22 Threebacterial species (Shewanella putrefaciens, Pseudomonas fluorescens and Pseudomonas stutzeri), isolated from the deep
subsurface and a uranium mine shale material for the former
uranium mine Ranstad was chosen for this study. The three
species were incubated in a chemically defined medium
supplemented with tailings material that had been exposed tonatural weathering conditions for 30 years having a content of
0.0013% U by weight. Non-leached uranium ore (0.61% U byweight) from the same area were also incubated. Pseudomonas
fluorescens, managed to mobilize 0.001 – 0.005% of uranium
from the two ores. This release of U was attributed to the
production of species specific pyoverdine chelators, as U could
not be detected in either sterile controls or in the experimentswith the other two bacteria. P. fluorescens also doubles the Crconcentration in solution as compared to the sterile controls
whereas P. stutzeri and S. putrefaciens result in a 5 − 6 foldincrease in Cr concentration. The difference in leaching behaviour between the bacteria used in this study is likely to be
explained by the production of different chelators, found to befour using HPLC, as described below.
If ligands are produced in a repository environment, it is
crucial to study whether the postulated rock-retardation mechanism of released radionuclides can be impaired by microbial
ligands. Three bacterial species (Shewanella putrefaciens,
Pseudomonas fluorescens, and Pseudomonas stutzeri), isolated
from the deep subsurface, and four radionuclides ( 59Fe(III),
147
Pm(III), 234Th(IV), and 241Am(III)) were selected for a laboratory study.23 The microbes were cultured in the laboratory,
separated from dissolved compounds that were produced by
the microbes and expelled into solution. The separation was
performed by centrifugation, and the supernatants werecollected. The supernatants were mixed with radionuclide andsolid phase (TiO2 or SiO2). The pH ranged between 7.5 – 9.0.
This is an interval, within which all investigated radionuclides
should adsorb to the added solid mineral phase, provided thesystem is free from ligands. All three bacterial species
produced ligands that were able to complex the radionuclides atvarious degrees in competition with the solid phase (Figure 2).
Further investigations were accomplished to identify thecomplexing agents that caused the obtained mobilization.23
High performance liquid chromatography (HPLC) was used to

Figure 2. Mobilisation of radionuclides by three different mixes ofdissolved compounds that were produced by the microbes andexpelled into solution, and two known chelating compounds(Hydroxamate and Catechol) in competition with solid phase SiO2 ataround neutral pH. Bars are, from left to right: Pseudomonas fluorescens (pH 8.9); Pseudomonas stutzeri (Ph 7.6); Shewanella putrefaciens (pH 7.3); Hydroxamate (pH 6.1); Catechol (pH 6.2; Culturing
medium (pH 8.4).

separate substances in the microbial supernatant for further
characterization. Prior to injection into the HPLC the bacterial
supernatants were purified and mixed with 59FeCl3. The eluate
was measured with UV- (435 nm) and scintillation detector inseries. The 59 Fe identified the retention times for metal
complexed substances, which had correlating peaks in the UVchromatogram. Four Fe-complexing substances were detectedin the supernatant from the P. fluorescens culture. The resultsof HPLC analysis with P. stutzeri and S. putrefaciens showed
two peaks and one peak respectively. All substances eluted
from the column varied in retention times, indicating that the
microbes studied produced several metabolites that havedifferent chelating abilities. Detailed identification of thoseand other complexing agents will facilitate the search for presence or absence of identified complexing agents in natural
repository environments.
The possible production of chelating compounds in deep
repository environments is unknown. Therefore, investigations are being launched during 2005 at the MICROBE site
450 m underground at Äspö HRL, Sweden. 24 Microbial
biofilms and planktonic microbes will be grown under anaerobic and reduced in situ conditions, including pressure,temperature, geochemistry and flow rate. Their possible
production of chelating agents will be investigated on solid anddissolved phases of selected radionuclides.
9. Research Needs
The literature on the microbial processes described here isextensive for laboratory research, but sparse when it comes toin situ experiments, performed under repository conditions.
Microbial processes are controlled by many different factors,of which several are extremely difficult to mimic in the laboratory. Physical parameters such as the high pressure, thecomposition of gases and the carbonate system, environmental
conditions such as anaerobic and reduced systems, and finally,
complex ecosystems with multi-species consortia are all very
difficult to reproduce in the laboratory. There is a need for insitu experimental conditions and those can be achieved inunderground laboratories. The MICROBE laboratory at the
450 m level in the Äspö HRL, Sweden fulfils most of therequirements for in situ investigations. 24 Several researchMicroorganisms and Their Influence on Radionuclide Migration

projects about microbial processes under in situ conditions areunder way at MICROBE.
10. Assessments in Radioactive Waste Disposal
Microbial processes are generally not included in various
performance assessments of radioactive waste disposal in aquantitative sense, in comparison with how, for example,
colloids, sorption and geochemistry are treated. Microbial
processes do in general add “new” concepts. Life processes
obey the rules of chemistry, thermodynamics, and movement
just as any process. The difference is that microbial processes
add a metabolic, and therefore, catalytic dimension that iscomplicated to predict and sometimes difficult to understand.
Modelling life processes is consequently more difficult thanmodelling most non-life processes due to the multi-component
nature of the former.
Microbial processes should not be ignored in. Two processes
are judged particularly important (Table 3). 1) Microbial production of chelating compounds in the repository environment; and2) the scavenging of intruding oxygen should be considered.
Oxygen reduction was for a long time expected to be solely an
inorganic process. New results, reviewed in this paper, haveindicated the opposite to be true. Microbial processes will thus
be an additional important oxygen scavenging process in repository environments.
TABLE 3: The Importance of Microbial Processes in the
Safety Analysis of Radioactive Waste Disposal Can be
Ranked According to its Assumed Effect, and the Current
Knowledge about the Process
Microbial processes that
may influence radionuclide
migration

Relative level of current
knowledge of in situ
processes
highImmobilisation processes
Bio-sorption
Bio-accumulation
Bio-transformation
Bio-mineralisation
Metabolic red-ox reactions
Mobilisation processes
Bio-sorption
Bio-accumulation
Production of complexing agents

medium

low
×
×

×
×
×

×
×
×

Ranking
1 = high
2 = medium
3 = low
2
2
3
2
1

3
3
1

This will give rough estimate of what processes are more important thanother. However, it must be clear that new data from ongoing and future
research may change the ranking in the table.

Those two examples demonstrate that overlooking microbial
processes may result in models and safety assessments that do
not reflect the true situation in future radioactive waste repositories. Conservative assumptions are commonly used to overcome
such problems. Therefore, our understanding of geosphere retention phenomena in the context of long-term safety of radioactive
waste disposal will benefit from making optimal use of available
knowledge on microbial processes in order to reduce suchconservatism in future safety assessments.
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