Soil depth and geographic distance modulate bacterial β‐diversity in deep soil profiles throughout the U.S. Corn Belt

Understanding how microbial communities are shaped across spatial dimensions is of fundamental importance in microbial ecology. However, most studies on soil biogeography have focused on the topsoil microbiome, while the factors driving the subsoil microbiome distribution are largely unknown. Here we used 16S rRNA amplicon sequencing to analyse the factors underlying the bacterial β‐diversity along vertical (0–240 cm of soil depth) and horizontal spatial dimensions (~500,000 km2) in the U.S. Corn Belt. With these data we tested whether the horizontal or vertical spatial variation had stronger impacts on the taxonomic (Bray‐Curtis) and phylogenetic (weighted Unifrac) β‐diversity. Additionally, we assessed whether the distance‐decay (horizontal dimension) was greater in the topsoil (0–30 cm) or subsoil (in each 30 cm layer from 30–240 cm) using Mantel tests. The influence of geographic distance versus edaphic variables on the bacterial communities from the different soil layers was also compared. Results indicated that the phylogenetic β‐diversity was impacted more by soil depth, while the taxonomic β‐diversity changed more between geographic locations. The distance‐decay was lower in the topsoil than in all subsoil layers analysed. Moreover, some subsoil layers were influenced more by geographic distance than any edaphic variable, including pH. Although different factors affected the topsoil and subsoil biogeography, niche‐based models explained the community assembly of all soil layers. This comprehensive study contributed to elucidating important aspects of soil bacterial biogeography including the major impact of soil depth on the phylogenetic β‐diversity, and the greater influence of geographic distance on subsoil than on topsoil bacterial communities in agroecosystems.

[1]  Li‐Mei Zhang,et al.  Environmental selection dominates over dispersal limitation in shaping bacterial biogeographical patterns across different soil horizons of the Qinghai-Tibet Plateau. , 2022, The Science of the total environment.

[2]  Hongyi Li,et al.  Large-scale homogenization of soil bacterial communities in response to agricultural practices in paddy fields, China , 2022, Soil Biology and Biochemistry.

[3]  J. Lynch Harnessing root architecture to address global challenges , 2021, The Plant journal : for cell and molecular biology.

[4]  D. Schneider,et al.  The ubiquitous soil verrucomicrobial clade 'Candidatus Udaeobacter' shows preferences for acidic pH. , 2021, Environmental microbiology reports.

[5]  A. Arnold,et al.  Drivers and implications of distance decay differ for ectomycorrhizal and foliar endophytic fungi across an anciently fragmented landscape , 2021, The ISME Journal.

[6]  Naling Bai,et al.  Stochastic processes drive bacterial and fungal community assembly in sustainable intensive agricultural soils of Shanghai, China. , 2021, The Science of the total environment.

[7]  D. Schachtman,et al.  Alkaline soil pH affects bulk soil, rhizosphere and root endosphere microbiomes of plants growing in a Sandhills ecosystem. , 2021, FEMS microbiology ecology.

[8]  T. Kuyper,et al.  High microbial diversity stabilizes the responses of soil organic carbon decomposition to warming in the subsoil on the Tibetan Plateau , 2021, Global change biology.

[9]  H. Kauserud,et al.  Soil depth matters: shift in composition and inter-kingdom co-occurrence patterns of microorganisms in forest soils , 2021, FEMS microbiology ecology.

[10]  X. Peng,et al.  Bio-tillage: A new perspective for sustainable agriculture , 2021 .

[11]  A. Madsen,et al.  Gemmatimonas groenlandica sp. nov. Is an Aerobic Anoxygenic Phototroph in the Phylum Gemmatimonadetes , 2021, Frontiers in Microbiology.

[12]  Jasper J. Koehorst,et al.  A metabolic and physiological design study of Pseudomonas putida KT2440 capable of anaerobic respiration , 2021, BMC microbiology.

[13]  Ye Deng,et al.  Steeper spatial scaling patterns of subsoil microbiota are shaped by deterministic assembly process , 2020, Molecular ecology.

[14]  Raziel A. Ordóñez,et al.  The Effects of Soil Depth on the Structure of Microbial Communities in Agricultural Soils in Iowa (United States) , 2020, Applied and Environmental Microbiology.

[15]  Jinming Song,et al.  Responses of bacterial communities and their carbon dynamics to subsoil exposure on the Loess Plateau. , 2020, The Science of the total environment.

[16]  D. Kaftan,et al.  Utilization of light energy in phototrophic Gemmatimonadetes. , 2020, Journal of photochemistry and photobiology. B, Biology.

[17]  B. Singh,et al.  Crop microbiome and sustainable agriculture , 2020, Nature Reviews Microbiology.

[18]  W. Feng,et al.  Soil properties rather than climate and ecosystem type control the vertical variations of soil organic carbon, microbial carbon, and microbial quotient , 2020 .

[19]  D. Daffonchio,et al.  Direct quantification of ecological drift at the population level in synthetic bacterial communities , 2020, The ISME journal.

[20]  M. Delgado‐Baquerizo,et al.  Soil Microbial Biogeography in a Changing World: Recent Advances and Future Perspectives , 2020, mSystems.

[21]  K. Guan,et al.  Integrated assessment of crop production and resource use efficiency indicators for the U.S. Corn Belt , 2020 .

[22]  J. Heino,et al.  Community size can affect the signals of ecological drift and niche selection on biodiversity. , 2020, Ecology.

[23]  K. Totsche,et al.  Environmental selection shapes the formation of near-surface groundwater microbiomes. , 2019, Water research.

[24]  Yunfeng Yang,et al.  Balance between community assembly processes mediates species coexistence in agricultural soil microbiomes across eastern China , 2019, The ISME Journal.

[25]  William A. Walters,et al.  Reproducible, interactive, scalable and extensible microbiome data science using QIIME 2 , 2019, Nature Biotechnology.

[26]  Julia Fukuyama Emphasis on the deep or shallow parts of the tree provides a new characterization of phylogenetic distances , 2019, Genome Biology.

[27]  Agustín M. Pardo,et al.  Core regulon of the global anaerobic regulator Anr targets central metabolism functions in Pseudomonas species , 2019, Scientific Reports.

[28]  W. Silver,et al.  Ecological and Genomic Attributes of Novel Bacterial Taxa That Thrive in Subsurface Soil Horizons , 2019, mBio.

[29]  Wenhong Ma,et al.  Contrasting Biogeographic Patterns of Bacterial and Archaeal Diversity in the Top- and Subsoils of Temperate Grasslands , 2019, mSystems.

[30]  Qiaoping Li,et al.  Soil microbiomes with distinct assemblies through vertical soil profiles drive the cycling of multiple nutrients in reforested ecosystems , 2018, Microbiome.

[31]  Falk Hildebrand,et al.  Structure and function of the global topsoil microbiome , 2018, Nature.

[32]  E. Ivanova,et al.  Investigation of the core microbiome in main soil types from the East European plain. , 2018, The Science of the total environment.

[33]  P. Wincker,et al.  Biogeography of soil bacteria and archaea across France , 2018, Science Advances.

[34]  A. Martín-Platero,et al.  Diversity and antimicrobial potential in sea anemone and holothurian microbiomes , 2018, PloS one.

[35]  B. Bohannan,et al.  Why do microbes exhibit weak biogeographic patterns? , 2018, The ISME Journal.

[36]  Rick L. Stevens,et al.  A communal catalogue reveals Earth’s multiscale microbial diversity , 2017, Nature.

[37]  A. Don,et al.  Controlling factors for the stability of subsoil carbon in a Dystric Cambisol , 2017 .

[38]  N. Fierer Embracing the unknown: disentangling the complexities of the soil microbiome , 2017, Nature Reviews Microbiology.

[39]  D. Or,et al.  Biophysical processes supporting the diversity of microbial life in soil , 2017, FEMS microbiology reviews.

[40]  Sukhwan Yoon,et al.  Nitrous Oxide Reduction by an Obligate Aerobic Bacterium, Gemmatimonas aurantiaca Strain T-27 , 2017, Applied and Environmental Microbiology.

[41]  J. Lennon,et al.  A macroecological theory of microbial biodiversity , 2017, Nature Ecology &Evolution.

[42]  Paul J. McMurdie,et al.  Exact sequence variants should replace operational taxonomic units in marker-gene data analysis , 2017, The ISME Journal.

[43]  R. G. Taketani,et al.  The drivers underlying biogeographical patterns of bacterial communities in soils under sugarcane cultivation , 2017 .

[44]  J. Neufeld,et al.  Depth‐dependent influence of different land‐use systems on bacterial biogeography , 2017, FEMS microbiology ecology.

[45]  J. Gilbert,et al.  Genome reduction in an abundant and ubiquitous soil bacterium ‘Candidatus Udaeobacter copiosus’ , 2016, Nature Microbiology.

[46]  Dan Knights,et al.  Systematic improvement of amplicon marker gene methods for increased accuracy in microbiome studies , 2016, Nature Biotechnology.

[47]  Heather A Viles,et al.  The spatial organization and microbial community structure of an epilithic biofilm. , 2015, FEMS microbiology ecology.

[48]  Robert G. Beiko,et al.  STAMP: statistical analysis of taxonomic and functional profiles , 2014, Bioinform..

[49]  A. Plante,et al.  Changes in extracellular enzyme activity and microbial community structure with soil depth at the Luquillo Critical Zone Observatory , 2014 .

[50]  H. Chu,et al.  High throughput sequencing analysis of biogeographical distribution of bacterial communities in the black soils of northeast China , 2014 .

[51]  Diana R. Nemergut,et al.  Patterns and Processes of Microbial Community Assembly , 2013, Microbiology and Molecular Reviews.

[52]  Sarah L. Westcott,et al.  Development of a Dual-Index Sequencing Strategy and Curation Pipeline for Analyzing Amplicon Sequence Data on the MiSeq Illumina Sequencing Platform , 2013, Applied and Environmental Microbiology.

[53]  E. Zhang,et al.  Phylogenetic beta diversity in bacterial assemblages across ecosystems: deterministic versus stochastic processes , 2013, The ISME Journal.

[54]  B. Bohannan,et al.  Conversion of the Amazon rainforest to agriculture results in biotic homogenization of soil bacterial communities , 2012, Proceedings of the National Academy of Sciences.

[55]  Scott T. Bates,et al.  Cross-biome metagenomic analyses of soil microbial communities and their functional attributes , 2012, Proceedings of the National Academy of Sciences.

[56]  M. Roberts,et al.  Intercontinental Dispersal of Bacteria and Archaea by Transpacific Winds , 2012, Applied and Environmental Microbiology.

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

[58]  S. P. Anderson,et al.  Digging deeper to find unique microbial communities: The strong effect of depth on the structure of bacterial and archaeal communities in soil , 2012 .

[59]  J. Fuhrman,et al.  Beyond biogeographic patterns: processes shaping the microbial landscape , 2012, Nature Reviews Microbiology.

[60]  M. Silby,et al.  Pseudomonas genomes: diverse and adaptable. , 2011, FEMS microbiology reviews.

[61]  Thomas Bell,et al.  The bacterial biogeography of British soils. , 2011, Environmental microbiology.

[62]  S. Allison,et al.  Drivers of bacterial β-diversity depend on spatial scale , 2011, Proceedings of the National Academy of Sciences.

[63]  R. Knight,et al.  UniFrac: an effective distance metric for microbial community comparison , 2011, The ISME Journal.

[64]  T. Bell Experimental tests of the bacterial distance–decay relationship , 2010, The ISME Journal.

[65]  William A. Walters,et al.  Global patterns of 16S rRNA diversity at a depth of millions of sequences per sample , 2010, Proceedings of the National Academy of Sciences.

[66]  W. Wanek,et al.  Alternative methods for measuring inorganic, organic, and total dissolved nitrogen in soil. , 2010 .

[67]  Calvin Dytham,et al.  Relative roles of niche and neutral processes in structuring a soil microbial community , 2010, The ISME Journal.

[68]  W. Liesack,et al.  Bryobacter aggregatus gen. nov., sp. nov., a peat-inhabiting, aerobic chemo-organotroph from subdivision 3 of the Acidobacteria. , 2010, International journal of systematic and evolutionary microbiology.

[69]  R. Knight,et al.  Pyrosequencing-Based Assessment of Soil pH as a Predictor of Soil Bacterial Community Structure at the Continental Scale , 2009, Applied and Environmental Microbiology.

[70]  C. Graham,et al.  Phylogenetic beta diversity: linking ecological and evolutionary processes across space in time. , 2008, Ecology letters.

[71]  J. Rine,et al.  Serial Analysis of rRNA Genes and the Unexpected Dominance of Rare Members of Microbial Communities , 2007, Applied and Environmental Microbiology.

[72]  R. Knight,et al.  Quantitative and Qualitative β Diversity Measures Lead to Different Insights into Factors That Structure Microbial Communities , 2007, Applied and Environmental Microbiology.

[73]  James H. Brown,et al.  Microbial biogeography: putting microorganisms on the map , 2006, Nature Reviews Microbiology.

[74]  R. B. Jackson,et al.  The diversity and biogeography of soil bacterial communities. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[75]  P. Dixon VEGAN, a package of R functions for community ecology , 2003 .

[76]  J. Tiedje,et al.  Biogeography and Degree of Endemicity of Fluorescent Pseudomonas Strains in Soil , 2000, Applied and Environmental Microbiology.

[77]  H. Bozdogan Model selection and Akaike's Information Criterion (AIC): The general theory and its analytical extensions , 1987 .

[78]  R. H. Bray,et al.  DETERMINATION OF TOTAL, ORGANIC, AND AVAILABLE FORMS OF PHOSPHORUS IN SOILS , 1945 .

[79]  J. Bockheim,et al.  Soil horizon variation: A review , 2020 .

[80]  Edward W. Davis,et al.  Tropical soils are a reservoir for fluorescent Pseudomonas spp. biodiversity , 2018, Environmental microbiology.

[81]  S. Derenne,et al.  Disentangling interactions between microbial communities and roots in deep subsoil. , 2017, The Science of the total environment.

[82]  Jinsheng He,et al.  Comparing microbial carbon sequestration and priming in the subsoil versus topsoil of a Qinghai-Tibetan alpine grassland , 2017 .

[83]  E. Paul,et al.  Soil microbiology, ecology, and biochemistry , 2015 .

[84]  Eugene Rosenberg,et al.  Introduction to the Proteobacteria , 2004 .

[85]  A. Page Methods of soil analysis. Part 2. Chemical and microbiological properties. , 1982 .