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Spatial Scaling Effects on Soil Bacterial Communities in Malaysian Tropical Forests

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Abstract

Spatial scaling to some extent determines biodiversity patterns in larger organisms, but its role in microbial diversity patterns is much less understood. Some studies have shown that bacterial community similarity decreases with distance, whereas others do not support this. Here, we studied soil bacterial communities of tropical rainforest in Malaysia at two spatial scales: a local scale with samples spaced every 5 m over a 150-m transect, and a regional scale with samples 1 to 1,800 km apart. PCR-amplified soil DNA for the bacterial 16S rRNA gene targeting the V1–V3 region was pyrosequenced using Roche/454 GS FLX Titanium platform. A ranked partial Mantel test showed a weak correlation between spatial distance and whole bacterial community dissimilarity, but only at the local scale. In contrast, environmental distance was highly correlated with community dissimilarity at both spatial scales, stressing the greater role of environmental variables rather than spatial distance in determining bacterial community variation at different spatial scales. Soil pH was the only environmental parameter that significantly explained the variance in bacterial community at the local scale, whereas total nitrogen and elevation were additional important factors at the regional scale. We obtained similar results at both scales when only the most abundant OTUs were analyzed. A variance partitioning analysis showed that environmental variables contributed more to bacterial community variation than spatial distance at both scales. In total, our results support a strong influence of the environment in determining bacterial community composition in the rainforests of Malaysia. However, it is possible that the remaining spatial distance effect is due to some of the myriad of other environmental factors which were not considered here, rather than dispersal limitation.

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References

  1. Huston MA (1994) Biological diversity: the coexistence of species on changing landscapes. Cambridge University Press, Cambridge, p 708

    Google Scholar 

  2. Bell G (2001) Ecology - neutral macroecology. Science 293(5539):2413–2418

    Article  CAS  PubMed  Google Scholar 

  3. Condit R, Pitman N, Leigh EG, Chave J, Terborgh J, Foster RB, Nunez P, Aguilar S, Valencia R, Villa G, Muller-Landau HC, Losos E, Hubbell SP (2002) Beta-diversity in tropical forest trees. Science 295(5555):666–669

    Article  CAS  PubMed  Google Scholar 

  4. Koleff P, Lennon JJ, Gaston KJ (2003) Are there latitudinal gradients in species turnover? Glob Ecol Biogeogr 12(6):483–498

    Article  Google Scholar 

  5. 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 

  6. Green J, Bohannan BJM (2006) Spatial scaling of microbial biodiversity. Trends Ecol Evol 21(9):501–507

    Article  PubMed  Google Scholar 

  7. 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 

  8. Nemergut DR, Costello EK, Hamady M, Lozupone C, Jiang L, Schmidt SK, Fierer N, Townsend AR, Cleveland CC, Stanish L, Knight R (2011) Global patterns in the biogeography of bacterial taxa. Environ Microbiol 13(1):135–144

    Article  PubMed  Google Scholar 

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

    PubMed Central  CAS  PubMed  Google Scholar 

  10. Bardgett RD, Freeman C, Ostle NJ (2008) Microbial contributions to climate change through carbon cycle feedbacks. ISME J 2(8):805–814

    Article  CAS  PubMed  Google Scholar 

  11. Baas-Becking LGM (1934) Geobiologie of inleiding tot de milieukunde. Van Stockum WP & Zoon NV, The Hague

    Google Scholar 

  12. Franklin RB, Mills AL (2003) Multi-scale variation in spatial heterogeneity for microbial community structure in an eastern Virginia agricultural field. FEMS Microbiol Ecol 44(3):335–346

    Article  CAS  PubMed  Google Scholar 

  13. Cho JC, Tiedje JM (2000) Biogeography and degree of endemicity of fluorescent Pseudomonas strains in soil. Appl Environ Microbiol 66(12):5448–5456

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  14. Horner-Devine MC, Lage M, Hughes JB, Bohannan BJ (2004) A taxa–area relationship for bacteria. Nature 432(7018):750–753

    Article  CAS  PubMed  Google Scholar 

  15. 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  PubMed Central  CAS  PubMed  Google Scholar 

  16. Angel R, Soares MIM, Ungar ED, Gillor O (2010) Biogeography of soil archaea and bacteria along a steep precipitation gradient. ISME J 4(4):553–563

    Article  PubMed  Google Scholar 

  17. Rousk J, Baath E, Brookes PC, Lauber CL, Lozupone C, Caporaso JG, Knight R, Fierer N (2010) Soil bacterial and fungal communities across a pH gradient in an arable soil. ISME J 4(10):1340–1351

    Article  PubMed  Google Scholar 

  18. Griffiths RI, Thomson BC, James P, Bell T, Bailey M, Whiteley AS (2011) The bacterial biogeography of British soils. Environ Microbiol 13(6):1642–1654

    Article  PubMed  Google Scholar 

  19. Tripathi BM, Kim M, Singh D, Lee-Cruz L, Lai-Hoe A, Ainuddin A, Go R, Rahim RA, Husni M, Chun J (2012) Tropical soil bacterial communities in Malaysia: pH dominates in the equatorial tropics too. Microb Ecol 64(2):474–484

    Article  PubMed  Google Scholar 

  20. 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 Microbiol 75(15):5111–5120

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  21. 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(7018):747–750

    Article  CAS  PubMed  Google Scholar 

  22. Telford RJ, Vandvik V, Birks HJB (2006) Dispersal limitations matter for microbial morphospecies. Science 312(5776):1015–1015

    Article  CAS  PubMed  Google Scholar 

  23. Chytrý M, Lososová Z, Horsák M, Uher B, Čejka T, Danihelka J, Fajmon K, Hájek O, Juřičková L, Kintrová K (2012) Dispersal limitation is stronger in communities of microorganisms than macroorganisms across Central European cities. J Biogeogr 39(6):1101–1111

    Article  Google Scholar 

  24. Myers N (1988) Threatened biotas: “hot spots” in tropical forests. Environmentalist 8(3):187–208

    Article  CAS  PubMed  Google Scholar 

  25. McGregor GR, Nieuwolt S (1998) Tropical climatology: an introduction to the clmates of the low latitudes, 2nd edn. Wiley, Chichester

    Google Scholar 

  26. Walsh RPD, Newbery DM (1999) The ecoclimatology of Danum, Sabah, in the context of the world’s rainforest regions, with particular reference to dry periods and their impact. Phil Trans R Soc B-Biol Sci 354(1391):1869–1883

    Article  CAS  Google Scholar 

  27. Chun J, Kim KY, Lee JH, Choi Y (2010) The analysis of oral microbial communities of wild-type and toll-like receptor 2-deficient mice using a 454 GS FLX titanium pyrosequencer. BMC Microbiol 10:101

    Article  PubMed Central  PubMed  Google Scholar 

  28. Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB, Lesniewski RA, Oakley BB, Parks DH, Robinson CJ, Sahl JW, Stres B, Thallinger GG, Van Horn DJ, Weber CF (2009) Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 75(23):7537–7541

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  29. Kim OS, Cho YJ, Lee K, Yoon SH, Kim M, Na H, Park SC, Jeon YS, Lee JH, Yi H, Won S, Chun J (2012) Introducing EzTaxon-e: a prokaryotic 16S rRNA gene sequence database with phylotypes that represent uncultured species. Int J Syst Evol Microbiol 62:716–721

    Article  CAS  PubMed  Google Scholar 

  30. Huse SM, Welch DM, Morrison HG, Sogin ML (2010) Ironing out the wrinkles in the rare biosphere through improved OTU clustering. Environ Microbiol 12(7):1889–1898

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  31. Edgar RC, Haas BJ, Clemente JC, Quince C, Knight R (2011) UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27(16):2194–2200

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  32. Logares R, Lindström ES, Langenheder S, Logue JB, Paterson H, Laybourn-Parry J, Rengefors K, Tranvik L, Bertilsson S (2013) Biogeography of bacterial communities exposed to progressive long-term environmental change. ISME J 7:937–948

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  33. Oksanen J, Kindt R, Legendre P, O’Hara B, Stevens MHH, Oksanen MJ, Suggests M (2007) Vegan: community ecology package. R package version 1.8-5. http://cran.r-project.org/ (accessed 10 April 2007)

  34. Goslee SC, Urban DL (2007) The ecodist package for dissimilarity-based analysis of ecological data. J Stat Softw 22(7):1–19

    Article  Google Scholar 

  35. Legendre P, Lapointe FJ, Casgrain P (1994) Modeling brain evolution from behavior — a permutational regression approach. Evolution 48(5):1487–1499

    Article  Google Scholar 

  36. Peres-Neto PR, Legendre P, Dray S, Borcard D (2006) Variation partitioning of species data matrices: estimation and comparison of fractions. Ecology 87(10):2614–2625

    Article  PubMed  Google Scholar 

  37. Borcard D, Legendre P (2002) All-scale spatial analysis of ecological data by means of principal coordinates of neighbour matrices. Ecol Model 153(1):51–68

    Article  Google Scholar 

  38. Borcard D, Legendre P, Avois-Jacquet C, Tuomisto H (2004) Dissecting the spatial structure of ecological data at multiple scales. Ecology 85(7):1826–1832

    Article  Google Scholar 

  39. Blanchet FG, Legendre P, Borcard D (2008) Forward selection of explanatory variables. Ecology 89(9):2623–2632

    Article  PubMed  Google Scholar 

  40. Wagner HH (2004) Direct multi-scale ordination with canonical correspondence analysis. Ecology 85(2):342–351

    Article  Google Scholar 

  41. R Core Team (2012) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna

    Google Scholar 

  42. Pasternak Z, Al-Ashhab A, Gatica J, Gafny R, Avraham S, Minz D, Gillor O, Jurkevitch E (2013) Spatial and temporal biogeography of soil microbial communities in arid and semiarid regions. Plos One 8(7):e69705

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  43. Martiny JB, Eisen JA, Penn K, Allison SD, Horner-Devine MC (2011) Drivers of bacterial beta-diversity depend on spatial scale. Proc Natl Acad Sci U S A 108(19):7850–7854

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  44. Gilbert B, Lechowicz MJ (2004) Neutrality, niches, and dispersal in a temperate forest understory. Proc Natl Acad Sci U S A 101(20):7651–7656

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  45. Campbell BJ, Polson SW, Hanson TE, Mack MC, Schuur EA (2010) The effect of nutrient deposition on bacterial communities in Arctic tundra soil. Environ Microbiol 12(7):1842–1854

    Article  CAS  PubMed  Google Scholar 

  46. Wessén E, Hallin S, Philippot L (2010) Differential responses of bacterial and archaeal groups at high taxonomical ranks to soil management. Soil Biol Biochem 42(10):1759–1765

    Article  Google Scholar 

  47. Singh D, Takahashi K, Kim M, Chun J, Adams JM (2012) A hump-backed trend in bacterial diversity with elevation on Mount Fuji, Japan. Microb Ecol 63(2):429–437

    Article  PubMed  Google Scholar 

  48. 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  PubMed Central  CAS  PubMed  Google Scholar 

  49. Pedrós-Alió C (2006) Marine microbial diversity: can it be determined? Trends Microbiol 14(6):257–263

    Article  PubMed  Google Scholar 

  50. Chesson PL, Warner RR (1981) Environmental variability promotes coexistence in lottery competitive-systems. Am Nat 117(6):923–943

    Article  Google Scholar 

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

    Google Scholar 

  52. Tuomisto H, Ruokolainen K, Yli-Halla M (2003) Dispersal, environment, and floristic variation of western Amazonian forests. Science 299(5604):241–244

    Article  CAS  PubMed  Google Scholar 

  53. Oh YM, Kim M, Lee-Cruz L, Lai-Hoe A, Go R, Ainuddin N, Rahim RA, Shukor N, Adams JM (2012) Distinctive bacterial communities in the rhizoplane of four tropical tree species. Microb Ecol 64(4):1018–1027

    Article  PubMed  Google Scholar 

  54. Morley RJ (2000) Origin and evolution of tropical rainforests. Wiley, Chichester

    Google Scholar 

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Acknowledgments

Jonathan Adams was funded by a Brain Gain grant from the Government of Malaysia and by an SNU New Faculty Research Grant. This work was partly supported by a grant from the National Research Foundation (NRF) grant funded by the Korean government, Ministry of Education, Science and Technology (MEST) (NRF-2013-031400). We are grateful to the anonymous reviewers for their help in improving the manuscript.

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Correspondence to Jonathan M. Adams.

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Tripathi, B.M., Lee-Cruz, L., Kim, M. et al. Spatial Scaling Effects on Soil Bacterial Communities in Malaysian Tropical Forests. Microb Ecol 68, 247–258 (2014). https://doi.org/10.1007/s00248-014-0404-7

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