Low Pore Connectivity Increases Bacterial Diversity in Soil

ABSTRACT One of soil microbiology's most intriguing puzzles is how so many different bacterial species can coexist in small volumes of soil when competition theory predicts that less competitive species should decline and eventually disappear. We provide evidence supporting the theory that low pore connectivity caused by low water potential (and therefore low water content) increases the diversity of a complex bacterial community in soil. We altered the pore connectivity of a soil by decreasing water potential and increasing the content of silt- and clay-sized particles. Two textures were created, without altering the chemical properties or mineral composition of the soil, by adding silt- and clay-sized particles of quartz to a quartz-based sandy soil at rates of 0% (sand) or 10% (silt+clay). Both textures were incubated at several water potentials, and the effect on the active bacterial communities was measured using terminal restriction fragment length polymorphism (TRFLP) of bacterial 16S rRNA. Bacterial richness and diversity increased as water potential decreased and soil became drier (P < 0.012), but they were not affected by texture (P > 0.553). Bacterial diversity increased at water potentials of ≤2.5 kPa in sand and ≤4.0 kPa in silt+clay, equivalent to ≤56% water-filled pore space (WFPS) in both textures. The bacterial community structure in soil was affected by both water potential and texture (P < 0.001) and was correlated with WFPS (sum of squared correlations [δ2] = 0.88, P < 0.001). These findings suggest that low pore connectivity is commonly experienced by soil bacteria under field conditions and that the theory of pore connectivity may provide a fundamental principle to explain the high diversity of bacteria in soil.

[1]  J. Six,et al.  Searching for unifying principles in soil ecology , 2009 .

[2]  D. Or,et al.  Dynamics of Microbial Growth and Coexistence on Variably Saturated Rough Surfaces , 2009, Microbial Ecology.

[3]  D. Gleeson,et al.  Minerals in soil select distinct bacterial communities in their microhabitats. , 2009, FEMS microbiology ecology.

[4]  J. Tibbits,et al.  Non-parametric multivariate comparisons of soil fungal composition : Sensitivity to thresholds and indications of structural redundancy in T-RFLP data , 2008 .

[5]  C. Campbell,et al.  Does the preferential microbial colonisation of ferromagnesian minerals affect mineral weathering in soil? , 2008, Die Naturwissenschaften.

[6]  D. Or,et al.  Limited diffusive fluxes of substrate facilitate coexistence of two competing bacterial strains. , 2008, FEMS microbiology ecology.

[7]  J. Connolly,et al.  ribosort: a program for automated data preparation and exploratory analysis of microbial community fingerprints , 2008, Molecular Ecology Resources.

[8]  Sébastien Barot,et al.  A Tale of Four Stories: Soil Ecology, Theory, Evolution and the Publication System , 2007, PloS one.

[9]  D. Gleeson,et al.  Altering the mineral composition of soil causes a shift in microbial community structure. , 2007, FEMS microbiology ecology.

[10]  Christopher B. Blackwood,et al.  Interpreting Ecological Diversity Indices Applied to Terminal Restriction Fragment Length Polymorphism Data: Insights from Simulated Microbial Communities , 2007, Applied and Environmental Microbiology.

[11]  F. Stange,et al.  Impact of soil texture on temporal and spatial development of osmotic-potential gradients between bulk soil and rhizosphere , 2007 .

[12]  L. Forney,et al.  Measuring Species Richness Based on Microbial Community Fingerprints: the Emperor Has No Clothes , 2007, Applied and Environmental Microbiology.

[13]  E. Boyd,et al.  Mineralogy Influences Structure and Diversity of Bacterial Communities Associated with Geological Substrata in a Pristine Aquifer , 2007, Microbial Ecology.

[14]  D. Gleeson,et al.  Structural diversity of bacterial communities in a heavy metal mineralized granite outcrop. , 2006, Environmental microbiology.

[15]  D. Gleeson,et al.  Characterization of Bacterial Community Structure on a Weathered Pegmatitic Granite , 2006, Microbial Ecology.

[16]  D. Gleeson,et al.  Characterization of Fungal Community Structure on a Weathered Pegmatitic Granite , 2005, Microbial Ecology.

[17]  Dani Or,et al.  Aquatic habitats and diffusion constraints affecting microbial coexistence in unsaturated porous media , 2005 .

[18]  Xavier Raynaud,et al.  SOIL CHARACTERISTICS PLAY A KEY ROLE IN MODELING NUTRIENT COMPETITION IN PLANT COMMUNITIES , 2004 .

[19]  Gerrit H. de Rooij,et al.  Methods of Soil Analysis. Part 4. Physical Methods , 2004 .

[20]  F. Widmer,et al.  Impact of Soil Drying-Rewetting Stress on Microbial Communities and Activities and on Degradation of Two Crop Protection Products , 2004, Applied and Environmental Microbiology.

[21]  Jizhong Zhou,et al.  Microbial Diversity and Heterogeneity in Sandy Subsurface Soils , 2004, Applied and Environmental Microbiology.

[22]  B. Bohannan,et al.  An ecological perspective on bacterial biodiversity , 2004, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[23]  W. M. Mcarthur Reference soils of south-western Australia , 2004 .

[24]  A. Bationo Managing Nutrient Cycles to Sustain Soil Fertility in Sub-Saharan Africa , 2004 .

[25]  R. Wagner The regulation of ribosomal RNA synthesis and bacterial cell growth , 2004, Archives of Microbiology.

[26]  R. Mural,et al.  Bacterial phylogenetic diversity and a novel candidate division of two humid region, sandy surface soils , 2003 .

[27]  C. Criddle,et al.  Understanding bias in microbial community analysis techniques due to rrn operon copy number heterogeneity. , 2003, BioTechniques.

[28]  Marti J. Anderson,et al.  CANONICAL ANALYSIS OF PRINCIPAL COORDINATES: A USEFUL METHOD OF CONSTRAINED ORDINATION FOR ECOLOGY , 2003 .

[29]  N. Stralis-Pavese,et al.  RNA isolation from soil for bacterial community and functional analysis: evaluation of different extraction and soil conservation protocols. , 2002, Journal of microbiological methods.

[30]  Thomas P. Curtis,et al.  Estimating prokaryotic diversity and its limits , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[31]  L. Øvreås,et al.  Microbial diversity and function in soil: from genes to ecosystems. , 2002, Current opinion in microbiology.

[32]  Anthony V. Palumbo,et al.  Spatial and Resource Factors Influencing High Microbial Diversity in Soil , 2002, Applied and Environmental Microbiology.

[33]  J. Tiedje,et al.  A Two-Species Test of the Hypothesis That Spatial Isolation Influences Microbial Diversity in Soil , 2002, Microbial Ecology.

[34]  E. Kandeler,et al.  Microbial Population Structures in Soil Particle Size Fractions of a Long-Term Fertilizer Field Experiment , 2001, Applied and Environmental Microbiology.

[35]  J. V. Van Impe,et al.  On the need for another type of predictive model in structured foods. , 2001, International journal of food microbiology.

[36]  Marti J. Anderson,et al.  Permutation tests for univariate or multivariate analysis of variance and regression , 2001 .

[37]  Marti J. Anderson,et al.  A new method for non-parametric multivariate analysis of variance in ecology , 2001 .

[38]  Lawrence O. Ticknor,et al.  Phylogenetic Specificity and Reproducibility and New Method for Analysis of Terminal Restriction Fragment Profiles of 16S rRNA Genes from Bacterial Communities , 2001, Applied and Environmental Microbiology.

[39]  K. R. Clarke,et al.  Change in marine communities : an approach to statistical analysis and interpretation , 2001 .

[40]  R. Rees,et al.  Soil teeming with life: new frontiers for soil science. , 2001 .

[41]  Brian H. McArdle,et al.  FITTING MULTIVARIATE MODELS TO COMMUNITY DATA: A COMMENT ON DISTANCE‐BASED REDUNDANCY ANALYSIS , 2001 .

[42]  R. Rees,et al.  Sustainable Management of Soil Organic Matter , 2000 .

[43]  R. Griffiths,et al.  Rapid Method for Coextraction of DNA and RNA from Natural Environments for Analysis of Ribosomal DNA- and rRNA-Based Microbial Community Composition , 2000, Applied and Environmental Microbiology.

[44]  W. D. de Vos,et al.  Response of a Soil Bacterial Community to Grassland Succession as Monitored by 16S rRNA Levels of the Predominant Ribotypes , 2000, Applied and Environmental Microbiology.

[45]  C. Kuske,et al.  Assessment of Microbial Diversity in Four Southwestern United States Soils by 16S rRNA Gene Terminal Restriction Fragment Analysis , 2000, Applied and Environmental Microbiology.

[46]  J. Thioulouse,et al.  Heterogeneous Cell Density and Genetic Structure of Bacterial Pools Associated with Various Soil Microenvironments as Determined by Enumeration and DNA Fingerprinting Approach (RISA) , 2000, Microbial Ecology.

[47]  Kemp,et al.  Small ribosomal RNA content in marine Proteobacteria during non-steady-state growth. , 1999, FEMS microbiology ecology.

[48]  W. P. Williams,et al.  The influence of data transformations on biological monitoring studies using macroinvertebrates , 1999 .

[49]  J. Deckers,et al.  World Reference Base for Soil Resources , 1998 .

[50]  Hans H. Cheng,et al.  Characterization of microbial diversity by determining terminal restriction fragment length polymorphisms of genes encoding 16S rRNA , 1997, Applied and environmental microbiology.

[51]  D. Wardle,et al.  The quest for a contemporary ecological dimension to soil biology , 1996 .

[52]  R. Dudal,et al.  World Reference Base For Soil Resources , 1994 .

[53]  W. Liesack,et al.  Bacterial diversity in a soil sample from a subtropical Australian environment as determined by 16S rDNA analysis , 1993, FASEB journal : official publication of the Federation of American Societies for Experimental Biology.

[54]  V. Torsvik,et al.  High diversity in DNA of soil bacteria , 1990, Applied and environmental microbiology.

[55]  M. Austin Plant strategies and the dynamics and structure of plant communities , 1989 .

[56]  D. Tilman Plant Strategies and the Dynamics and Structure of Plant Communities. (MPB-26), Volume 26 , 1988 .

[57]  Van Genuchten,et al.  A closed-form equation for predicting the hydraulic conductivity of unsaturated soils , 1980 .

[58]  Mtambanengwe Decomposition of Organic Matter in Soil as Influenced by Texture and Pore Size Distribution , 1956 .

[59]  William B. Haines,et al.  Studies in the physical properties of soil. V. The hysteresis effect in capillary properties, and the modes of moisture distribution associated therewith , 1930, The Journal of Agricultural Science.