Community Structure Analyses Are More Sensitive to Differences in Soil Bacterial Communities than Anonymous Diversity Indices

ABSTRACT Changes in the diversity and structure of soil microbial communities may offer a key to understanding the impact of environmental factors on soil quality in agriculturally managed systems. Twenty-five years of biodynamic, bio-organic, or conventional management in the DOK long-term experiment in Switzerland significantly altered soil bacterial community structures, as assessed by terminal restriction fragment length polymorphism (T-RFLP) analysis. To evaluate these results, the relation between bacterial diversity and bacterial community structures and their discrimination potential were investigated by sequence and T-RFLP analyses of 1,904 bacterial 16S rRNA gene clones derived from the DOK soils. Standard anonymous diversity indices such as Shannon, Chao1, and ACE or rarefaction analysis did not allow detection of management-dependent influences on the soil bacterial community. Bacterial community structures determined by sequence and T-RFLP analyses of the three gene libraries substantiated changes previously observed by soil bacterial community level T-RFLP profiling. This supported the value of high-throughput monitoring tools such as T-RFLP analysis for assessment of differences in soil microbial communities. The gene library approach also allowed identification of potential management-specific indicator taxa, which were derived from nine different bacterial phyla. These results clearly demonstrate the advantages of community structure analyses over those based on anonymous diversity indices when analyzing complex soil microbial communities.

[1]  G. Soulas,et al.  A simplified procedure for terminal restriction fragment length polymorphism analysis of the soil bacterial community to study the effects of pesticides on the soil microflora using 4,6-dinitroorthocresol as a test case , 2003, Biology and Fertility of Soils.

[2]  D. Crowley,et al.  Development of specific rhizosphere bacterial communities in relation to plant species, nutrition and soil type , 2004, Plant and Soil.

[3]  R. Seidler,et al.  Analysis of nifH Gene Pool Complexity in Soil and Litter at a Douglas Fir Forest Site in the Oregon Cascade Mountain Range , 1999, Applied and Environmental Microbiology.

[4]  P. L. Manachini,et al.  Bacillus thermodenitrificans sp. nov., nom. rev. , 2000, International journal of systematic and evolutionary microbiology.

[5]  D. Gevers,et al.  Re-evaluating prokaryotic species , 2005, Nature Reviews Microbiology.

[6]  James R. Cole,et al.  The Ribosomal Database Project (RDP-II): sequences and tools for high-throughput rRNA analysis , 2004, Nucleic Acids Res..

[7]  W. Liesack,et al.  Succession of bacterial community structure and diversity in a paddy soil oxygen gradient. , 2005, Environmental microbiology.

[8]  J. T. Staley,et al.  Biodiversity: are microbial species threatened? , 1997, Current opinion in biotechnology.

[9]  D. Bossio,et al.  Determinants of Soil Microbial Communities: Effects of Agricultural Management, Season, and Soil Type on Phospholipid Fatty Acid Profiles , 1998, Microbial Ecology.

[10]  M. Hartmann,et al.  A novel strategy to extract specific phylogenetic sequence information from community T-RFLP. , 2006, Journal of microbiological methods.

[11]  E. Smit,et al.  Diversity and Seasonal Fluctuations of the Dominant Members of the Bacterial Soil Community in a Wheat Field as Determined by Cultivation and Molecular Methods , 2001, Applied and Environmental Microbiology.

[12]  M. Friedrich,et al.  Axial Dynamics, Stability, and Interspecies Similarity of Bacterial Community Structure in the Highly Compartmentalized Gut of Soil-Feeding Termites (Cubitermes spp.) , 2003, Applied and Environmental Microbiology.

[13]  J. Handelsman,et al.  Introducing DOTUR, a Computer Program for Defining Operational Taxonomic Units and Estimating Species Richness , 2005, Applied and Environmental Microbiology.

[14]  Martin Hartmann,et al.  Semi-automated genetic analyses of soil microbial communities: comparison of T-RFLP and RISA based on descriptive and discriminative statistical approaches. , 2005, Journal of microbiological methods.

[15]  M. Hartmann,et al.  Community structures and substrate utilization of bacteria in soils from organic and conventional farming systems of the DOK long-term field experiment , 2006 .

[16]  M. Friedrich,et al.  Formation of Pseudo-Terminal Restriction Fragments, a PCR-Related Bias Affecting Terminal Restriction Fragment Length Polymorphism Analysis of Microbial Community Structure , 2003, Applied and Environmental Microbiology.

[17]  J. Raaijmakers,et al.  Statistical analysis of the Michaelis-Menten equation. , 1987, Biometrics.

[18]  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 .

[19]  J. Hughes,et al.  Counting the Uncountable: Statistical Approaches to Estimating Microbial Diversity , 2001, Applied and Environmental Microbiology.

[20]  P. Garbeva,et al.  Effects of agronomical measures on the microbial diversity of soils as related to the suppression of soil-borne plant pathogens , 2004, Biodegradation.

[21]  B. Stenberg Monitoring Soil Quality of Arable Land: Microbiological Indicators , 1999 .

[22]  T. Schmidt,et al.  The structure of microbial communities in soil and the lasting impact of cultivation , 2001, Microbial Ecology.

[23]  C. Kaplan,et al.  Variation between observed and true Terminal Restriction Fragment length is dependent on true TRF length and purine content. , 2003, Journal of microbiological methods.

[24]  S. K. Morgan Ernest,et al.  HOMEOSTASIS AND COMPENSATION: THE ROLE OF SPECIES AND RESOURCES IN ECOSYSTEM STABILITY , 2001 .

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

[26]  J. Prosser,et al.  Numerical Analysis of Grassland Bacterial Community Structure under Different Land Management Regimens by Using 16S Ribosomal DNA Sequence Data and Denaturing Gradient Gel Electrophoresis Banding Patterns , 2001, Applied and Environmental Microbiology.

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

[28]  W. Raun,et al.  Bacterial Community Structure and Diversity in a Century-Old Manure-Treated Agroecosystem , 2004, Applied and Environmental Microbiology.

[29]  W. Sloan,et al.  Prokaryotic diversity and its limits: microbial community structure in nature and implications for microbial ecology. , 2004, Current opinion in microbiology.

[30]  U. Göbel,et al.  Determination of microbial diversity in environmental samples: pitfalls of PCR-based rRNA analysis. , 1997, FEMS microbiology reviews.

[31]  F. Oaks,et al.  Improved single-strand DNA sizing accuracy in capillary electrophoresis. , 1997, Nucleic acids research.

[32]  Lawrence O. Ticknor,et al.  Empirical and Theoretical Bacterial Diversity in Four Arizona Soils , 2002, Applied and Environmental Microbiology.

[33]  C. Pankhurst,et al.  Biodiversity of soil microbial communities in agricultural systems , 1996, Biodiversity & Conservation.

[34]  J. Prosser,et al.  Molecular Analysis of Bacterial Community Structure and Diversity in Unimproved and Improved Upland Grass Pastures , 1999, Applied and Environmental Microbiology.

[35]  A. C. Kennedy Bacterial diversity in agroecosystems , 1999 .

[36]  H. Oyaizu,et al.  Microbial indices of soil fertility , 2005, Journal of applied microbiology.

[37]  H. Heuer,et al.  Analysis of actinomycete communities by specific amplification of genes encoding 16S rRNA and gel-electrophoretic separation in denaturing gradients , 1997, Applied and environmental microbiology.

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

[39]  D. Greenland,et al.  Soil Resilience and Sustainable Land Use , 1994 .

[40]  D. Dubois,et al.  Soil Fertility and Biodiversity in Organic Farming , 2002, Science.

[41]  C. Woese,et al.  Bacterial evolution , 1987, Microbiological reviews.

[42]  Joachim Doll,et al.  Organization for Economic Cooperation and Development , 2021, International Organization.

[43]  M. Hartmann,et al.  Ranking the magnitude of crop and farming system effects on soil microbial biomass and genetic structure of bacterial communities. , 2006, FEMS microbiology ecology.

[44]  John P. Reganold,et al.  Organic and Biodynamic Management Effects on Soil Biology , 2000 .

[45]  E. Delong,et al.  Environmental diversity of bacteria and archaea. , 2001, Systematic biology.

[46]  Sang Joon Kim,et al.  A Mathematical Theory of Communication , 2006 .

[47]  V. Torsvik,et al.  Pesticide effects on bacterial diversity in agricultural soils – a review , 2001, Biology and Fertility of Soils.

[48]  R. Bardgett Causes and consequences of biological diversity in soil. , 2002, Zoology.

[49]  S. J. Flynn,et al.  Opening the black box of soil microbial diversity , 1999 .

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

[51]  H. Kirchmann Biological dynamic farming — An occult form of alternative agriculture? , 1994 .

[52]  K. Timmis,et al.  An evaluation of terminal-restriction fragment length polymorphism (T-RFLP) analysis for the study of microbial community structure and dynamics. , 2000, Environmental microbiology.

[53]  N. Lupwayi,et al.  Soil microbial diversity and community structure under wheat as influenced by tillage and crop rotation , 1998 .

[54]  A. Kent,et al.  Microbial communities and their interactions in soil and rhizosphere ecosystems. , 2002, Annual review of microbiology.

[55]  Philip Hugenholtz,et al.  Impact of Culture-Independent Studies on the Emerging Phylogenetic View of Bacterial Diversity , 1998, Journal of bacteriology.

[56]  Jizhong Zhou,et al.  Evaluation of PCR-Generated Chimeras, Mutations, and Heteroduplexes with 16S rRNA Gene-Based Cloning , 2001, Applied and Environmental Microbiology.

[57]  Takahiro Kanagawa,et al.  Bias and artifacts in multitemplate polymerase chain reactions (PCR). , 2003, Journal of bioscience and bioengineering.

[58]  T. Marsh Terminal restriction fragment length polymorphism (T-RFLP): an emerging method for characterizing diversity among homologous populations of amplification products. , 1999, Current opinion in microbiology.

[59]  A. C. Kennedy,et al.  Soil microbial diversity and the sustainability of agricultural soils , 1995, Plant and Soil.

[60]  B L Maidak,et al.  The RDP-II (Ribosomal Database Project) , 2001, Nucleic Acids Res..

[61]  O. White,et al.  Environmental Genome Shotgun Sequencing of the Sargasso Sea , 2004, Science.

[62]  J. Trevors,et al.  Methods of studying soil microbial diversity. , 2004, Journal of microbiological methods.

[63]  C. E. SHANNON,et al.  A mathematical theory of communication , 1948, MOCO.

[64]  A. Edwards,et al.  Selective influence of plant species on microbial diversity in the rhizosphere , 1998 .

[65]  F. Widmer,et al.  Identification and Specific Detection of a Novel Pseudomonadaceae Cluster Associated with Soils from Winter Wheat Plots of a Long-Term Agricultural Field Experiment , 2006, Applied and Environmental Microbiology.

[66]  Yves Van de Peer,et al.  TREECON for Windows: a software package for the construction and drawing of evolutionary trees for the Microsoft Windows environment , 1994, Comput. Appl. Biosci..

[67]  P. M. Gale,et al.  Soil microbial community responses to dairy manure or ammonium nitrate applications , 2001 .

[68]  J. Hughes,et al.  New approaches to analyzing microbial biodiversity data. , 2003, Current opinion in microbiology.

[69]  Rodrigo Lopez,et al.  Multiple sequence alignment with the Clustal series of programs , 2003, Nucleic Acids Res..

[70]  R. Conrad,et al.  Impact of flooding on soil bacterial communities associated with poplar (Populus sp.) trees. , 2005, FEMS microbiology ecology.

[71]  S. Zechmeister-Boltenstern,et al.  Comparison of Diversities and Compositions of Bacterial Populations Inhabiting Natural Forest Soils , 2004, Applied and Environmental Microbiology.

[72]  P. Kemp,et al.  Estimating prokaryotic diversity: When are 16S rDNA libraries large enough? , 2004 .

[73]  G J Olsen,et al.  Phylogenetic group-specific oligodeoxynucleotide probes for identification of single microbial cells , 1988, Journal of bacteriology.

[74]  Victor Seguritan,et al.  FastGroup: A program to dereplicate libraries of 16S rDNA sequences , 2001, BMC Bioinformatics.

[75]  J. Bengtsson Which species? What kind of diversity? Which ecosystem function? Some problems in studies of relations between biodiversity and ecosystem function , 1998 .