Changes in Soil Bacterial Community Structure with Increasing Disturbance Frequency

Little is known of the responsiveness of soil bacterial community structure to disturbance. In this study, we subjected a soil microcosm to physical disturbance, sterilizing 90 % of the soil volume each time, at a range of frequencies. We analysed the bacterial community structure using 454 pyrosequencing of the 16S rRNA gene. Bacterial diversity was found to decline with the increasing disturbance frequencies. Total bacterial abundance was, however, higher at intermediate and high disturbance frequencies, compared to low and no-disturbance treatments. Changing disturbance frequency also led to changes in community composition, with changes in overall species composition and some groups becoming abundant at the expense of others. Some phylogenetic groups were found to be relatively more disturbance-sensitive or tolerant than others. With increasing disturbance frequency, phylogenetic species variability (an index of community composition) itself became more variable from one sample to another, suggesting a greater role of chance in community composition. Compared to the tightly clustered community of the original undisturbed soil, in all the aged disturbed soils the lists of most abundant operational taxonomic units (OTUs) in each replicate were very different, suggesting a possible role of stochasticity in resource colonization and exploitation in the aged and disturbed soils. For example, colonization may be affected by whichever localized concentrations of bacterial populations happen to survive the last disturbance and be reincorporated in abundance into each pot. Overall, it appears that the soil bacterial community is very sensitive to physical disturbance, losing diversity, and that certain groups have identifiable ‘high disturbance’ vs. ‘low disturbance’ niches.

[1]  H. Heuer,et al.  Bulk and Rhizosphere Soil Bacterial Communities Studied by Denaturing Gradient Gel Electrophoresis: Plant-Dependent Enrichment and Seasonal Shifts Revealed , 2001, Applied and Environmental Microbiology.

[2]  Thoughts on the processes that maintain local species diversity of ectomycorrhizal fungi , 1995 .

[3]  J. Rousk,et al.  Growth of saprotrophic fungi and bacteria in soil. , 2011, FEMS microbiology ecology.

[4]  J. Izard,et al.  The Human Oral Microbiome , 2010, Journal of bacteriology.

[5]  W. Whitman,et al.  Prokaryotes: the unseen majority. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[6]  L. Øvreås,et al.  Prokaryotic Diversity--Magnitude, Dynamics, and Controlling Factors , 2002, Science.

[7]  T. Bruns,et al.  Community structure of ectomycorrhizal fungi in a Pinus muricata forest: minimal overlap between the mature forest and resistant propagule communities , 1999, Molecular ecology.

[8]  A. Classen,et al.  Community-level physiological profiles of bacteria and fungi: plate type and incubation temperature influences on contrasting soils. , 2003, FEMS microbiology ecology.

[9]  Erko Stackebrandt,et al.  Taxonomic Note: A Place for DNA-DNA Reassociation and 16S rRNA Sequence Analysis in the Present Species Definition in Bacteriology , 1994 .

[10]  Patrick D. Schloss,et al.  Reducing the Effects of PCR Amplification and Sequencing Artifacts on 16S rRNA-Based Studies , 2011, PloS one.

[11]  C. Cannon,et al.  Communities contain closely related species during ecosystem disturbance. , 2010, Ecology letters.

[12]  J. Borneman,et al.  Molecular microbial diversity in soils from eastern Amazonia: evidence for unusual microorganisms and microbial population shifts associated with deforestation , 1997, Applied and environmental microbiology.

[13]  P. Chesson,et al.  Environmental Variability Promotes Coexistence in Lottery Competitive Systems , 1981, The American Naturalist.

[14]  C. Violle,et al.  Experimental demonstration of the importance of competition under disturbance , 2010, Proceedings of the National Academy of Sciences.

[15]  P. Hugenholtz,et al.  Investigation of Candidate Division TM7, a Recently Recognized Major Lineage of the Domain Bacteria with No Known Pure-Culture Representatives , 2001, Applied and Environmental Microbiology.

[16]  H. Barnett,et al.  Umbelopsis versiformis, a New Genus and Species of the Imperfects , 1966 .

[17]  B. Jonsson,et al.  Exploring potential biodiversity indicators in boreal forests , 1999, Biodiversity & Conservation.

[18]  J. Tiedje,et al.  Naïve Bayesian Classifier for Rapid Assignment of rRNA Sequences into the New Bacterial Taxonomy , 2007, Applied and Environmental Microbiology.

[19]  R. Henrik Nilsson,et al.  Improved software detection and extraction of ITS1 and ITS2 from ribosomal ITS sequences of fungi and other eukaryotes for analysis of environmental sequencing data , 2013 .

[20]  Katherine D. McMahon,et al.  Typhoons initiate predictable change in aquatic bacterial communities , 2008 .

[21]  Alexandros Stamatakis,et al.  RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models , 2006, Bioinform..

[22]  D. Edwards,et al.  The Impact of Selective-Logging and Forest Clearance for Oil Palm on Fungal Communities in Borneo , 2014, PloS one.

[23]  N. Stenseth,et al.  Convergent temporal dynamics of the human infant gut microbiota , 2010, The ISME Journal.

[24]  A. Colombo,et al.  Update on the Genus Trichosporon , 2008, Mycopathologia.

[25]  Graham Bell,et al.  Disturbance and diversity in experimental microcosms , 2000, Nature.

[26]  X. Le Roux,et al.  Decline of soil microbial diversity does not influence the resistance and resilience of key soil microbial functional groups following a model disturbance. , 2007, Environmental microbiology.

[27]  D. Tilman Competition and Biodiversity in Spatially Structured Habitats , 1994 .

[28]  D. Karl,et al.  Estimation of diversity and community structure through restriction fragment length polymorphism distribution analysis of bacterial 16S rRNA genes from a microbial mat at an active, hydrothermal vent system, Loihi Seamount, Hawaii , 1994, Applied and environmental microbiology.

[29]  John C. Avise,et al.  Resistance, Resilience, and Redundancy in Microbial Communities , 2008 .

[30]  R. B. Jackson,et al.  Toward an ecological classification of soil bacteria. , 2007, Ecology.

[31]  Eric R. Pianka,et al.  On r- and K-Selection , 1970, The American Naturalist.

[32]  Jessica Gurevitch,et al.  The ecology of plants , 2002 .

[33]  H. de Kroon,et al.  Does disturbance favour weak competitors? Mechanisms of changing plant abundance after flooding , 2004 .

[34]  P. Hobbs,et al.  Plant species and nitrogen effects on soil biological properties of temperate upland grasslands , 1999 .

[35]  J. Augustin,et al.  Plant rhizodeposition — an important source for carbon turnover in soils , 2002 .

[36]  E. Bååth,et al.  Comparison of temperature effects on soil respiration and bacterial and fungal growth rates. , 2005, FEMS microbiology ecology.

[37]  W. Liesack,et al.  Phylogenetic identity, growth-response time and rRNA operon copy number of soil bacteria indicate different stages of community succession. , 2007, Environmental microbiology.

[38]  P. Hobbs,et al.  Structure and function of the soil microbial community in microhabitats of a heavy metal polluted soil , 2000, Biology and Fertility of Soils.

[39]  N. Fierer,et al.  Influence of Drying–Rewetting Frequency on Soil Bacterial Community Structure , 2002, Microbial Ecology.

[40]  J. Rousk,et al.  Fungal biomass production and turnover in soil estimated using the acetate-in-ergosterol technique , 2007 .

[41]  J. Prosser,et al.  Maintenance of soil functioning following erosion of microbial diversity. , 2006, Environmental microbiology.

[42]  J. E. Harper,et al.  An experimental analysis of the coprophilous fungus succession , 1964 .

[43]  A. Arnold,et al.  Fungal endophytes: diversity and functional roles. , 2009, The New phytologist.

[44]  R. Macarthur,et al.  The Theory of Island Biogeography , 1969 .

[45]  Chin H. Wu,et al.  Resistance, resilience and recovery: aquatic bacterial dynamics after water column disturbance. , 2011, Environmental microbiology.

[46]  A. Fitter,et al.  Interactions between mycorrhizal fungi and other soil organisms , 1994, Plant and Soil.

[47]  Liang-Dong Guo,et al.  Ectomycorrhizae associated with Castanopsis fargesii (Fagaceae) in a subtropical forest, China , 2011, Mycological Progress.

[48]  R. Knight,et al.  UniFrac: a New Phylogenetic Method for Comparing Microbial Communities , 2005, Applied and Environmental Microbiology.

[49]  Jason D. Gans,et al.  Computational Improvements Reveal Great Bacterial Diversity and High Metal Toxicity in Soil , 2005, Science.

[50]  H. Ikeda Testing the intermediate disturbance hypothesis on species diversity in herbaceous plant communities along a human trampling gradient using a 4-year experiment in an old-field , 2003, Ecological Research.

[51]  D. Read,et al.  Mycorrhizas in ecosystems , 1991, Experientia.

[52]  W. Sousa The Role of Disturbance in Natural Communities , 1984 .

[53]  R. Paine,et al.  Intertidal Landscapes: Disturbance and the Dynamics of Pattern , 1981 .

[54]  William M. Schaffer,et al.  Plant strategies and the dynamics and structure of plant communities , 1989 .

[55]  J. P. Grime,et al.  Plant Strategies, Vegetation Processes, and Ecosystem Properties , 2006 .

[56]  L. Abbott,et al.  Hyphae of a vesicular—arbuscular mycorrhizal fungus maintain infectivity in dry soil, except when the soil is disturbed , 1989 .

[57]  R. Henrik Nilsson,et al.  Unravelling Soil Fungal Communities from Different Mediterranean Land-Use Backgrounds , 2012, PloS one.

[58]  E. Anaissie,et al.  Taxonomy, biology, and clinical aspects of Fusarium species , 1994, Clinical Microbiology Reviews.

[59]  J. Lawton,et al.  Variation in the Size of Animal Populations: Patterns, Problems and Artefacts , 1990 .

[60]  Mincheol Kim,et al.  Distinct Bacterial Communities Dominate Tropical and Temperate Zone Leaf Litter , 2014, Microbial Ecology.

[61]  M. Willig,et al.  Functional Diversity of Soil Bacterial Communities in the Tabonuco Forest: Interaction of Anthropogenic and Natural Disturbance1 , 1996 .

[62]  Peter B Adler,et al.  A niche for neutrality. , 2007, Ecology letters.

[63]  M. McPeek,et al.  Coexistence of the niche and neutral perspectives in community ecology. , 2006, Ecology.

[64]  J. Lovett-Doust,et al.  Plant strategies, vegetation processes, and ecosystem properties , 2002 .

[65]  H. Scherm,et al.  Biology of flower-infecting fungi. , 2006, Annual review of phytopathology.

[66]  J. Chun,et al.  Introducing EzTaxon-e: a prokaryotic 16S rRNA gene sequence database with phylotypes that represent uncultured species. , 2012, International journal of systematic and evolutionary microbiology.

[67]  P. Janssen Identifying the Dominant Soil Bacterial Taxa in Libraries of 16S rRNA and 16S rRNA Genes , 2006, Applied and Environmental Microbiology.

[68]  Matthew R. Helmus,et al.  Phylogenetic Measures of Biodiversity , 2007, The American Naturalist.

[69]  James F. Meadow,et al.  Importance of dispersal and thermal environment for mycorrhizal communities: lessons from Yellowstone National Park. , 2011, Ecology.

[70]  P. Renault,et al.  Early-stage bacterial colonization between a sterilized remoulded soil clod and natural soil aggregates of the same soil , 2007 .

[71]  E. Evans Studies on Mortierella ramanniana , 1971 .

[72]  J. Martiny,et al.  Patterns of fungal diversity and composition along a salinity gradient , 2011, The ISME Journal.

[73]  M. Sogin,et al.  Microbial community composition in sediments resists perturbation by nutrient enrichment , 2011, The ISME Journal.

[74]  Dominique Gravel,et al.  Reconciling niche and neutrality: the continuum hypothesis. , 2006, Ecology letters.

[75]  Daniel Sabatier,et al.  Tree Diversity in Tropical Rain Forests: A Validation of the Intermediate Disturbance Hypothesis , 2001, Science.

[76]  A. Magurran,et al.  Biological diversity : the coexistence of species on changing landscapes , 1994 .

[77]  E. Pianka,et al.  Niche overlap and diffuse competition. , 1974, Proceedings of the National Academy of Sciences of the United States of America.

[78]  Eduardo P. C. Rocha,et al.  The Systemic Imprint of Growth and Its Uses in Ecological (Meta)Genomics , 2010, PLoS genetics.

[79]  E. W. Beals,et al.  Bray-curtis ordination: an effective strategy for analysis of multivariate ecological data , 1984 .

[80]  M. Huston A General Hypothesis of Species Diversity , 1979, The American Naturalist.

[81]  J. Prosser,et al.  Plant host habitat and root exudates shape soil bacterial community structure , 2008, The ISME Journal.

[82]  Sanghoon Kang,et al.  SOIL BACTERIAL COMMUNITY STRUCTURE CHANGES FOLLOWING DISTURBANCE OF THE OVERLYING PLANT COMMUNITY , 2004 .

[83]  E. Bååth Growth Rates of Bacterial Communities in Soils at Varying pH: A Comparison of the Thymidine and Leucine Incorporation Techniques , 1998, Microbial Ecology.

[84]  J. Connell Diversity in tropical rain forests and coral reefs. , 1978, Science.

[85]  Campbell O. Webb,et al.  Picante: R tools for integrating phylogenies and ecology , 2010, Bioinform..

[86]  S. Bertilsson,et al.  Function-specific response to depletion of microbial diversity , 2011, The ISME Journal.

[87]  J. Lubchenco,et al.  Community Development and Persistence in a Low Rocky Intertidal Zone , 1978 .

[88]  D. M. Newbery,et al.  M. A. Huston, Biological Diversity: the coexistence of species on changing landscapes . Cambridge University Press. ISBN 0-521-36930-4 (pbk). 681 + xix. pages. £24.95. , 1995, Journal of Tropical Ecology.

[89]  E. Bååth Estimation of fungal growth rates in soil using 14C-acetate incorporation into ergosterol , 2001 .

[90]  D. Simberloff The Guild Concept and the Structure of Ecological Communities , 1991 .

[91]  S. Tringe,et al.  Comparative Metagenomics of Microbial Communities , 2004, Science.

[92]  Andreas Wilke,et al.  phylogenetic and functional analysis of metagenomes , 2022 .

[93]  R. Poulin,et al.  Species abundance distributions and numerical dominance in gastrointestinal helminth communities of fish hosts , 2008, Journal of Helminthology.

[94]  Daniel G. Brown,et al.  PANDAseq: paired-end assembler for illumina sequences , 2012, BMC Bioinformatics.

[95]  J. Chun,et al.  The analysis of oral microbial communities of wild-type and toll-like receptor 2-deficient mice using a 454 GS FLX Titanium pyrosequencer , 2010, BMC Microbiology.

[96]  Irina Dana Ofiteru,et al.  Combined niche and neutral effects in a microbial wastewater treatment community , 2010, Proceedings of the National Academy of Sciences.

[97]  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.

[98]  J. DeBruyn,et al.  Global Biogeography and Quantitative Seasonal Dynamics of Gemmatimonadetes in Soil , 2011, Applied and Environmental Microbiology.

[99]  S. Sørensen,et al.  Ecosystem response of pasture soil communities to fumigation-induced microbial diversity reductions: an examination of the biodiversity-ecosystem function relationship , 2000 .

[100]  J. P. Grime Control of species density in herbaceous vegetation , 1973 .

[101]  Martin Hartmann,et al.  Introducing mothur: Open-Source, Platform-Independent, Community-Supported Software for Describing and Comparing Microbial Communities , 2009, Applied and Environmental Microbiology.

[102]  S. Langenheder,et al.  Species sorting and neutral processes are both important during the initial assembly of bacterial communities , 2011, The ISME Journal.