Soil Microbiome Is More Heterogeneous in Organic Than in Conventional Farming System

Organic farming system and sustainable management of soil pathogens aim at reducing the use of agricultural chemicals in order to improve ecosystem health. Despite the essential role of microbial communities in agro-ecosystems, we still have limited understanding of the complex response of microbial diversity and composition to organic and conventional farming systems and to alternative methods for controlling plant pathogens. In this study we assessed the microbial community structure, diversity and richness using 16S rRNA gene next generation sequences and report that conventional and organic farming systems had major influence on soil microbial diversity and community composition while the effects of the soil health treatments (sustainable alternatives for chemical control) in both farming systems were of smaller magnitude. Organically managed system increased taxonomic and phylogenetic richness, diversity and heterogeneity of the soil microbiota when compared with conventional farming system. The composition of microbial communities, but not the diversity nor heterogeneity, were altered by soil health treatments. Soil health treatments exhibited an overrepresentation of specific microbial taxa which are known to be involved in soil suppressiveness to pathogens (plant-parasitic nematodes and soil-borne fungi). Our results provide a comprehensive survey on the response of microbial communities to different agricultural systems and to soil treatments for controlling plant pathogens and give novel insights to improve the sustainability of agro-ecosystems by means of beneficial microorganisms.

[1]  B. Griffiths,et al.  Effect of organic, conventional and mixed cultivation practices on soil microbial community structure and nematode abundance in a cultivated onion crop. , 2013, Journal of the science of food and agriculture.

[2]  J. Postma,et al.  Soil suppressiveness and functional diversity of the soil microflora in organic farming systems , 2008 .

[3]  R. Tofalo,et al.  Long-term impact of farm management and crops on soil microorganisms assessed by combined DGGE and PLFA analyses , 2014, Front. Microbiol..

[4]  Kai Xue,et al.  Functional Gene Differences in Soil Microbial Communities from Conventional, Low-Input, and Organic Farmlands , 2012, Applied and Environmental Microbiology.

[5]  A. Ueki,et al.  Development of anaerobic bacterial community consisted of diverse clostridial species during biological soil disinfestation amended with plant biomass , 2012 .

[6]  P. Haydock,et al.  Disease complexes involving plant parasitic nematodes and soilborne pathogens , 2002 .

[7]  Shuijin Hu,et al.  Effect of organic, sustainable, and conventional management strategies in grower fields on soil physical, chemical, and biological factors and the incidence of Southern blight , 2007 .

[8]  C. Mehta,et al.  Compost: its role, mechanism and impact on reducing soil-borne plant diseases. , 2014, Waste management.

[9]  M. Rundlöf,et al.  Assessing the effect of the time since transition to organic farming on plants and butterflies , 2011, The Journal of applied ecology.

[10]  R. Knight,et al.  Soil bacterial and fungal communities across a pH gradient in an arable soil , 2010, The ISME Journal.

[11]  Lynne A. Goodwin,et al.  Complete genome sequence of Chitinophaga pinensis type strain ( UQM 2034 T ) , 2010 .

[12]  Y. Oka.  Mechanisms of nematode suppression by organic soil amendments—A review , 2010 .

[13]  M. V. D. van der Heijden,et al.  Soil biodiversity and soil community composition determine ecosystem multifunctionality , 2014, Proceedings of the National Academy of Sciences.

[14]  M. Hartmann,et al.  Distinct soil microbial diversity under long-term organic and conventional farming , 2014, The ISME Journal.

[15]  B. Cardinale,et al.  Biodiversity conservation in agriculture requires a multi-scale approach , 2014, Proceedings of the Royal Society B: Biological Sciences.

[16]  Rob Knight,et al.  UCHIME improves sensitivity and speed of chimera detection , 2011, Bioinform..

[17]  M. Schloter,et al.  Response of soil microbial biomass and community structures to conventional and organic farming systems under identical crop rotations. , 2007, FEMS microbiology ecology.

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

[19]  E. Khafipour,et al.  Pyrosequencing Reveals the Influence of Organic and Conventional Farming Systems on Bacterial Communities , 2012, PloS one.

[20]  T. Lumley,et al.  gplots: Various R Programming Tools for Plotting Data , 2015 .

[21]  M. Schloter,et al.  Dynamics of Soil Bacterial Communities in Response to Repeated Application of Manure Containing Sulfadiazine , 2014, PloS one.

[22]  W. Verstraete,et al.  Effect of Phenylurea Herbicides on Soil Microbial Communities Estimated by Analysis of 16S rRNA Gene Fingerprints and Community-Level Physiological Profiles , 1999, Applied and Environmental Microbiology.

[23]  D. Neher.  Ecology of plant and free-living nematodes in natural and agricultural soil. , 2010, Annual review of phytopathology.

[24]  Jinkui Yang,et al.  Bacteria used in the biological control of plant-parasitic nematodes: populations, mechanisms of action, and future prospects. , 2007, FEMS microbiology ecology.

[25]  P. Legendre,et al.  Associations between species and groups of sites: indices and statistical inference. , 2009, Ecology.

[26]  M. McBride,et al.  Flavobacterium johnsoniae Chitinase ChiA Is Required for Chitin Utilization and Is Secreted by the Type IX Secretion System , 2013, Journal of bacteriology.

[27]  Peer Bork,et al.  Interactive Tree Of Life (iTOL): an online tool for phylogenetic tree display and annotation , 2007, Bioinform..

[28]  Mattias de Hollander,et al.  Impact of long-term N, P, K, and NPK fertilization on the composition and potential functions of the bacterial community in grassland soil. , 2014, FEMS microbiology ecology.

[29]  O. S. Correa,et al.  Pyrosequencing Reveals Changes in Soil Bacterial Communities after Conversion of Yungas Forests to Agriculture , 2015, PloS one.

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

[31]  Min Yang,et al.  Long-term fertilization regimes affect bacterial community structure and diversity of an agricultural soil in northern China , 2008 .

[32]  Sven Rahmann,et al.  Genome analysis , 2022 .

[33]  Teja Tscharntke,et al.  Beta diversity at different spatial scales: plant communities in organic and conventional agriculture. , 2006, Ecological applications : a publication of the Ecological Society of America.

[34]  P. Claus,et al.  Methanogenic archaea are globally ubiquitous in aerated soils and become active under wet anoxic conditions , 2011, The ISME Journal.

[35]  J. Bengtsson,et al.  The effects of organic agriculture on biodiversity and abundance: a meta‐analysis , 2005 .

[36]  I. Good.  THE POPULATION FREQUENCIES OF SPECIES AND THE ESTIMATION OF POPULATION PARAMETERS , 1953 .

[37]  Karoline Faust,et al.  Soil microbiome responses to the short‐term effects of Amazonian deforestation , 2015, Molecular ecology.

[38]  William N. Venables,et al.  Modern Applied Statistics with S , 2010 .

[39]  A. Ploeg,et al.  Using marigold (Tagetes spp.) as a cover crop to protect crops from plant-parasitic nematodes , 2010 .

[40]  P. Simonet,et al.  Soil Bacterial Community Shifts after Chitin Enrichment: An Integrative Metagenomic Approach , 2013, PloS one.

[41]  E. Kuramae,et al.  Acidobacterial community responses to agricultural management of soybean in Amazon forest soils. , 2013, FEMS microbiology ecology.

[42]  James A. Foster,et al.  Phylogenetics Clearcut : a fast implementation of relaxed neighbor joining , 2006 .

[43]  J. Olden,et al.  Ecological and evolutionary consequences of biotic homogenization. , 2004, Trends in ecology & evolution.

[44]  P. Struik,et al.  Ecological concepts in organic farming and their consequences for an organic crop ideotype , 2002 .

[45]  Eoin L. Brodie,et al.  Shifts in the phylogenetic structure and functional capacity of soil microbial communities follow alteration of native tussock grassland ecosystems , 2013 .

[46]  G. Brown,et al.  Soil biodiversity for agricultural sustainability , 2007 .

[47]  G. Korthals,et al.  Long-term effects of eight soil health treatments to control plant-parasitic nematodes and Verticillium dahliae in agro-ecosystems , 2014 .

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

[49]  Pelin Yilmaz,et al.  The SILVA ribosomal RNA gene database project: improved data processing and web-based tools , 2012, Nucleic Acids Res..

[50]  C. Kremen,et al.  Synthesis, part of a Special Feature on A Social-Ecological Analysis of Diversified Farming Systems: Benefits, Costs, Obstacles, and Enabling Policy Frameworks Ecosystem Services in Biologically Diversified versus Conventional Farming Systems: Benefits, Externalities, and Trade-Offs , 2012 .

[51]  J. Vivanco,et al.  Pyrosequencing Assessment of Soil Microbial Communities in Organic and Conventional Potato Farms. , 2010, Plant disease.

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

[53]  David Kleijn,et al.  Agri-environment schemes do not effectively protect biodiversity in Dutch agricultural landscapes , 2001, Nature.

[54]  M. Moens,et al.  Effect of marigold (Tagetes patula) on population dynamics of Pratylenchus penetrans in a field , 2006 .

[55]  Dominique Türkowsky,et al.  Crop monoculture rather than agriculture reduces the spatial turnover of soil bacterial communities at a regional scale. , 2015, Environmental microbiology.

[56]  T. Widmer,et al.  Relationship Between Levels of Cyanide in Sudangrass Hybrids Incorporated into Soil and Suppression of Meloidogyne hapla. , 2002, Journal of nematology.

[57]  Cynthie Wong,et al.  Bacillus thuringiensis crystal proteins that target nematodes , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[58]  M. Strand,et al.  Organic agriculture promotes evenness and natural pest control , 2010, Nature.

[59]  J. Thies,et al.  Diversity of Planctomycetes in Soil in Relation to Soil History and Environmental Heterogeneity , 2006, Applied and Environmental Microbiology.

[60]  B. M. Gardener,et al.  Microbial populations responsible for specific soil suppressiveness to plant pathogens. , 2002, Annual review of phytopathology.

[61]  J. Kolasa,et al.  Contrasts between habitat generalists and specialists: an empirical extension to the basic metacommunity framework. , 2009, Ecology.

[62]  V. Chaudhry,et al.  Changes in Bacterial Community Structure of Agricultural Land Due to Long-Term Organic and Chemical Amendments , 2012, Microbial Ecology.

[63]  M. Tenuta,et al.  Ammonia and Nitrous Acid from Nitrogenous Amendments Kill the Microsclerotia of Verticillium dahliae. , 2002, Phytopathology.

[64]  T. Schmidt,et al.  Diversity and dynamics of microbial communities in soils from agro-ecosystems. , 2003, Environmental microbiology.

[65]  L. Biju-Duval,et al.  Microscale evidence for a high decrease of soil bacterial density and diversity by cropping , 2014, Agronomy for Sustainable Development.

[66]  Susan Holmes,et al.  phyloseq: An R Package for Reproducible Interactive Analysis and Graphics of Microbiome Census Data , 2013, PloS one.

[67]  Lynne A. Goodwin,et al.  Complete genome sequence of Chitinophaga pinensis type strain (UQM 2034T) , 2010, Standards in genomic sciences.

[68]  J. V. van Elsas,et al.  Chitin Amendment Increases Soil Suppressiveness toward Plant Pathogens and Modulates the Actinobacterial and Oxalobacteraceal Communities in an Experimental Agricultural Field , 2013, Applied and Environmental Microbiology.

[69]  C. Aita,et al.  Temporal variability of soil microbial communities after application of dicyandiamide-treated swine slurry and mineral fertilizers , 2016 .

[70]  Marti J. Anderson,et al.  Multivariate dispersion as a measure of beta diversity. , 2006, Ecology letters.

[71]  D. Faith,et al.  SYSTEMATICS AND CONSERVATION: ON PREDICTING THE FEATURE DIVERSITY OF SUBSETS OF TAXA , 1992, Cladistics : the international journal of the Willi Hennig Society.

[72]  J. D. Elsas,et al.  Bacterial communities in chitin-amended soil as revealed by 16S rRNA gene based pyrosequencing , 2014 .

[73]  M. Mazzola.  Assessment and management of soil microbial community structure for disease suppression. , 2004, Annual review of phytopathology.