Key Points
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Soil microbiology is enjoying a period of challenge and discovery made possible by the availability of new approaches for characterizing microbial communities and for imaging the soil environment.
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Soils are highly complex and the development of soil microbiology as a systems science requires that microbial ecologists take full account of the spatio–temporal heterogeneity of microbial communities and their physical environments. The evolution of microbial communities (diversity) and their response in space and time (function) can be seen as emergent properties of this physicochemical environment.
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The introduction of imaging techniques such as fluorescence in situ hybridization (FISH), FISH-microautoradiography (MAR), nano-secondary ion mass spectrometry (Nano-SIMS) and X-ray tomography offer new opportunities for locating microorganisms in their three-dimensional (3D) environment and for relating this to selected functions. However, none of the current analytical approaches offer an ideal solution for quantitatively imaging microorganisms in their physical environment, and further developments are needed.
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Innovations in modelling are providing the tools needed to tackle the twin problems of integrating the physical heterogeneity of the soil environment with the dynamics of microbial communities. These methods have all been derived from developments in physics and have the advantage of enabling the stochastic behaviour of individual components of these complex, spatially segregated systems to be modelled.
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Three modelling approaches are described. The first of these, individual based (IB) models, makes it possible to deal with individual particles and simulate their behaviours stochastically. General IB models are used when variability in individual components are deemed important in governing system processes. However, IB models are limited in their application to soils as they cannot model the dynamic impacts of microbial activity on the physical environment.
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The lattice Boltzmann (LBM) method can be used to describe the multiphase transport processes typical of soil environments and is itself an IB model that simulates the 3D environment by tracking individual particles. It has the advantage over general IB models in that it uses interaction rules to reproduce surface tension and viscosity effects and can accommodate how these are modified by microbial growth and activity.
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Network models are based on graph theory and, like IB and LBM, can be used to model individual components such as colonies of individual cells in a biological system. They differ in their application from IB and LBM in that the interactions between individual components are modelled as individual entities rather than as emergent properties. An important limitation of network models is that they currently do not explicitly address space.
Abstract
The introduction of new approaches for characterizing microbial communities and imaging soil environments has benefited soil microbiology by providing new ways of detecting and locating microorganisms. Consequently, soil microbiology is poised to progress from simply cataloguing microbial complexity to becoming a systems science. A systems approach will enable the structures of microbial communities to be characterized and will inform how microbial communities affect soil function. Systems approaches require accurate analyses of the spatio–temporal properties of the different microenvironments present in soil. In this Review we advocate the need for the convergence of the experimental and theoretical approaches that are used to characterize and model the development of microbial communities in soils.
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References
Brantley, S. L. Frontiers in Exploration of the Critical Zone: Report of a Workshop sponsored by the National Science Foundation (NSF), October 24–26, 2005. Newark, Delaware, 30p [online] <http://www.czen.org/files/CZENBookletJuly06_0.pdf>, (2005). A must-read discussion of the importance of soils in the environment and of the need to protect them. Includes a full discussion of the developing soil science research agenda.
Lawton, J. H. What do species do in ecosystems? Oikos 71, 367–374 (1994).
Griffiths, R. I., Whiteley, A. S., O'Donnell, A. G. & Bailey, M. J. Influence of depth and sampling time on bacterial community structure in an upland grassland soil. FEMS Microbiol. Ecol. 43, 35–43 (2003).
Crecchio, C. et al. Functional and molecular responses of soil microbial communities under differing soil management practices. Soil Biol. Biochem. 36, 1873–1883 (2004).
Girvan, M. S. et al. Bacterial diversity promotes community stability and functional resilience after perturbation. Env. Microbiol. 7, 301–313 (2005).
Constanza, R. et al. The value of the world's ecosystem services and natural capital. Nature 387, 253–260 (1997)
Young, I. M. & Crawford, J. W. Interactions and self-organization in the soil–microbe complex. Science 304, 1634–1637 (2004) Sets out the arguments for treating the soil–plant–microorganism complex as a self-organizing system. in which microorganisms work to modify their immediate physical environment.
Lüttge, A., Zhang, L. & Nealson, K. H. Mineral surfaces and their implications for microbial attachment: results from Monte Carlo simulations and direct surface observations. Am. J. Sci. 305, 766–790 (2005).
Nannipieri, P. et al. Microbial diversity and soil functions. Eur. J. Soil Sci. 54, 655–670 (2003).
Crawford, J. W, Harris, J. A., Ritz, K. & Young, I. M. Towards an evolutionary ecology of life in soil. Trends Ecol. Evol. 20, 81–87 (2005) Makes the case for treating soils as a dynamic system and of the need for a conceptual framework for soil ecology research.
Ettema, C. H. & Wardle, D. A. Spatial soil ecology. Trends Ecol. Evol. 17, 77–183 (2002).
Brock, T. D. Principles of Microbial Ecology (Prentice-Hall, Englewood Cliffs, 1966).
Wu, J., O'Donnell, A. G., He, Z. L. & Syers, J. K. A fumigation-extraction method for the measurement of soil microbial biomass-S. Soil Biol. Biochem. 26, 117–125 (1994).
Wu, J., He, Z. L., Wei, W. X., O'Donnell, A. G. & Syers, J. K. Quantifying microbial biomass phosphorus in acid soils. Biol. Fert. Soils 32, 500–507 (2000).
McLauchlan, K. The nature and longevity of agricultural impacts on soil carbon and nutrients: a review. Ecosystems 9, 1364–1382 (2006).
Parton, W. J. & Rasmussen, P. E. Long-term effects of crop management in wheat fallow: II. CENTURY model simulations. Soil Sci. Soc. Am. J. 58, 530–536 (1994).
Wu, J., O'Donnell, A. G., Syers, J. K., Adey, M. A. & Vityakon, P. Modelling soil organic matter changes in ley-arable rotations in sandy soils of northeast Thailand. Eur. J. Soil Sci. 49, 463–470 (1998).
Shibu, M. E., Leffelaar, P. A., Van Keulen, H. & Aggarwal, P. K. Quantitative description of soil organic matter dynamics — a review of approaches with reference to rice-based cropping systems. Geoderma 137, 1–18 (2006).
Coleman, K. & Jenkinson, D. S. in Evaluation of Soil Organic Matter Models Using Existing Long-term Datasets. Proceedings of the NATO Advanced Research workshop, NATO ASI Series I vol. 38 (eds Powlson et al.) 237–246 (Springer-Verlag, Berlin, 1996).
Amman, R. I., Ludwig, W. & Schleifer, K. H. Phylogenetic identification and in situ detection and identification of individual microbial cells without cultivation. Microbiol. Rev. 50, 143–169 (1995).
Torsvik, V. & Ovreas, L. Microbial diversity and function in soil: from genes to ecosystems. Curr. Opin. Microbiol. 5, 240–245 (2002).
Young, I. M. & Ritz, K. in Biological Diversity and Function in Soils (eds Bardgett et al.) 44–56 (Cambridge University Press, Cambridge, 2005).
O'Donnell, A. G., Colvan, S. R., Supaphol, S. & Malosso, E. in Biological Diversity and Function in Soils (eds Bardgett et al.) 44–56 (Cambridge University Press, Cambridge, 2005).
Miller, S. D., Haddock, S. H. D., Elvidge, C. D. & Lee, T. F. Detection of a bioluminescent milky sea from space. Proc. Natl Acad. Sci. USA 102, 14181–14184 (2005).
Miller M. B. & Bassler B. L. Quorum sensing in bacteria. Ann. Rev. Microbiol. 55, 165–199 (2001).
Sorensen, S. J. et al. Studying plasmid horizontal transfer in situ: a critical review. Nature Rev. Microbiol. 9, 700–710 (2005).
Martiny, J. B. H. et al. Microbial biogeography: putting microorganisms on the map. Nature Rev. Microbiol. 4, 102–112 (2006).
Horner-Devine, M. C. et al. A taxa–area relationship for bacteria. Nature 432, 750–753 (2004).
Grundmann, G. L. Spatial scales of soil bacterial diversity — the size of a clone. FEMS Microbiol. Ecol. 48, 119–127 (2004). Provides an excellent overview of the problems and challenges of studying microorganisms in soils. A good source of references for further reading on studies of microbial processes at the microscale.
Grundmann, G. L. et al. Spatial modeling of nitrifier microhabitats in soil. Soil Sci. Soc Am. J. 65, 1709–1716 (2001).
Harris, P. J. in Beyond the Biomass (eds Ritz et al.) 239–246 (John Wiley & Sons, Chichester, 1994).
Nunan, N. et al. In situ spatial patterns of soil bacterial populations, mapped at multiple scales, in an arable soil. Microb. Ecol. 44, 296–305 (2002).
Pallud, C. et al. Modification of spatial distribution of 2,4-dichloro-phenoxyacetic acid degrader microhabitats during growth in soil columns. Appl. Environ. Microbiol. 70, 2709–2716 (2004).
Amato, M. & Ladd, J. N. Assay for microbial biomass based on ninhydrin-reactive nitrogen in extracts of fumigated soils. Soil Biol. Biochem. 20, 107–114 (1988)
Brookes, P. C., Powlson, D. S. & Jenkinson, D. S. Measurement of microbial biomass phosphorus in soil. Soil Biol. Biochem. 15, 9–16 (1982).
O'Donnell, A. G. et al. Plants and fertilisers as drivers of change in microbial community structure and function in soils. Plant Soil 232, 135–145 (2001).
Rogers, S. W., Moorman, T. B. & Ong, S. K. Fluorescent in situ hybridisation and microautoradiography applied to ecophysiology in soil. Soil Sci. Soc. Am. J. 71, 620–631 (2007).
Klauth, P., Wilhelm, R., Klumpp, E., Poschen, L. & Groeneweg, J. Enumeration of soil bacteria with the green fluorescent nucleic acid dye Sytox green in the presence of soil particles. J. Microbiol Meth. 59, 189–198 (2004).
Ness, J. M. et al. Combined tyramide signal amplification and quantum dots for sensitive and photostable immunofluorescence detection. J. Histochem. Cytochem. 51, 981–987 (2003).
Alivisatos, A. P., Gu, W. & Larabell, C. Quantum dots as cellular probes. Ann. Rev. Biomed. Eng. 7, 55–76 (2005).
Nunan, N., Wu, K. J., Young, I. M., Crawford, J. W. & Ritz, K. Spatial distribution of bacterial communities and their relationships with the micro-architecture of soil. FEMS Microbiol. Ecol. 44, 203–215 (2003).
DeLong, E. F., Wickham, G. S. & Pace, N. R. Phylogenetic stains: ribosomal RNA based probes for the identification of single microbial cells. Science 243, 1360–1363 (1989).
Amann, R. I., Ludwig, W., Gortz, H. D. & Schleifer, K. H. Identification in situ and phylogeny of uncultured bacterial endosymbionts. Nature 351, 161–164 (1991).
Murrell, J. C. & Radajewski, S. Cultivation-independent techniques for studying methanotroph ecology. Res. Microbiol. 151, 807–814 (2000).
Lee, N. et al. Combination of fluorescent in situ hybridization and microautoradiography — a new tool for structure-function analyses in microbial ecology. Appl. Environ. Microbiol. 65, 1289–1297 (1999).
Ouverney, C. C. & Fuhrman, J. A. Combined microautoradiography — 16S rRNA probe technique for determination of radioisotope uptake by specific microbial cell types in situ. Appl. Environ. Microbiol. 65, 1746–1752 (1999).
Wagner, M., Nielsen, P. H., Loy, A., Nielsen, J. L. & Daims, H. Linking microbial community structure with function: fluorescence in situ hybridization-microautoradiography and isotope arrays. Curr. Opin. Biotechnol. 17, 83–91 (2006). Reviews the current state-of-the-art techniques in FISH. Includes a critical analysis of the advantages and disadvantages of the different approaches.
Orphan, V. J. et al. Methane-consuming archaea revealed by directly coupled isotopic and phylogenetic analysis. Science 293, 484–487 (2001). Presents an elegant application of SIMS and its use in microbial ecology for colocating microorganisms and function.
Ferrari, B. C., Tujula N., Stoner, K. & Kjelleberg, S. Catalyzed reporter deposition-fluorescence in situ hybridization allows for enrichment-independent detection of microcolony-forming soil bacteria. Appl. Environ. Microbiol. 72, 918–922 (2006).
Nielsen, J. L., Christensen, D., Kloppenborg, M. & Nielsen, P. H. Quantification of cell-specific substrate uptake by probe-defined bacteria under in situ conditions by microautoradiography and fluorescence in situ hybridization. Environ. Microbiol. 5, 202–211 (2003).
Nielsen, J. L. & Nielsen, P. H. in Methods in Enzymology (ed. Leadbetter, J.) 237–256 (Academic Press, San Diego, 2005).
Hesselsoe, M., Nielsen, J. L., Roslev, P. & Nielsen, P. H. Isotope labeling and microautoradiography of active heterotrophic bacteria on the basis of assimilation of 14CO2 . Appl. Environ. Microbiol. 71, 646–655 (2005).
Davis, K. J. & Lüttge, A. Quantifying the relationship between microbial attachment and mineral surface dynamics using vertical scanning interferometry (VSI). Am. J. Sci. 305, 727–751 (2005).
Lower, S. K., Hochella, M. F. & Beveridge, T. J. Bacterial recognition of mineral surfaces: nanoscale interactions between Shewanella and α-FeOOH. Science 292, 1360–1363 (2001).
Boyd, R. D. et al. Use of the atomic force microscope to determine the effect of substratum surface topography on bacterial adhesion. Langmuir 18, 2343–2346 (2002).
Slodzian, G., Daigne, B., Girard, F., Boust, F. & Hillion, F. Scanning secondary ion analytical microscopy with parallel detection. Biol. Cell 74, 43–50 (1992).
Herrmann, A. M. et al. A novel method for the study of the biophysical interface in soils using nano-scale secondary ion mass spectrometry. Rapid Comm. Mass Spectrom. 21, 29–34 (2007).
Cliff, J. B., Gaspar, D. J., Bottomley, P. J. & Myrold, D. D. Exploration of inorganic C and N assimilation by soil microbes with time-of-flight secondary ion mass spectrometry. Appl. Environ. Microbiol. 68, 4067–4073 (2002).
Cliff, J. B., Bottomley, P. J., Gaspar, D. J. & Myrold, D. D. Nitrogen mineralization and assimilation at millimeter scales. Soil Biol. Biochem. 39, 823–826 (2007).
McIntosh, R., Nicastro, D. & Mastronarde, D. New views of cells in 3D: an introduction to electron tomography. Trends Cell Biol. 15, 43–51 (2005). This paper provides a comprehensive introduction to the use of X-ray tomography in biology.
Le Gros, M. A., McDermott, G. & Larabell, C. A. X-ray tomography of whole cells. Curr. Opin. Struct. Biol. 15, 593–600 (2005).
Davis, G. R. & Elliott, J. C. X-ray microtomography scanner using time-delay integration for elimination of ring artefacts in the reconstructed image. Nucl. Instrum. Methods Phys. Res. A 394, 157–162 (1997).
Rogasik, H. et al. Discrimination of soil phases by dual energy X-ray tomography. Soil Sci. Soc. Am. J. 63, 741–751 (1999).
Feeney, D. S. et al. Three-dimensional microorganization of the soil–root–microbe system. Microbial Ecol. 52, 151–158 (2006). Provides some of the first data on microhabitat space obtained using bench-top CT scanners and describes how geostatistical analysis of these data supports the hypothesis that soil is a self-organizing system.
Johnson, S. N., Read, D. B. & Gregory, P. J. Tracking larval insect movement within soil using high resolution X-ray micro-tomography. Ecol. Entomol. 29, 117–122 (2004).
Cohen, M. C. Sexual isolation and speciation in bacteria. Genetica 116, 359–370 (2002).
Ward, N. & Fraser, C. M. How genomics has affected the concept of microbiology. Curr. Opin. Microbiol. 8, 564–571 (2005).
Klein, D. A. & Paschke M. W. Filamentous fungi: the indeterminate lifestyle and microbial ecology. Microbial Ecol. 47, 224–235 (2004).
Ward, D. M. A macrobiological perspective on microbial species. Microbe 1, 269–278 (2006).
Gao, L., Liang, W., Jinag, Y. & Wen, D. Comparison of soil organic matter models. J. Appl. Ecol. 14, 1804–1808 (2003).
Lomnicki, A. in Individual-based models and approaches in ecology (eds DeAngelis, D. L. & Gross, L. J.) 3–17 (Chapman and Hall, New York, 1992).
DeAngelis, D. L. & Mooij, W. M. Individual-based modeling of ecological and evolutionary processes. Ann. Rev. Ecol. Evol Syst. 36, 147–168 (2005). Provides a good introduction to IB modelling and its applications in biology.
Kreft, J. U., Booth, G. & Wimpenny, J. W. T. BacSim, a simulator for individual-based modelling of bacterial colony growth. Microbiol. 144, 3275–3287 (1998).
Picioreanu, C., Kreft, J. U. & van Loosdrecht, M. C. M. Particle-based multidimensional multi-species biofilm model. Appl. Environ. Microbiol. 70, 3024–3040 (2004).
Vlachos, C., Gregory, R., Paton, R. C., Saunders, J. R. & Wu, Q. H. Individual-based modelling of bacterial ecologies and evolution. Comp. Funct. Genom. 5, 100–104 (2004).
Ginovart, M., López, D. & Gras, A. Individual-based modelling of microbial activity to study mineralization of C and N and nitrification process in soil. Nonlinear Anal. Real World Apps. 6, 773–795 (2005). First report of IB modelling applied to microorganisms and their role in carbon and nitrogen cycling in soils.
Raabe, D. Overview of the lattice Boltzmann method for nano- and microscale fluid dynamics in materials science and engineering. Model. Sim. Mat. Sci. Eng. 6, R13–R46 (2004).
Zhang, X. et al. Determination of soil hydraulic conductivity with the lattice Boltzmann method and soil thin-section technique. J. Hydrol. 306, 59–70 (2005).
Erdös, P. & Réyni, A. On the evolution of random graphs. Publ. Math. Inst. Hung. Acad. Sci. 5, 17–61 (1960).
Agrawal, H. Extreme self-organization in networks constructed from gene expression data. Phys. Rev. Lett. 89, 268702 (2002).
Wuchty, S. Scale-free behaviour in protein domain networks. Mol. Biol. Evol. 18, 1694–1702 (2001).
Shirley, M. D. F. & Rushton, S. P. The impacts of network topology on disease spread. Ecol. Complex. 2, 287–99 (2005).
Meakin P. Fractal aggregates in geophysics. Rev. Geophys. 29, 317–354 (1991).
Gisiger, T. Scale invariance in biology: coincidence or footprint of a universal mechanism? Biol. Rev. 76, 161–209 (2001).
Rappoldt, C. & Crawford, J. W. The distribution of anoxic volume in a fractal model of soil. Geoderma 88, 329–347 (1999).
Lieberman, E., Hauert C. & Nowak M. A. Evolutionary dynamics on graphs. Nature 433, 312–316 (2005).
Anderson, P. E. & Jensen, H. J. Network properties, species abundance and evolution in a model of evolutionary ecology. J. Theor. Biol. 232, 551–558 (2005).
Acknowledgements
We are grateful to the anonymous reviewers for helpful and constructive comments on the manuscript. Our work in this area is supported by a range of sponsors, but in particular by the Biotechnology and Biological Sciences Research Council (BBSRC), the Natural Environment Research Council (NERC) and the Engineering and Physical Sciences Research Council (EPSRC), UK.
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Glossary
- Soil porosity
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Although there is no sharp demarcation, macropores allow the movement of air and percolating water, whereas micropores, under normal field conditions, are generally filled with water and limit the movement of air. Water movement in micropores is usually restricted to slow capillary movement. A good illustration of the importance of pore-size distribution is a sandy soil, where despite a low total porosity the movement of air and water is rapid because macropores dominate.
- Capillary force
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As used in this Review, a capillary force enables water to move against gravity and is the net effect of the attractive force of water for the solid matrix through which it moves (adhesion) and the surface tension of water. Surface tension of water is largely a consequence of the attraction of polar water molecules for each other (cohesion).
- Gravimetric force
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Refers to the movement of soil water under the force of gravity. Gravitational water drains easily from soils and is not influenced by interactions with the solid matrix.
- Soil microbial biomass
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The soil microbial biomass concept assumes that the entire soil microbial population (bacteria, fungi, protozoa and so on) can be treated as a single entity. It is easy to measure and has been used extensively in soil science to assess and predict the impact of management, climate, pollution and other factors on the soil biota.
- Ecophysiology
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Refers to the adaptation of microorganisms to growth in natural environments. In soils, the physiology of individual members of a population can change according to the individual biotic and abiotic environments. It is the distribution of these physiologies in space and time that delivers soil functions.
- Kriging
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Kriging is a set of geostatistical methods that are used to interpolate values of spatial patterns at unsampled points. Kriging recognizes that in any set of samples or measurements there may be underlying and systematic spatial patterning of the data.
- Mean field theory
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Mean field theory deals with multiple system components by replacing the complexity of interactions with an average interaction. The accuracy of mean field analyses is dependent on the number of interacting systems. High dimension systems are more accurate.
- Graph theory
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Graph theory is the study of graphs, which in mathematics and computer sciences are used to model pair-wise relationships between objects. The interactions (edges) between each pair of objects (vertices) can be directed (for example, vertex A predates vertex B), or undirected (for example, vertices A and B are in competition).
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O'Donnell, A., Young, I., Rushton, S. et al. Visualization, modelling and prediction in soil microbiology. Nat Rev Microbiol 5, 689–699 (2007). https://doi.org/10.1038/nrmicro1714
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DOI: https://doi.org/10.1038/nrmicro1714
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