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Experimental Testing of Dispersal Limitation in Soil Bacterial Communities with a Propagule Addition Approach

  • Environmental Microbiology
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Abstract

The role of dispersal in the assembly of microbial communities remains contentious. This study tested the importance of dispersal limitation for the structuring of local soil bacterial communities using an experimental approach of propagule addition. Microbes extracted from soil pooled from samples collected at 20 localities across ~ 400 km in a temperate steppe were added to microcosms of local soils at three sites; the microcosms were then incubated in situ for 3 months. We then assessed the composition and diversity of bacterial taxa in the soils using 16S rRNA gene amplicon sequencing. The addition of the regional microbial pool did not cause significant changes in the overall composition or diversity of the total bacterial community, although a very small number of individual taxa may have been affected by the addition treatment. Our results suggest a negligible role of dispersal limitation in structuring soil bacterial communities in our study area.

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References

  1. Ricklefs RE, Schluter D (1993) Species diversity: regional and historical influences. In: Ricklefs RE, Schluter D (eds) Species diversity in ecological communities. University of Chicago Press, Chicago, pp 350–363

    Google Scholar 

  2. Vellend M (2010) Conceptual synthesis in community ecology. Q. Rev. Biol. 85:183–206. https://doi.org/10.1086/652373

    Article  PubMed  Google Scholar 

  3. Ricklefs RE (1987) Community diversity: relative roles of local and regional processes. Science 235:167–171. https://doi.org/10.1126/science.235.4785.167

    Article  CAS  PubMed  Google Scholar 

  4. Finlay BJ (2002) Global dispersal of free-living microbial eukaryote species. Science 296:1061–1063. https://doi.org/10.1126/science.1070710

    Article  CAS  PubMed  Google Scholar 

  5. Fenchel T, Finlay BJ (2004) The ubiquity of small species: patterns of local and global diversity. BioScience 54:777–784. https://doi.org/10.1641/0006-3568(2004)054[0777:TUOSSP]2.0.CO;2

  6. de Wit R, Bouvier T (2006) ‘Everything is everywhere, but, the environment selects’; what did baas Becking and Beijerinck really say? Environ. Microbiol. 8:755–758. https://doi.org/10.1111/j.1462-2920.2006.01017.x

    Article  PubMed  Google Scholar 

  7. O’Malley MA (2008) ‘Everything is everywhere: but the environment selects’: ubiquitous distribution and ecological determinism in microbial biogeography. Stud Hist Phil Biol Biomed Sci 39:314–325. https://doi.org/10.1016/j.shpsc.2008.06.005

    Article  Google Scholar 

  8. Nemergut DR, Schmidt SK, Fukami T, O'Neill SP, Bilinski TM, Stanish LF, Knelman JE, Darcy JL, Lynch RC, Wickey P, Ferrenberg S (2013) Patterns and processes of microbial community assembly. Microbiol. Mol. Biol. Rev. 77:342–356. https://doi.org/10.1128/mmbr.00051-12

    Article  PubMed  PubMed Central  Google Scholar 

  9. Hanson CA, Fuhrman JA, Horner-Devine MC, Martiny JBH (2012) Beyond biogeographic patterns: processes shaping the microbial landscape. Nat Rev Microbiol 10:497–506. https://doi.org/10.1038/nrmicro2795

    Article  CAS  PubMed  Google Scholar 

  10. 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, Øvreås L, Reysenbach A-L, Smith VH, Staley JT (2006) Microbial biogeography: putting microorganisms on the map. Nat Rev Microbiol 4:102–112. https://doi.org/10.1038/nrmicro1341

    Article  CAS  PubMed  Google Scholar 

  11. Papke RT, Ramsing NB, Bateson MM, Ward DM (2003) Geographical isolation in hot spring cyanobacteria. Environ. Microbiol. 5:650–659. https://doi.org/10.1046/j.1462-2920.2003.00460.x

    Article  CAS  PubMed  Google Scholar 

  12. Whitaker RJ, Grogan DW, Taylor JW (2003) Geographic barriers isolate endemic populations of hyperthermophilic archaea. Science 301:976–978. https://doi.org/10.1126/science.1086909

    Article  CAS  PubMed  Google Scholar 

  13. Yannarell AC, Triplett EW (2005) Geographic and environmental sources of variation in lake bacterial community composition. Appl. Environ. Microbiol. 71:227–239. https://doi.org/10.1128/aem.71.1.227-239.2005

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Green JL, Holmes AJ, Westoby M, Oliver I, Briscoe D, Dangerfield M, Gillings M, Beattie AJ (2004) Spatial scaling of microbial eukaryote diversity. Nature 432:747–750. https://doi.org/10.1038/nature03034

    Article  CAS  PubMed  Google Scholar 

  15. Reche I, Pulido-Villena E, Morales-Baquero R, Casamayor EO (2005) Does ecosystem size determine aquatic bacterial richness? Ecology 86:1715–1722. https://doi.org/10.1890/04-1587

    Article  Google Scholar 

  16. Caruso T, Chan Y, Lacap DC, Lau MCY, McKay CP, Pointing SB (2011) Stochastic and deterministic processes interact in the assembly of desert microbial communities on a global scale. ISME J 5:1406–1413. https://doi.org/10.1038/ismej.2011.21

    Article  PubMed  PubMed Central  Google Scholar 

  17. Ge Y, He J-z, Zhu Y-G, Zhang J-B, Xu Z, Zhang L-M, Zheng Y-M (2008) Differences in soil bacterial diversity: driven by contemporary disturbances or historical contingencies? ISME J 2:254–264. https://doi.org/10.1038/ismej.2008.2

    Article  CAS  PubMed  Google Scholar 

  18. Horner-Devine MC, Lage M, Hughes JB, Bohannan BJM (2004) A taxa–area relationship for bacteria. Nature 432:750–753. https://doi.org/10.1038/nature03073

    Article  CAS  PubMed  Google Scholar 

  19. Vos M, Velicer GJ (2008) Isolation by distance in the spore-forming soil bacterium Myxococcus xanthus. Curr. Biol. 18:386–391. https://doi.org/10.1016/j.cub.2008.02.050

    Article  CAS  PubMed  Google Scholar 

  20. Telford RJ, Vandvik V, Birks HJB (2006) Dispersal limitations matter for microbial morphospecies. Science 312:1015. https://doi.org/10.1126/science.1125669

    Article  CAS  PubMed  Google Scholar 

  21. van der Gucht K, Cottenie K, Muylaert K, Vloemans N, Cousin S, Declerck S, Jeppesen E, Conde-Porcuna J-M, Schwenk K, Zwart G, Degans H, Vyverman W, De Meester L (2007) The power of species sorting: local factors drive bacterial community composition over a wide range of spatial scales. Proc. Natl. Acad. Sci. U. S. A. 104:20404–20409. https://doi.org/10.1073/pnas.0707200104

    Article  PubMed  PubMed Central  Google Scholar 

  22. Ptacnik R, Andersen T, Brettum P, Lepistö L, Willén E (2010) Regional species pools control community saturation in lake phytoplankton. Proc. R. Soc. B 277:3755–3764. https://doi.org/10.1098/rspb.2010.1158

    Article  PubMed  PubMed Central  Google Scholar 

  23. Ryšánek D, Hrčková K, Škaloud P (2015) Global ubiquity and local endemism of free-living terrestrial protists: phylogeographic assessment of the streptophyte alga Klebsormidium. Environ. Microbiol. 17:689–698. https://doi.org/10.1111/1462-2920.12501

    Article  PubMed  Google Scholar 

  24. Chase JM, Myers JA (2011) Disentangling the importance of ecological niches from stochastic processes across scales. Philos. Trans. R. Soc. Lond. Ser. B Biol. Sci. 366:2351–2363. https://doi.org/10.1098/rstb.2011.0063

    Article  Google Scholar 

  25. Hao Y-Q, Zhao X-F, Zhang D-Y (2016) Field experimental evidence that stochastic processes predominate in the initial assembly of bacterial communities. Environ. Microbiol. 18:1730–1739. https://doi.org/10.1111/1462-2920.12858

    Article  CAS  PubMed  Google Scholar 

  26. Comte J, Lindström ES, Eiler A, Langenheder S (2014) Can marine bacteria be recruited from freshwater sources and the air? ISME J 8:2423–2430. https://doi.org/10.1038/ismej.2014.89

    Article  PubMed  PubMed Central  Google Scholar 

  27. Langenheder S, Székely AJ (2011) Species sorting and neutral processes are both important during the initial assembly of bacterial communities. ISME J 5:1086–1094. https://doi.org/10.1038/ismej.2010.207

    Article  PubMed  PubMed Central  Google Scholar 

  28. Bell T (2010) Experimental tests of the bacterial distance–decay relationship. ISME J 4:1357–1365. https://doi.org/10.1038/ismej.2010.77

    Article  PubMed  Google Scholar 

  29. Myers JA, Harms KE (2009) Seed arrival, ecological filters, and plant species richness: a meta-analysis. Ecol. Lett. 12:1250–1260. https://doi.org/10.1111/j.1461-0248.2009.01373.x

    Article  PubMed  Google Scholar 

  30. Spalding VM (1909) Distribution and movement of desert plants. Carnegie Institute of Washington, Washington, DC

    Google Scholar 

  31. Cornell HV, Harrison SP (2014) What are species pools and when are they important? Annu. Rev. Ecol. Evol. Syst. 45:45–67. https://doi.org/10.1146/annurev-ecolsys-120213-091759

    Article  Google Scholar 

  32. Foster BL, Tilman D (2003) Seed limitation and the regulation of community structure in oak savanna grassland. J. Ecol. 91:999–1007. https://doi.org/10.1046/j.1365-2745.2003.00830.x

    Article  Google Scholar 

  33. Germain RM, Strauss SY, Gilbert B (2017) Experimental dispersal reveals characteristic scales of biodiversity in a natural landscape. Proc. Natl. Acad. Sci. U. S. A. 114:4447–4452. https://doi.org/10.1073/pnas.1615338114

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Peña AG, Goodrich JK, Gordon JI, Huttley GA, Kelley ST, Knights D, Koenig JE, Ley RE, Lozupone CA, McDonald D, Muegge BD, Pirrung M, Reeder J, Sevinsky JR, Turnbaugh PJ, Walters WA, Widmann J, Yatsunenko T, Zaneveld J, Knight R (2010) QIIME allows analysis of high-throughput community sequencing data. Nat. Methods 7:335–336. https://doi.org/10.1038/nmeth.f.303

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Edgar RC, Haas BJ, Clemente JC, Quince C, Knight R (2011) UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27:2194–2200. https://doi.org/10.1093/bioinformatics/btr381

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Edgar RC (2013) UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nat. Methods 10:996–998. https://doi.org/10.1038/nmeth.2604

    Article  CAS  PubMed  Google Scholar 

  37. Quast C, Pruesse E, Yilmaz P, Gerken J, Schweer T, Yarza P, Peplies J, Glöckner FO (2013) The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res. 41:D590–D596. https://doi.org/10.1093/nar/gks1219

    Article  CAS  PubMed  Google Scholar 

  38. Zhang F-G, Zhang Q-G (2015) Patterns in species persistence and biomass production in soil microcosms recovering from a disturbance reject a neutral hypothesis for bacterial community assembly. PLoS One 10:e0126962. https://doi.org/10.1371/journal.pone.0126962

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Wertz S, Degrange V, Prosser JI, Poly F, Commeaux C, Freitag T, Guillaumaud N, Roux XL (2006) Maintenance of soil functioning following erosion of microbial diversity. Environ. Microbiol. 8:2162–2169. https://doi.org/10.1111/j.1462-2920.2006.01098.x

    Article  CAS  PubMed  Google Scholar 

  40. van Elsas JD, Chiurazzi M, Mallon CA, Elhottovā D, Krištůfek V, Salles JF (2012) Microbial diversity determines the invasion of soil by a bacterial pathogen. Proc. Natl. Acad. Sci. U. S. A. 109:1159–1164. https://doi.org/10.1073/pnas.1109326109

    Article  PubMed  PubMed Central  Google Scholar 

  41. Peter H, Beier S, Bertilsson S, Lindström ES, Langenheder S, Tranvik LJ (2011) Function-specific response to depletion of microbial diversity. ISME J 5:351–361. https://doi.org/10.1038/ismej.2010.119

    Article  CAS  PubMed  Google Scholar 

  42. Oksanen J, Blanchet FG, Kindt R, Legendre P, O'Hara RB, Simpson GL, Solymos P, Stevens MHH, Wagner H (2011) Vegan: community ecology package. R package version 1.17–8

  43. R Core Team (2014) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna

    Google Scholar 

  44. Bray JR, Curtis JT (1957) An ordination of the upland forest communities of southern Wisconsin. Ecol. Monogr. 27:325–349. https://doi.org/10.2307/1942268

    Article  Google Scholar 

  45. Anderson MJ (2001) A new method for non-parametric multivariate analysis of variance. Austral Ecol 26:32–46. https://doi.org/10.1111/j.1442-9993.2001.01070.pp.x

    Article  Google Scholar 

  46. Griffin DW (2007) Atmospheric movement of microorganisms in clouds of desert dust and implications for human health. Clin. Microbiol. Rev. 20:459–477. https://doi.org/10.1128/cmr.00039-06

    Article  PubMed  PubMed Central  Google Scholar 

  47. Perfumo A, Marchant R (2010) Global transport of thermophilic bacteria in atmospheric dust. Environ. Microbiol. Rep. 2:333–339. https://doi.org/10.1111/j.1758-2229.2010.00143.x

    Article  CAS  PubMed  Google Scholar 

  48. Bowers RM, Sullivan AP, Costello EK, Collett JL, Knight R, Fierer N (2011) Sources of bacteria in outdoor air across cities in the midwestern United States. Appl. Environ. Microbiol. 77:6350–6356. https://doi.org/10.1128/aem.05498-11

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Peter H, Hörtnagl P, Reche I, Sommaruga R (2014) Bacterial diversity and composition during rain events with and without Saharan dust influence reaching a high mountain lake in the Alps. Environ. Microbiol. Rep. 6:618–624. https://doi.org/10.1111/1758-2229.12175

    Article  PubMed  PubMed Central  Google Scholar 

  50. Zhang H, Zhu SD, John R, Li RH, Liu H, Ye Q (2017) Habitat filtering and exclusion of weak competitors jointly explain fern species assemblage along a light and water gradient. Sci. Rep. 7:298. https://doi.org/10.1038/s41598-017-00429-9

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Götzenberger L, de Bello F, Bråthen KA, Davison J, Dubuis A, Guisan A, Lepš J, Lindborg R, Moora M, Pärtel M, Pellissier L, Pottier J, Vittoz P, Zobel K, Zobel M (2012) Ecological assembly rules in plant communities—approaches, patterns and prospects. Biol. Rev. 87:111–127. https://doi.org/10.1111/j.1469-185X.2011.00187.x

    Article  PubMed  Google Scholar 

  52. Chen IC, Hsieh C-h, Kondoh M, Lin H-J, Miki T, Nakamura M, Ohgushi T, Urabe J, Yoshida T (2017) Filling the gaps in ecological studies of socioecological systems. Ecol. Res. 32:873–885. https://doi.org/10.1007/s11284-017-1521-9

    Article  Google Scholar 

  53. Fukami T (2015) Historical contingency in community assembly: integrating niches, species pools, and priority effects. Annu Rev Ecol Evol Syst 46:1–23. https://doi.org/10.1146/annurev-ecolsys-110411-160340

    Article  Google Scholar 

  54. Cho J-C, Tiedje JM (2000) Biogeography and degree of endemicity of fluorescent Pseudomonas strains in soil. Appl. Environ. Microbiol. 66:5448–5456. https://doi.org/10.1128/aem.66.12.5448-5456.2000

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  55. Morriën E, Hannula SE, Snoek LB, Helmsing NR, Zweers H, de Hollander M, Soto RL, Bouffaud M-L, Buée M, Dimmers W, Duyts H, Geisen S, Girlanda M, Griffiths RI, Jørgensen H-B, Jensen J, Plassart P, Redecker D, Schmelz RM, Schmidt O, Thomson BC, Tisserant E, Uroz S, Winding A, Bailey MJ, Bonkowski M, Faber JH, Martin F, Lemanceau P, de Boer W, van Veen JA, van der Putten WH (2017) Soil networks become more connected and take up more carbon as nature restoration progresses. Nat. Commun. 8:14349. https://doi.org/10.1038/ncomms14349

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  56. Calderón K, Spor A, Breuil M-C, Bru D, Bizouard F, Violle C, Barnard RL, Philippot L (2017) Effectiveness of ecological rescue for altered soil microbial communities and functions. ISME J 11:272–283. https://doi.org/10.1038/ismej.2016.86

    Article  CAS  PubMed  Google Scholar 

  57. Vannette RL, Fukami T, Wootton T (2014) Historical contingency in species interactions: towards niche-based predictions. Ecol. Lett. 17:115–124. https://doi.org/10.1111/ele.12204

    Article  PubMed  Google Scholar 

  58. Hesse E, O'Brien S, Tromas N, Bayer F, Luján AM, van Veen EM, Hodgson DJ, Buckling A, Klironomos J (2018) Ecological selection of siderophore-producing microbial taxa in response to heavy metal contamination. Ecol. Lett. 21:117–127. https://doi.org/10.1111/ele.12878

    Article  PubMed  Google Scholar 

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Funding

This study was funded by the National Natural Science Foundation of China (31700434, 31725006, and 31670376) and the 111 project (B13008). The 16S rRNA gene sequence data were deposited in the NCBI Sequence Read Archive under accession number SRP057046.

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Authors and Affiliations

  1. College of Life Sciences, Shanxi Normal University, Linfen, 041004, Shanxi, China

    Fen-Guo Zhang

  2. Department of Life Sciences, Imperial College London, Ascot, Berkshire, SL5 7PY, UK

    Thomas Bell

  3. State Key Laboratory of Earth Surface Processes and Resource Ecology and MOE Key Laboratory for Biodiversity Science and Ecological Engineering, College of Life Sciences, Beijing Normal University, Beijing, 100875, China

    Quan-Guo Zhang

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  1. Fen-Guo Zhang
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Zhang, FG., Bell, T. & Zhang, QG. Experimental Testing of Dispersal Limitation in Soil Bacterial Communities with a Propagule Addition Approach. Microb Ecol 77, 905–912 (2019). https://doi.org/10.1007/s00248-018-1284-z

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