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Environmental Filtering Process Has More Important Roles than Dispersal Limitation in Shaping Large-Scale Prokaryotic Beta Diversity Patterns of Grassland Soils

  • Soil Microbiology
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Abstract

Despite the utmost importance of microorganisms in maintaining ecosystem functioning and their ubiquitous distribution, our knowledge of the large-scale pattern of microbial diversity is limited, particularly in grassland soils. In this study, the microbial communities of 99 soil samples spanning over 3000 km across grassland ecosystems in northern China were investigated using high-throughput sequencing to analyze the beta diversity pattern and the underlying ecological processes. The microbial communities were dominated by Proteobacteria, Actinobacteria, Acidobacteria, Chloroflexi, and Planctomycetes across all the soil samples. Spearman’s correlation analysis indicated that climatic factors and soil pH were significantly correlated with the dominant microbial taxa, while soil microbial richness was positively linked to annual precipitation. The environmental divergence–dissimilarity relationship was significantly positive, suggesting the importance of environmental filtering processes in shaping soil microbial communities. Structural equation modeling found that the deterministic process played a more important role than the stochastic process on the pattern of soil microbial beta diversity, which supported the predictions of niche theory. Partial mantel test analysis have showed that the contribution of independent environmental variables has a significant effect on beta diversity, while independent spatial distance has no such relationship, confirming that the deterministic process was dominant in structuring soil microbial communities. Overall, environmental filtering process has more important roles than dispersal limitation in shaping microbial beta diversity patterns in the grassland soils.

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References

  1. Gaston KJ (2000) Global patterns in biodiversity. Nature 405(6783):220–227

    Article  CAS  PubMed  Google Scholar 

  2. Rohwer F, Seguritan V, Azam F, Knowlton N (2002) Diversity and distribution of coral-associated bacteria. Mar Ecol Prog Ser 243:1–10

    Article  Google Scholar 

  3. Green JL, Holmes AJ, Westoby M, Oliver I, Briscoe D, Dangerfield M et al (2004) Spatial scaling of microbial eukaryote diversity. Nature 432(7018):747–750

    Article  CAS  PubMed  Google Scholar 

  4. Reche I, Pulido-Villena E, Morales-Baquero R, Casamayor EO (2005) Does ecosystem size determine aquatic bacterial richness? Ecology 86(7):1715–1722

    Article  Google Scholar 

  5. MacArthur RH (1965) Patterns of species diversity. Biol Rev 40(4):510–533

    Article  Google Scholar 

  6. Tang Z, Fang J, Chi X, Yang Y, Ma W, Mohhamot A, Guo Z, Liu Y, Gaston KJ (2012) Geography, environment, and spatial turnover of species in China’s grasslands. Ecography 35(12):1103–1109

    Article  Google Scholar 

  7. Rodríguez P, Arita HT (2004) Beta diversity and latitude in North American mammals: testing the hypothesis of covariation. Ecography 27(5):547–556

    Article  Google Scholar 

  8. Qian H, Ricklefs RE (2007) A latitudinal gradient in large-scale beta diversity for vascular plants in North America. Ecol Lett 10(8):737–744

    Article  PubMed  Google Scholar 

  9. Soininen J, Lennon JJ, Hillebrand H (2007) A multivariate analysis of beta diversity across organisms and environments. Ecology 88(11):2830–2838

    Article  PubMed  Google Scholar 

  10. Kraft NJ, Comita LS, Chase JM, Sanders NJ, Swenson NG, Crist TO, Stegen JC, Vellend M, Boyle B, Anderson MJ (2011) Disentangling the drivers of β diversity along latitudinal and elevational gradients. Science 333(6050):1755–1758

    Article  CAS  PubMed  Google Scholar 

  11. Buckley LB, Jetz W (2008) Linking global turnover of species and environments. Proc Natl Acad Sci U S A 105(46):17836–17841

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Harrison S, Ross SJ, Lawton JH (1992) Beta diversity on geographic gradients in Britain. J Appl Ecol 61(1):151–158

    Article  Google Scholar 

  13. Qian H, Ricklefs RE, White PS (2005) Beta diversity of angiosperms in temperate floras of eastern Asia and eastern North America. Ecol Lett 8(1):15–22

    Article  Google Scholar 

  14. Graham CH, Moritz C, Williams SE (2006) Habitat history improves prediction of biodiversity in rainforest fauna. Proc Natl Acad Sci U S A 103(3):632–636

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. McKnight MW, White PS, McDonald RI, Lamoreux JF, Sechrest W, Ridgely RS et al (2007) Putting beta-diversity on the map: broad-scale congruence and coincidence in the extremes. PLoS Biol 5(10):e272

    Article  PubMed  PubMed Central  Google Scholar 

  16. Yan Y, Yang X, Tang Z (2013) Patterns of species diversity and phylogenetic structure of vascular plants on the Qinghai-Tibetan Plateau. Ecol Evol 3(13):4584–4595

    Article  PubMed  PubMed Central  Google Scholar 

  17. Prober SM, Leff JW, Bates ST, Borer ET, Firn J, Harpole WS, Lind EM, Seabloom EW, Adler PB, Bakker JD (2015) Plant diversity predicts beta but not alpha diversity of soil microbes across grasslands worldwide. Ecol Lett 18(1):85–95

    Article  PubMed  Google Scholar 

  18. Ranjard L, Dequiedt S, Chemidlin Prévost-Bouré N et al (2013) Turnover of soil bacterial diversity driven by wide-scale environmental heterogeneity. Nat Commun 4:1434

    Article  CAS  PubMed  Google Scholar 

  19. Chemidlin Prévost-Bouré N, Dequiedt S, Thioulouse J et al (2014) Similar processes but different environmental filters for soil bacterial and fungal community composition turnover on a broad spatial scale. PLoS One 9:e111667

    Article  PubMed  PubMed Central  Google Scholar 

  20. Powell JR, Karunaratne S, Campbell CD et al (2015) Deterministic processes vary during community assembly for ecologically dissimilar taxa. Nat Commun 6:8444

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. MacArthur RH, Wilson EO (1967) The theory of island biogeography. Princeton University Press, Princeton

    Google Scholar 

  22. Bell G (2001) Neutral macroecology. Science 293(5539):2413

    Article  CAS  PubMed  Google Scholar 

  23. Hubbell SP (2001) The unified neutral theory of biodiversity and biogeography. Princeton University Press, Princeton

    Google Scholar 

  24. Caruso T, Chan Y, Lacap DC, Lau MC, McKay CP, Pointing SB (2011) Stochastic and deterministic processes interact in the assembly of desert microbial communities on a global scale. ISME J 5(9):1406–1413

    Article  PubMed  PubMed Central  Google Scholar 

  25. Lebrija-Trejos E, Pérez-García EA, Meave JA, Bongers F, Poorter L (2010) Functional traits and environmental filtering drive community assembly in a species-rich tropical system. Ecology 91(2):386–398

    Article  PubMed  Google Scholar 

  26. Graham CH, Fine PV (2008) Phylogenetic beta diversity: linking ecological and evolutionary processes across space in time. Ecol Lett 11(12):1265–1277

    Article  PubMed  Google Scholar 

  27. Cavender‐Bares J, Kozak KH, Fine PV, Kembel SW (2009) The merging of community ecology and phylogenetic biology. Ecol Lett 12(7):693–715

    Article  PubMed  Google Scholar 

  28. Martiny JBH, Bohannan BJM, Brown JH, Colwell RK, Fuhrman JA, Green JL, Horner-Devine MC, Kane M, Krumins JA, Kuske CR, Morin PJ, Naeem S, Ovreas L, Reysenbach AL, Smith VH, Staley JT (2006) Microbial biogeography: putting microorganisms on the map. Nat Rev Microbiol 4(2):102–112

    Article  CAS  PubMed  Google Scholar 

  29. Fierer N (2008) Microbial biogeography: patterns in microbial diversity across space and time. Accessing uncultivated microorganisms: from the environment to organisms and genomes and back. ASM Press, Washington DC, pp 95–115

    Google Scholar 

  30. Schiaffino MR, Unrein F, Gasol JM, Massana R, Balagué V, Izaguirre I (2011) Bacterial community structure in a latitudinal gradient of lakes: the roles of spatial versus environmental factors. Freshw Biol 56(10):1973–1991

    Article  Google Scholar 

  31. Wang J, Shen J, Wu Y, Tu C, Soininen J, Stegen JC, He J, Liu X, Zhang L, Zhang E (2013) Phylogenetic beta diversity in bacterial assemblages across ecosystems: deterministic versus stochastic processes. ISME J 7(7):1310–1321

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Hu HW, Chen DL, He JZ (2015) Microbial regulation of terrestrial nitrous oxide formation: understanding the biological pathways for prediction of emission rates. FEMS Microbiol Rev. doi:10.1093/femsre/fuv021

    PubMed  Google Scholar 

  33. Fisk MC, Ruether KF, Yavitt JB (2003) Microbial activity and functional composition among northern peatland ecosystems. Soil Biol Biochem 35(4):591–602

    Article  CAS  Google Scholar 

  34. Fierer N, Breitbart M, Nulton J, Salamon P, Lozupone C, Jones R, Robeson M, Edwards RA, Felts B, Rayhawk S (2007) Metagenomic and small-subunit rRNA analyses reveal the genetic diversity of bacteria, archaea, fungi, and viruses in soil. Appl Environ Microb 73(21):7059–7066

    Article  CAS  Google Scholar 

  35. Hansel CM, Fendorf S, Jardine PM, Francis CA (2008) Changes in bacterial and archaeal community structure and functional diversity along a geochemically variable soil profile. Appl Environ Microb 74(5):1620–1633

    Article  CAS  Google Scholar 

  36. Fierer N, Leff JW, Adams BJ, Nielsen UN, Bates ST, Lauber CL, Owens S, Gilbert JA, Wall DH, Caporaso JG (2012) Cross-biome metagenomic analyses of soil microbial communities and their functional attributes. Proc Natl Acad Sci 109(52):21390–21395

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Wang JT, Cao P, Hu HW, Li J, Han LL, Zhang LM et al (2015) Altitudinal distribution patterns of soil bacterial and archaeal communities along Mt. Shegyla on the Tibetan Plateau. Microb Ecol 69(1):135–145

    Article  PubMed  Google Scholar 

  38. Zelenev VV, van Bruggen AHC, Semenov AM (2005) Short-term wavelike dynamics of bacterial populations in response to nutrient input from fresh plant residues. Microb Ecol 49(1):83–93

    Article  CAS  PubMed  Google Scholar 

  39. Kang L, Han X, Zhang Z, Sun OJ (2007) Grassland ecosystems in China: review of current knowledge and research advancement. Philos T R Soc B 362(1482):997–1008

    Article  Google Scholar 

  40. Sun H (2005) Ecosystems of China. Science Press, Beijing

    Google Scholar 

  41. McGill WB, Rutherford PM, Figueiredo CT & Arocena JM (2007) Total nitrogen. Soil sampling and methods of analysis, 2nd edn (Carter MR & Gregorich EG, eds), pp. 239–250. CRC press, Taylor and Francis Group, London, UK

  42. Cao P, Zhang L-M, Shen J-P, Zheng Y-M, Di HJ, He J-Z (2012) Distribution and diversity of archaeal communities in selected Chinese soils. FEMS Microbiol Ecol 80(1):146–158

    Article  CAS  PubMed  Google Scholar 

  43. Frank K, Beegle D, Denning J (1998) Phosphorus. In: Brown JR (ed) Recommended chemical soil test procedures for the North Central Region. NCR Publication No. 221. Missouri Agricultural Experiment Station, Columbia, pp 24–32

    Google Scholar 

  44. Warncke D, Brown JR (1998) Potassium and other basic cations. In: Brown JR (ed) Recommended chemical soil test procedures for the North Central Region. NCR Publication No. 221. Missouri Agricultural Experiment Station, Columbia, pp 33–39

    Google Scholar 

  45. Caporaso JG, Lauber CL, Walters WA, Berg-Lyons D, Lozupone CA, Turnbaugh PJ, Fierer N, Knight R (2011) Global patterns of 16S rRNA diversity at a depth of millions of sequences per sample. Proc Natl Acad Sci U S A 108(Supplement 1):4516–4522

    Article  CAS  PubMed  Google Scholar 

  46. Caporaso JG, Lauber CL, Walters WA, Berg-Lyons D, Huntley J, Fierer N, Owens SM, Betley J, Fraser L, Bauer M (2012) Ultra-high-throughput microbial community analysis on the Illumina HiSeq and MiSeq platforms. ISME J 6(8):1621–1624

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Pena AG, Goodrich JK, Gordon JI (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7(5):335–336

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Magoč T, Salzberg SL (2011) FLASH: fast length adjustment of short reads to improve genome assemblies. Bioinformatics 27(21):2957–2963

    Article  PubMed  PubMed Central  Google Scholar 

  49. Edgar RC (2013) UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nat Methods 10(10):996–998

    Article  CAS  PubMed  Google Scholar 

  50. Caporaso JG, Bittinger K, Bushman FD, DeSantis TZ, Andersen GL, Knight R (2010) PyNAST: a flexible tool for aligning sequences to a template alignment. Bioinformatics 26(2):266–267

    Article  CAS  PubMed  Google Scholar 

  51. Wang Q, Garrity GM, Tiedje JM, Cole JR (2007) Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microb 73(16):5261–5267

    Article  CAS  Google Scholar 

  52. McDonald D, Price MN, Goodrich J, Nawrocki EP, DeSantis TZ, Probst A, Andersen GL, Knight R, Hugenholtz P (2012) An improved Greengenes taxonomy with explicit ranks for ecological and evolutionary analyses of bacteria and archaea. ISME J 6(3):610–618

    Article  CAS  PubMed  Google Scholar 

  53. Hijmans RJ, Cameron SE, Parra JL, Jones PG, Jarvis A (2005) Very high resolution interpolated climate surfaces for global land areas. Int J Climatol 25(15):1965–1978

    Article  Google Scholar 

  54. Chase MW, Reveal JL (2009) A phylogenetic classification of the land plants to accompany APG III. Bot J Linn Soc 161(2):122–127

    Article  Google Scholar 

  55. Grace JB, Keeley JE (2006) A structural equation model analysis of postfire plant diversity in California shrublands. Ecol Appl 16(2):503–514

    Article  PubMed  Google Scholar 

  56. Portillo MC, Leff JW, Lauber CL, Fierer N (2013) Cell size distributions of soil bacterial and archaeal taxa. Appl Environ Microb 79(24):7610–7617

    Article  CAS  Google Scholar 

  57. Zhou X, Chen C, Wang Y (2012) Long-term exclusion of grazing increases soil microbial biomass but not diversity in a temperate grassland. Open J Soil Sci 2(4):364–371

    Article  Google Scholar 

  58. Garrity GM, Bell JA, Lilburn TG (2004) Taxonomic outline of the prokaryotes, release 5.0. Springer-Verlag, New York

    Google Scholar 

  59. Jones RT, Robeson MS, Lauber CL, Hamady M, Knight R, Fierer N (2009) A comprehensive survey of soil acidobacterial diversity using pyrosequencing and clone library analyses. ISME J 3(4):442–453

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  60. Lauber CL, Hamady M, Knight R, Fierer N (2009) Pyrosequencing-based assessment of soil pH as a predictor of soil bacterial community structure at the continental scale. Appl Environ Microb 75(15):5111–5120

    Article  CAS  Google Scholar 

  61. Rappe´ MS, Giovannoni SJ (2003) The uncultured microbial majority. Annu Rev Microbiol 57:369–394

    Article  PubMed  Google Scholar 

  62. Janssen PH (2006) Identifying the dominant soil bacterial taxa in libraries of 16S rRNA and 16S rRNA genes. Appl Environ Microb 72(3):1719–1728

    Article  CAS  Google Scholar 

  63. Fuerst JA (2005) Intracellular compartmentation in planctomycetes. Annu Rev Microbiol 59:299–328

    Article  CAS  PubMed  Google Scholar 

  64. Torsvik V, Goksøyr J, Daae FL (1990) High diversity in DNA of soil bacteria. Appl Environ Microb 56(3):782–787

    CAS  Google Scholar 

  65. Curtis TP, Sloan WT, Scannell JW (2002) Estimating prokaryotic diversity and its limits. Proc Natl Acad Sci U S A 99(16):10494–10499

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  66. Roesch LF, Fulthorpe RR, Riva A, Casella G, Hadwin AK, Kent AD, Daroub SH, Camargo FA, Farmerie WG, Triplett EW (2007) Pyrosequencing enumerates and contrasts soil microbial diversity. ISME J 1(4):283–290

    CAS  PubMed  PubMed Central  Google Scholar 

  67. Fierer N, Jackson RB (2006) The diversity and biogeography of soil bacterial communities. Proc Natl Acad Sci U S A 103(3):626–631

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  68. O’Brien EM, Field R, Whittaker RJ (2000) Climatic gradients in woody plant (tree and shrub) diversity: water-energy dynamics, residual variation, and topography. Oikos 89(3):588–600

    Article  Google Scholar 

  69. Field R, O’Brien EM, Whittaker RJ (2005) Global models for predicting woody plant richness from climate: development and evaluation. Ecology 86(9):2263–2277

    Article  Google Scholar 

  70. Dumbrell AJ, Nelson M, Helgason T, Dytham C, Fitter AH (2010) Relative roles of niche and neutral processes in structuring a soil microbial community. ISME J 4(3):337–345

    Article  PubMed  Google Scholar 

  71. Chesson S (2000) Mechanisms of maintenance of species diversity. Annu Rev Ecol Syst 31:343–366

    Article  Google Scholar 

  72. Chase JM, Leibold MA (2003) Ecological niches—linking classical and contemporary approaches. University of Chicago Press, Chicago

    Book  Google Scholar 

  73. Casamayor EO, Barberán A (2010) Global phylogenetic community structure and β-diversity patterns in surface bacterioplankton metacommunities. Aquat Microb Ecol 59:1–10

    Article  Google Scholar 

  74. Zinger L, Amaral-Zettler LA, Fuhrman JA, Horner-Devine MC, Huse SM, Welch DBM, Martiny JB, Sogin M, Boetius A, Ramette A (2011) Global patterns of bacterial beta-diversity in seafloor and seawater ecosystems. PLoS One 6(9):e24570

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  75. Wardle DA, Bardgett RD, Klironomos JN, Setälä H, Van Der Putten WH, Wall DH (2004) Ecological linkages between aboveground and belowground biota. Science 304(5677):1629–1633

    Article  CAS  PubMed  Google Scholar 

  76. Van Der Gast CJ, Ager D, Lilley AK (2008) Temporal scaling of bacterial taxa is influenced by both stochastic and deterministic ecological factors. Environ Microbiol 10(6):1411–1418

    Article  PubMed  Google Scholar 

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Acknowledgments

This work was supported by the Ministry of Science and Technology 2013CB956300 and Chinese Academy of Sciences (XDB15020200, STSN-21-02) and the Natural Science Foundation of China (41230857). We are very grateful to Peng Han, Liang Xiang, Dr. Jing Li, Prof. Baodong Chen, and Prof. Weiping Chen for their assistance in soil sampling and analyzing.

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Cao, P., Wang, JT., Hu, HW. et al. Environmental Filtering Process Has More Important Roles than Dispersal Limitation in Shaping Large-Scale Prokaryotic Beta Diversity Patterns of Grassland Soils. Microb Ecol 72, 221–230 (2016). https://doi.org/10.1007/s00248-016-0762-4

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