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Agricultural Sciences, 7(2):39-45 (2002) 
© 2002 Sultan Qaboos University 
  

Physical Processes Affecting Microbial 
Habitats and Activity in Unsaturated  

Porous Media  
 
 

D. Or 
 

Department of Civil and Environmental Engineering 
University of Connecticut, Storrs, CT 06269-2037, USA 

 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 

 
 

 
 
ABSTRACT: Recent advances in soil pore space visualization and geometrical characterization coupled with improved 
models for liquid and gaseous behaviour provide the impetus for examination of physical influences on microbial habitats 
and activity. Desaturation of a porous medium is accompanied by marked changes in liquid-vapour interfacial 
configurations, which result in confinement and fragmentation of aquatic habitats, alteration of liquid and gaseous 
diffusion pathways, and introduction of mechanical stresses exerted by films and receding menisci. At the pore scale, we 
examine relationships between liquid element size (at a given potential) and typical organism or colony size, in an attempt 
to explain physical triggers for enhanced biological production of extracellular polysaccharides (EPS) coating. The role of 
EPS in habitat alteration is deduced from its structural, mechanical and transport characteristics. The interplay between 
increasing liquid-vapour interfacial area and decreasing liquid diffusion pathways with decreasing water content can be 
formulated as a function of pore space geometry. Such relationships are potentially important for optimal biological control 
of various bioremediation activities taking place at the soil profile scale. Interactions between microorganisms and solid 
surfaces are investigated in the context of adhesion and formation of biofilms. In such prevailing microbial communities, 
EPS forms complex three-dimensional structures that facilitate efficient transport processes and support a rich spatial 
arrangement of microorganisms with different affinities to oxygen and various nutrients. Effects of microbial activity on 
properties of solid surfaces including weathering and wettability, and structural stabilization of the solid matrix by 
biological products are examined. 
 
Keywords:  Microbial, unsaturated, porous media, organism, EPS, bioremediation, biofilm, bio-filter, bacteria, 
diffusion, hydraulic conductivity, soil structure. 

 
 

review of soil physics and hydrologic literature 
reveals that despite remarkable advances in soil 

characterization and sophisticated physical process 

modeling, the role of microbiological activity in 
controlling micro- and macro-scale fluxes and its 
potential impact on soil structural and transport 

A



OR 
 
 
 

 40

properties is largely ignored. As Gardner (1993) stated: 
“Soil flora and fauna may be inconvenient for the soil 
physicist, but even we should be taking them seriously 
and be thinking and writing sensibly about them.” 
Similarly, the microbiological literature is plagued with 
oversimplified depiction of natural environments and 
physical processes affecting microbial activity in 
unsaturated soils. Considering the importance and 
ubiquity of microbiological processes, the increasing 
reliance on biological processes to remedy polluted 
soils, and the use of the unsaturated zone of 
agricultural soils as an active bio-filter for wastewater 
reuse, bridging these gaps is a timely and necessary 
undertaking. 

Recent improvements in modeling pore-scale 
liquid and gaseous behavior have altered some of the 
oversimplified concepts of static (Tuller et al., 1999; 
Or and Tuller, 1999) and dynamic (Friedman, 1999) 
interfacial processes. Concurrent advances in 
biological microsensors, confocal microscopy, and in 
fluorescent in-situ hybridization (FISH) methods offer 
a potential for analyzing complex in situ microbial 
community structure and function without traditional 
bias of cultivation methods (Okabe et al., 1999; Lipski 
et al., 2001). This review is aimed at elucidating 
primary physical processes influencing microbial 
habitats and activity in unsaturated agricultural soils by 
focusing on the fragmentation of aquatic habitats with 
concurrent changes in liquid and gaseous diffusion 
pathways during desaturation. These physical changes 
trigger an array of biological responses including 
enhanced production of extracellular polysaccharides 
(EPS) that form the biofilm matrix and serve as a 
protective coating for the embedded bacterial cells 
(Roberson and Firestone, 1992; Chenu and Roberson, 
1996). 

The reduction in contiguous liquid volumes 
affects substrate and gaseous diffusion, and reduces 
mobility of bacteria and microbiovorous grazers (Savin 
et al., 2001). The largest impact of liquid 
reconfiguration is on diffusion; a key process in most 
aspects of bacterial biology (Koch, 1990). The 
reduction in aqueous continuity and reduced liquid film 
thickness as soils dry reduces nutrient (and toxic 
excretion) diffusion rates to/from bacterial 
communities. In contrast, liquid-vapor interfacial area 
and gaseous phase continuity increase with decreasing 
water content, resulting in enhancement of gaseous 
diffusion and improved exchange with the atmosphere. 
The interplay between increasing liquid-vapor 
interfacial area and decreasing liquid diffusion 
pathways with decreasing water content (Skopp, et al., 
1990) is potentially important for biological control of 
wastewater reuse and for bioremediation activities 
taking place in a soil profile (Huesemann, 1994). 

Desaturation affects diffusion processes at a 
continuum of scales ranging from diffusion within 
individual microbial colonies to diffusion at the soil 
profile scale. Discrepancies between successful 
laboratory experiments and failures under field 
conditions can be attributed to incomplete 
consideration of physical constraints operating at the 
various scales; diffusion processes in particular. 
Diffusion constrains the spatial arrangement of 
microbial colonies in soil pore spaces, their size and 
thickness, and internal arrangement of bacterial strains 
within a bacterial community.  Such spatial 
distributions can affect transport and mechanical 
properties of soils as will be discussed below.  

In a recent review of microbial biofilms Davey 
and O’toole (2000) stated that: “our perception of 
bacteria as unicellular life forms is deeply rooted in the 
pure-culture paradigm”. Observations in a variety of 
natural habitats have established that microbes persist 
attached to solid surfaces within structured biofilms 
and not free floating. Since an individual bacterium is 
unable to modify its environment they aggregate and 
form a community that provides a certain degree of 
shelter and homeostasis.  A key component of such 
microbial micro-environments is the surrounding 
extrapolymeric matrix (EPS, protein, and other 
substances). EPS forms complex three-dimensional 
structures that facilitate efficient transport processes 
and support a rich spatial arrangement of 
microorganisms with different affinities to oxygen and 
various substrates (Watnick and Kolter, 2000; Okabe et 
al., 1999).  

Microbial colonies or biofilms can significantly 
reduce the pore space available for water flow, 
resulting in a reduction in the hydraulic conductivity, 
termed biological clogging (Avnimelech and Nevo, 
1964; Okubo and Matsumoto, 1979; Baveye et 
al.,1998). Reduction in saturated hydraulic 
conductivity up to four orders of magnitude has been 
observed. Experiments in bioclogging of unsaturated 
soils under controlled laboratory conditions are 
virtually non-existent; hence it is unclear whether the 
presence of immersed biofilms will accentuate the 
highly nonlinear decrease in unsaturated hydraulic 
conductivity. Under unsaturated conditions the role of 
biofilms is likely to be dependent on spatial 
arrangement and extent, and their intrinsic transport 
properties.  

The lack of a coherent conceptual framework is 
coupled with rapid progress and emergence of highly 
specialized jargon that not only form disciplinary 
barriers, but also hamper efforts to assemble a more 
realistic picture of the complex interactions described 
above. Thus progress in these areas requires 
interdisciplinary and collaborative effort. The objective 



PHYSICAL PROCESSES AFFECTING MICROBIAL HABITATS AND 
ACTIVITY IN UNSATURATED POROUS MEDIA 

 
 

  41

 

of this work is to provide an overview of primary 
physical processes and constraints affecting microbial 
habitats and microbial activity in unsaturated soils at 
the pore scale, and highlight implications for behavior 
at the soil profile scale. Aspects of microbial activity 
and response on soil pore space, soil structure, and soil 
transport and water retention properties will be 
discussed. 
 

Overview of Physical and Microbial 
Processes in Unsaturated Soils 

 
DIFFUSION PROCESSES AND MICROBIAL ACTIVITY IN 
UNSATURATED SOILS: The reduction in conducting 
liquid pathways as soil dries reduces liquid and nutrient 
diffusion rates at all scales, particularly at the 
microscale of individual bacterial communities and 
within a biofilm. Macroscopically, the primary effect is 
on gaseous diffusion and convective supply of 
substrates. As water content decreases soil air content 
and liquid-vapor interfacial area increase resulting in 
enhancement of gaseous diffusion and improved 
gaseous exchange  (with atmosphere) at both the 
micro- and macroscale. The interplay between the 
increase in liquid-vapor interfacial area and the 
decrease in liquid diffusion pathways with decreasing 
water content can be formulated as a function of pore 
space geometry and water status. Skopp et al., (1990) 
analyzed this interplay focusing on macroscopic 
diffusion coefficients to identify an “optimal” water 
content that maximizes microbial activity at soil 
sample- or profile-scales (Figure 1). 

At the microscale, both, structure and position of a 
bacterial colony within the soil pore space are likely to 
play an important role in the onset of diffusional 
constraints for different liquid configurations. Under 
“dry” conditions soil water is primarily in the form of 
films held by surface forces. The thickness of the liquid 
film coating solid surfaces, and hydraulic connectivity 
between the liquid-filled crevices, play a primary role 
in determining substrate diffusion rates (Mills and 
Powelson , 1996).  Rivkina et al. (2000) show data 
from Siberian permafrost  (Figure 2) suggestive of 
diffusional constraints on amounts of 14C-lable acetate 
incorporation imposed by thin liquid films (film 
thickness is a function of ambient temperature). For 
relatively dry soils, the relationships between soil water 
potential and film thickness are readily available 
according to Tuller et al. (1999). 

Even at the biofilm scale, dramatic changes in 
diffusion rates are experienced as soil dries (Chenu and 
Roberson, 1996; Holden et al., 1997).  Attempts to 
quantify such effects on microbial activity have 
focused on individual processes, such as effects of  

Figure 1. (a) A conceptual sketch of (aerobic) microbial 
activity as a function of water content; and (b) comparison 
with data for Yolo soil (Skopp et al., 1990). 
 

  
Figure 2. Incorporated 14C- labeled acetate by native bacterial 
population in Siberian permafrost (cpm) vs. measured amounts 
of unfrozen soil water (% mass) and estimated film thickness 
(nm) (Rivkina, et al., 2000). 



OR 
 
 
 

 42

matric potential on diffusion through the EPS coating 
(Chenu and Roberson, 1996), effects of matric vs. 
solute potentials on nitrification (Stark and Firestone 
1995), and effects of pore space heterogeneity on 
nutrient acquisition. 

A unifying theory is clearly needed, as Crawford et 
al. (1993) state: “it is clear from the order of magnitude 
considerations presented above that to understand the 
dynamics of soil microbial population it is necessary to 
have a quantitative framework which encapsulates soil 
structure”.  By corollary, it will require detailed 
consideration of liquid organization as well. 
 
EFFECTS OF MICROBIAL ACTIVITY ON SOIL HYDRAULIC 
CONDUCTIVITY AND WATER RETENTION: The 
formation and growth of microbial biofilms, and their 
extent and spatial arrangement almost certainly affect 
soil transport, retention, and structural properties.  
 
Effects on hydraulic conductivity: Microscopic observations 
in bioclogging studies indicated that in some cases a 
continuous biofilm covering the grains had developed 
(Cunningham et al., 1991), while in other cases 
discrete microcolonies were detected (Vandevivere and 
Baveye, 1992). Observations made in a two-
dimensional glass network micromodel study indicated 
that the biomass accumulated both as biofilms covering 
the pore walls and discrete aggregates clogging the 
pore throats (Kim and Fogler, 2000). This study also 
revealed that changing from nutrient to starvation 
conditions resulted in partial biofilm sloughing and 
permeability recovery (Figure 3). 

Estimates of biofilm thickness were in the range of 
15 µm (for 0.12mm sand grains) to 150 µm (for 0.7mm 
sand grains), which could explain the significant 
porosity and permeability reductions. Rittmann (1993) 
claimed that the most important factor determining 
bacterial deposition patterns is substrate supply rate 
and proposed a normalized surface loading criterion, 
which is defined to be the actual substrate flux (i.e. rate 
of removal per unit surface area) divided by the 
minimum flux capable of supporting a deep biofilm. 
When this number is larger than 1, a continuous 
biofilm develops, and when less than 0.25 patchy 
biofilms develop, mostly in pore throats. Additional 
geometrical (pore size) (Vandevivere and Baveye, 
1992), and hydrodynamic factors (Nevo and Mitchel, 
1967) also affect the spatial arrangement of bacterial 
populations. 

Modeling efforts for bioclogging effects on 
permeability reduction were based on different 
approaches to describe the saturated hydraulic 
conductivity of the clean bed: a single cylindrical 
capillary model (Okubo and Matsumoto, 1979), cut-and-
rejoin bundle of capillaries models (Taylor et al., 1990;  

Figure 3. Dynamics of bioclogging in a glass 
micromodel (Kim and Fogler, 2000). 

 
Vandevivere et al., 1995) and the Kozeny-Carmen 
equation (Taylor et al., 1990; Vandevivere et al., 1995). 
In all the above models a uniform narrowing of the 
pore space by the continuous developing biofilm was 
assumed, which is highly unlikely. A more realistic 
assumption is that biofilms develop preferentially in 
larger pores with larger water flow (substrate supply, 
toxic compound removal), whereas for discrete 
colonies, a probable location for initial bacterial 
deposition is at pore constrictions and near grain 
contacts. Such microscopic biofilm thickening and 
single bacterial deposition patterns are characterized by 
different macroscopic permeability-porosity 
relationships along the bio-clogging process. Another  
 



PHYSICAL PROCESSES AFFECTING MICROBIAL HABITATS AND 
ACTIVITY IN UNSATURATED POROUS MEDIA 

 
 

  43

Figure 4: Changes in (a) water potential, and (b) water content 
during 14 h of drying in sand with and without EPS added 
(Roberson and Firestone, 1992). 
 
bioclogging mechanism in saturated porous media is 
gas (e.g., methane) release and consequent pore 
blockage due to entrapped bubbles (Sanchez de Lozada 
et al., 1994). 

 
Effects on water retention properties: Under unsaturated 
conditions with fragmented aquatic habitats it is likely 
that bacteria will form discrete colonies where a 
biofilm is discontinuous, thin, and covers only a 
fraction of soil mineral surfaces. Consequently, the 
different wettability properties of such organic “spots” 
on mineral surfaces will produce soil water retention 
characteristic that exhibit a fractional wettability 
behavior (Bradford and Leij, 1996; Ustohal et al., 
1998). 

In the presence of appreciable amounts of EPS, 
soil water-holding capacity increases (Figure 4), as 
demonstrated by Roberson and Firestone (1992) and 
Chenu (1993). The increased water retention during 
drying is attributed to both the direct addition of 
EPS with its very high water holding capacity (up to 
> 50g/g) and also to creation of a more open pore 
space and separation between solid particles with a 
fibrous network attached to clay particles (Chenu, 1993).  
However, upon rewetting of kaolinite-EPS complexes, 
a decrease in the amount of water absorbed was 
observed (Chenu, 1993), probably due to irreversible 
structural changes in EPS during drying (Holden et al., 
1997), and perhaps due to changes in clay wettability. 

 
Figure 5. EPS scleroglucen adsorbed on kaolinite particles 
(w.c. 1.5 g/g) (Chenu and Tessier, 1995). 
 
 
EFFECTS OF MICROBIAL ACTIVITY ON SOIL STRUCTURE:  
Formation of microbial colonies adhered to solid 
surfaces has an important effect on soil structural 
properties primarily through the formation of polymer 
bridges that bind soil particles (Chenu and Guerif, 
1991; Chenu, 1993). The microbial enmeshing of soil 
particles shown in Figure 5 has a dual role in forming 
microaggregates, and more importantly their 
stabilization (Oades, 1993). The spatial arrangement of 
microbial activity (hence microbial debris) likely plays 
an important role in the structural efficiency of such 
stabilizing agents. Moreover, we expect that the soil 
strength (and structural stability) acquired by 
accumulation of microbial debris would be strongly 
correlated to the mechanical properties of EPS forming 
the bacterial colonies (Thwaites and Mendelson, 1991). 
As clearly illustrated in Figure 5, the presence of EPS 
helps maintain an open structure among clay particles 
(and at an aggregate bed scale). Such an open structure 
is favorable for soil transport properties. Hadas et al. 
(1994) attributed the increase in aggregate size and 
strength one week after plant residue addition to 
reinforcement by fungi hyphae, whereas changes 
appearing after the sixth week were attributed to 
bacterial secretions. Following intense colonization of 
wheat rhizosphere by EPS-producing bacteria, Amellal 
et al. (1998) observed significant soil aggregation and 
concluded that P. agglomerans plays an important role 
in soil water regulation by improving aggregation. 
 

 
 



OR 
 
 
 

 44

MORPHOLOGICAL AND FUNCTIONAL ADAPTATION OF 
MICROBIAL COLONIES DURING SOIL DRYING: Studies 
have shown that under drying conditions bacterial 
colonies respond by enhanced production of EPS 
(Roberson and Firestone, 1992). Additionally, 
dehydration of non-submerged biofilms will cause 
collapse of the open structure and affect transport 
properties of the biofilm (Holden et al., 1997). An 
illustration of the morphological changes in the EPS 3-
D structure is shown in Figure 6. In contrast to the 
fibrous and open structure on the left (wet soil), the 
EPS becomes dense and amorphous. It was 
hypothesized that such a change reduces rates of water 
loss and possibly traps nutrients within the dense 
protective coating thereby assisting bacteria to survive 
desiccation (Chenu, 1993). 

An important aspect of such changes is the 
mechanical response of EPS to changes in its hydration 
status. It has been observed with similar biopolymers 
(Thwaites and Mendelson, 1991) that the tensile 
strength and the Young’s modulus increase by several 
orders of magnitude as the relative humidity (or water 
potential) decreases from near saturation. Moreover, 
the biopolymer changes from soft and ductile at high 
humidity to stiff and brittle at low humidity. 
Knowledge concerning these mechanical changes could 
help explain the role of EPS in providing mechanical 
and diffusional protection for bacterial biofilms during 
desiccation. A related issue is the marked increase in 
soil strength with decreasing soil water content. It 
would be interesting to obtain estimates of the 
proportion of observed increase in soil strength 
attributable to the increase in the strength of EPS as a 
bonding agent. 

 
Conclusions 

 
Rapid changes in liquid and interfacial 

configurations in unsaturated soils present various 
constraints to activity of microbial communities 
thereby triggering an array of biological responses to 
changes in ambient conditions. An important constraint 
highlighted in the present review is the dramatic 
change in diffusion pathways of substrates and gases. 
As the energy state of soil water (matric potential) 
decreases, the physico-biological adjustment of 
microbial communities becomes more evidenced by the 
enhanced production of EPS. The review provides a 
starting point for quantitative modeling of interactions 
between physical (a biotic) processes and microbial 
adaptation in a given pore space. Ongoing research 
focuses on pore scale interplay between solution and 
gaseous exchange in angular pores, and on 
understanding of the physical consequences of 
enhanced EPS production on micro- and macro-scale 
processes and on soil macroscopic properties. 

References 
 
Amellal, N., G. Burtin, F. Bartoli, and T. Heulin. 1998. 

Colonization of wheat roots by an exopolysaccharide-producing 
Pantoea agglomerans strain and its effect on rhizosphere soil 
aggregation. Appl. Environ. Microbiol 64:3740-3747. 

Avnimelech, Y. and Z. Nevo. 1964. Biological clogging of sands.  
Soil Sci. 98:222-226. 

Baveye, P., P. Vandevivere, B.L. Hoyle, P.C. DeLeo, and D. Sanchez 
de Lozada. 1998.  Environmental impact mechanisms of the 
biological clogging of saturated soils and aquifer materials.  
Crit. Rev. Environ. Sci. Technol. 28:123-191. 

Bradford, S.A. and F.J. Leij. 1996. Predicting two- and three-fluid 
capillary pressure-saturation relationships of porous media with 
fractional wettability. Water Resour. Res., 32, 251-259. 

Chenu, C. 1993. Clay-or-sand-polysaccharide associations as 
models for the interface between micro-organisms and soil: 
water related properties and microstructure. Geoderma 56:143-
156. 

Chenu, C. and J. Guerif. 1991. Mechanical strength of clay minerals 
as influenced by an adsorbed polysaccharide. Soil Sci. Soc. Am. 
J. 55:1076-1080. 

Chenu, C. and E.B. Roberson. 1996. Diffusion of Glucose in 
Microbial Extracellular Polysaccharide as Affected by Water 
Potential. Soil Biol.Biochem 28:877-884. 

Chenu, C. and D. Tessier. 1995. Low temperature scanning electron 
microscopy of clay and organic constituents and their relevance 
to soil microstructure. Scanning Microscopy 9:989-1010. 

Crawford, J.W., K. Ritz, and I.M. Young. 1993. Quantification of 
fungal morphology, gaseous transport and microbial dynamics 
in soil: an integrated framework utilizing fractal geometry. 
Geoderma 56:157-172. 

Cunningham, A.B., W.G. Charaklis, F. Abedeen, and D. Crawford. 
1991. Influence of biofilm accumulation on porous media 
hydrodynamics.   Environ. Sci. Technol. 25:1305-1311. 

Davey, M.A. and G.A. O’toole. 2000. Microbial biofilms: from 
ecology to molecular genetics. Microb. Molecul. Biol. Rev. 
64:847-867. 

Friedman, S. P.  1999. Dynamic contact angle explanation of flow 
rate-dependent saturation-pressure relationships during transient 
liquid flow in unsaturated porous media.  Adhesion Sci. and 
Technol 13:1495-1518. 

Gardner, W.R. 1993. A call for action.  Soil Sci. Soc. Am. J. 5:1403-
1405. 

Hadas, A., E. Rawitz, H. Etkin, and M. Margolin. 1994. Short-term 
variations of soil physical properties as a function of the amount 
and C/N ratio of decomposing cotton residues: I. Soil 
aggregation and aggregate tensile strength. Soil Till. Res. 32: 
183-198. 

Holden, P.A., J.R. Hunt, and M.K. Firestone. 1997. Toluene 
diffusion and reaction in unsaturated Pseudomonas putida 
biofilms. Biotech. Bioeng. 56:656-670. 

Huesemann, M.H. 1994. Guidelines for land-treating petroleum 
hydrocarbon-contaminated soil.  J. Soil Contamin 3:1-20. 

Kim, D.S. and H.S. Fogler. 2000. Biomass evolution in porous 
media and its effects on permeability under starvation 
conditions. Biotech. Bioeng. 69:47-56. 

Koch, A.L. 1990. Diffusion the crucial process in many aspects of 
the biology of bacteria. Adv. Microbiol. Ecology 11:37-70.  

Lipski, A., U. Friedrich, and K. Altendorf. 2001. Application of 
rRNA-targeted oligonucleotide probes in biotechnology. Appl 
Microbiol Biotechnol 56:40–57. 

Mills, A.L. and D.K. Powelson. 1996. Bacterial interactions with 
surfaces in soils. In: Bacterial Adhesion, M. Fletcher (ed.), pp. 
25-57, Wiely-Liss, New York. 

Nevo, Z. and R. Mitchel. 1967. Factors affecting biological 
clogging of sand associated with ground water recharge.  Water 
Res. 1:231-236.  



PHYSICAL PROCESSES AFFECTING MICROBIAL HABITATS AND 
ACTIVITY IN UNSATURATED POROUS MEDIA 

 
 

  45

Oades, J.M. 1993. The role of biology in the formation, stabilization, 
and degradation of soil structure. Geoderma 56:377-400. 

Okabe, S., H. Satoh, and Y. Watanabe. 1999. In situ analysis of 
nitrifying biofilms as determined by in situ hybridization and the 
use of microelectrodes.  Appl. Environ. Microbiol. 65:3182-3191. 

Okubo, T. and J. Matsumoto. 1979. Effect on infiltration rate 
biological clogging and water quality changes during artificial 
recharge. Water Resour. Res. 15:1536-1542. 

Or, D. and M. Tuller. 1999. Liquid retention and interfacial area in 
variably saturated porous media: Upscaling from pore to sample 
scale model.  Water Resour. Res. 35(12), 3591-3605. 

Rittmann, B.E. 1993. The significance of biofilms in porous media, 
Water Resour. Res. 29:2195-2202. 

Rivkina, E.M., E.I. Friedmann, C.P. Mckay, and D.A. Gilichinsky. 
2000. Metabolic activity of permafrost bacteria below the freezing 
point. Appl. Environ. Microbiol. 66:3230-3233. 

Roberson E.B. and M.K. Firestone. 1992. Relationship between 
desiccation and exopolysachharide production in soil 
Pseudomonas sp. Appl. Environ. Microbiol. 58:1284-1291. 

Roberson, E.B., C. Chenu, and M.K. Firestone. 1993. Microstructural 
changes in bacterial exopolysccharides during desiccation. Soil 
Biol.Biochem. 25:1299-1301. 

Sanchez de Lozada, D., P. Vandevivere, P. Baveye, and S. Zinder. 
1994. Decrease of the hydraulic conductivity of sand columns by 
Methanosacrina barkeri. World J. Microbiol. Biotechnol., 10:325-
333. 

Savin, M.C., J.H. Gorres, D.A. Neher, and J.A. Amador. 2001. 
Biogeophysical factors influencing soil respiration and mineral 
nitrogen content in an old field soil.  Soil Biol. Biochem. 33:429-
438. 

Skopp, J., M.D. Jawson, and J.W. Doran. 1990. Steady-state aerobic 
microbial activity as a function of soil water content. Soil Sci. 
Soc. Am. J. 54:1619-1625. 

Stark, J.M. and M.K. Firestone. 1995. Mechanisms for soil moisture 
effects on activity of nitrifying bacteria. Appl. Environ. 
Microbiol. 61:218-221. 

Taylor, S.W., P.C.D. Milly, and P.R. Jaffe. 1990.  Biofilm growth 
and the related changes in the physical properties of porous 
medium: 2. Permeability.  Water Resour. Res. 26:2161-2169. 

Thwaites, J.J. and N.H. Mendelson. 1991. Mechanical behavior of 
bacterial cell walls.  Adv. Microb. Physiol. 32:173-223. 

Tuller, M., D. Or, and L.M. Dudley. 1999. Adsorption and capillary 
condensation in porous media: Liquid retention and interfacial 
configurations in angular pores.  Water Resour. Res. 35(7): 
1949-1964. 

Ustohal, P., F. Stauffer, and T. Dracos. 1998. Measurement and 
modeling of hydraulic characteristics of unsaturated porous 
media with mixed wettability.  J. Contaminant Hydrol. 33:5-37. 

Vandevivere, P. and P. Baveye. 1992. Saturated hydraulic 
conductivity reduction caused by aerobic bacteria in sand 
columns.  Soil Sci. Soc. Am. J. 56:1-13. 

Vandevivere, P., P. Baveye, D. Sanchez de Lozada, and P. DeLeo. 
1995. Microbial clogging of saturated soils and aquifer 
materials: Evaluation of mathematical models.  Water Resour. 
Res. 31:2173-2180. 

Watnick, P. and R. Kolter. 2000. Biofilm, City of microbes. J. 
Bacter. 182:2675-2679. 

______________________________________________________   
Received  August 2002. 
Accepted  November 2002.