Skip to main content

Temperature and Precipitation Drive Elevational Patterns of Microbial Beta Diversity in Alpine Grasslands

Abstract

Understanding the mechanisms underlying biodiversity patterns is a central issue in ecology, while how temperature and precipitation jointly control the elevational patterns of microbes is understudied. Here, we studied the effects of temperature, precipitation and their interactions on the alpha and beta diversity of soil archaea and bacteria in alpine grasslands along an elevational gradient of 4300–5200 m on the Tibetan Plateau. Alpha diversity was examined on the basis of species richness and evenness, and beta diversity was quantified with the recently developed metric of local contributions to beta diversity (LCBD). Typical alpine steppe and meadow ecosystems were distributed below and above 4850 m, respectively, which was consistent with the two main constraints of mean annual temperature (MAT) and mean annual precipitation (MAP). Species richness and evenness showed decreasing elevational patterns in archaea and nonsignificant or U-shaped patterns in bacteria. The LCBD of both groups exhibited significant U-shaped elevational patterns, with the lowest values occurring at 4800 m. For the three diversity metrics, soil pH was the primary explanatory variable in archaea, explaining over 20.1% of the observed variation, whereas vegetation richness, total nitrogen and the K/Al ratio presented the strongest effects on bacteria, with relative importance values of 16.1%, 12.5% and 11.6%, respectively. For the microbial community composition of both archaea and bacteria, the moisture index showed the dominant effect, explaining 17.6% of the observed variation, followed by MAT and MAP. Taken together, temperature and precipitation exerted considerable indirect effects on microbial richness and evenness through local environmental and energy supply-related variables, such as vegetation richness, whereas temperature exerted a larger direct influence on LCBD and the community composition. Our findings highlighted the profound influence of temperature and precipitation interactions on microbial beta diversity in alpine grasslands on the Tibetan Plateau.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

References

  1. 1.

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

    CAS  PubMed  Article  Google Scholar 

  2. 2.

    Rahbek C, Borregaard MK, Colwell RK et al (2019) Humboldt’s enigma: what causes global patterns of mountain biodiversity? Science 365:1108–1113

    CAS  PubMed  Article  Google Scholar 

  3. 3.

    Peters MK, Hemp A, Appelhans T et al (2019) Climate-land-use interactions shape tropical mountain biodiversity and ecosystem functions. Nature 568:88–92

    CAS  PubMed  Article  Google Scholar 

  4. 4.

    Zhou J, Deng Y, Shen L et al (2016) Temperature mediates continental-scale diversity of microbes in forest soils. Nat Commun 7:12083

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  5. 5.

    Tian J, Wu B, Chen H et al (2017) Patterns and drivers of fungal diversity along an altitudinal gradient on Mount Gongga, China. J Soils Sediments 17:2856–2865

    Article  Google Scholar 

  6. 6.

    Duclos TR, DeLuca WV, King DI (2019) Direct and indirect effects of climate on bird abundance along elevation gradients in the Northern Appalachian Mountains. Divers Distrib 25:1670–1683

    Article  Google Scholar 

  7. 7.

    Shen C, Gunina A, Luo Y et al (2020) Contrasting patterns and drivers of soil bacterial and fungal diversity across a mountain gradient. Environ Microbiol 22:3287–3301

    PubMed  Article  Google Scholar 

  8. 8.

    Price CA, Weitz JS, Savage VM et al (2012) Testing the metabolic theory of ecology. Ecol Lett 15:1465–1474

    PubMed  Article  Google Scholar 

  9. 9.

    Hurlbert AH, Stegen JC (2014) When should species richness be energy limited, and how would we know? Ecol Lett 17:401–413

    PubMed  Article  PubMed Central  Google Scholar 

  10. 10.

    Miyamoto Y, Nakano T, Hattori M et al (2014) The mid-domain effect in ectomycorrhizal fungi: range overlap along an elevation gradient on Mount Fuji, Japan. ISME J 8:1739–1746

    PubMed  PubMed Central  Article  Google Scholar 

  11. 11.

    Lennon JT, Aanderud ZT, Lehmkuhl BK et al (2012) Mapping the niche space of soil microorganisms using taxonomy and traits. Ecology 93:1867–1879

    PubMed  Article  PubMed Central  Google Scholar 

  12. 12.

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

    PubMed  Article  PubMed Central  Google Scholar 

  13. 13.

    Treves DS, Xia B, Zhou J et al (2003) A two-species test of the hypothesis that spatial isolation influences microbial diversity in soil. Microb Ecol 45:20–28

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  14. 14.

    McCain CM (2009) Global analysis of bird elevational diversity. Glob Ecol Biogeogr 18:346–360

    Article  Google Scholar 

  15. 15.

    Yeh CF, Soininen J, Teittinen A et al (2019) Elevational patterns and hierarchical determinants of biodiversity across microbial taxonomic scales. Mol Ecol 28:86–99

    PubMed  Article  PubMed Central  Google Scholar 

  16. 16.

    Hu A, Wang J, Sun H et al (2020) Mountain biodiversity and ecosystem functions: interplay between geology and contemporary environments. ISME J 14:931–944

    PubMed  PubMed Central  Article  Google Scholar 

  17. 17.

    McCain CM, Grytnes JA (2010) Elevational Gradients in Species Richness Encyclopedia of Life Sciences. John Wiley & Sons, Chichester

    Google Scholar 

  18. 18.

    Lanzen A, Epelde L, Blanco F et al (2016) Multi-targeted metagenetic analysis of the influence of climate and environmental parameters on soil microbial communities along an elevational gradient. Sci Rep 6:28257

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  19. 19.

    Frindte K, Pape R, Werner K et al (2019) Temperature and soil moisture control microbial community composition in an arctic-alpine ecosystem along elevational and micro-topographic gradients. ISME J 13:2031–2043

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  20. 20.

    Gorban AN, Pokidysheva LI, Smirnova EV et al (2011) Law of the Minimum Paradoxes. Bull Math Biol 73:2013–2044

    PubMed  Article  Google Scholar 

  21. 21.

    Kessler M, Kluge J, Hemp A et al (2011) A global comparative analysis of elevational species richness patterns of ferns. Glob Ecol Biogeogr 20:868–880

    Article  Google Scholar 

  22. 22.

    Wang Z, Luo T, Li R et al (2013) Causes for the unimodal pattern of biomass and productivity in alpine grasslands along a large altitudinal gradient in semi-arid regions. J Veg Sci 24:189–201

    Article  Google Scholar 

  23. 23.

    Nottingham AT, Fierer N, Turner BL et al (2018) Microbes follow Humboldt: temperature drives plant and soil microbial diversity patterns from the Amazon to the Andes. Ecology 99:2455–2466

    PubMed  Article  Google Scholar 

  24. 24.

    Singh D, Lee-Cruz L, Kim WS et al (2014) Strong elevational trends in soil bacterial community composition on Mt. Halla, South Korea. Soil Biol Biochem 68:140–149

    CAS  Article  Google Scholar 

  25. 25.

    Deshmukh A, Singh RA (2019) Whittaker biome-based framework to account for the impact of climate change on catchment behavior. Water Resour Res 55:11208–11224

    Article  Google Scholar 

  26. 26.

    Hijmans RJ, Cameron SE, Parra JL et al (2005) Very high resolution interpolated climate surfaces for global land areas. Int J Climatol 25:1965–1978

    Article  Google Scholar 

  27. 27.

    Fang J, Yoda K (1990) Climate and vegetation in China III water balance and distribution of vegetation. Ecol Res 5:9–23

    Article  Google Scholar 

  28. 28.

    Bremner JM (1960) Determination of nitrogen in soil by the Kjeldahl method. J Agr Sci 55:11–33

    CAS  Article  Google Scholar 

  29. 29.

    Shi Y, Li Y, Xiang X et al (2018) Spatial scale affects the relative role of stochasticity versus determinism in soil bacterial communities in wheat fields across the North China Plain. Microbiome 6:27

    PubMed  PubMed Central  Article  Google Scholar 

  30. 30.

    Yang Y, Fang X, Galy A et al (2016) Plateau uplift forcing climate change around 8.6 Ma on the northeastern Tibetan Plateau: evidence from an integrated sedimentary Sr record. Palaeogeogr Palaeoclimatol Palaeoecol 461:418–431

    Article  Google Scholar 

  31. 31.

    Nesbitt HW, Young GM (1982) Early proterozoic climates and plate motions inferred from major element chemistry of lutites. Nature 299:715–717

    CAS  Article  Google Scholar 

  32. 32.

    Caporaso JG, Lauber CL, Walters WA et al (2011) Global patterns of 16S rRNA diversity at a depth of millions of sequences per sample. Proc Natl Acad Sci USA 108:4516–4522

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  33. 33.

    Van den Hoecke S, Verhelst J, Vuylsteke M et al (2015) Analysis of the genetic diversity of influenza A viruses using next-generation DNA sequencing. BMC Genom 16:79

    Article  Google Scholar 

  34. 34.

    Li H, Handsaker B, Wysoker A et al (2009) The sequence alignment/map (SAM) format and SAMtools. Bioinformatics 25:2078–2079

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  35. 35.

    Cole JR, Wang Q, Cardenas E et al (2009) The Ribosomal Database Project: improved alignments and new tools for rRNA analysis. Nucleic Acids Res 37:D141–D145

    CAS  PubMed  Article  Google Scholar 

  36. 36.

    Wang J, Meier S, Soininen J et al (2017) Regional and global elevational patterns of microbial species richness and evenness. Ecography 40:393–402

    Article  Google Scholar 

  37. 37.

    Pielou EC (1966) Measurement of diversity in different types of biological collections. J Theor Biol 13:131–144

    Article  Google Scholar 

  38. 38.

    Legendre P, De Caceres M (2013) Beta diversity as the variance of community data: dissimilarity coefficients and partitioning. Ecol Lett 16:951–963

    PubMed  Article  Google Scholar 

  39. 39.

    Roberts FS (2019) Measurement of biodiversity: richness and evenness. Springer, Cham

    Google Scholar 

  40. 40.

    Jost L (2010) The relation between evenness and diversity. Diversity 2:207–232

    Article  Google Scholar 

  41. 41.

    Martiny JB, Eisen JA, Penn K et al (2011) Drivers of bacterial beta-diversity depend on spatial scale. Proc Natl Acad Sci USA 108:7850–7854

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  42. 42.

    Wang J, Wu Y, Jiang H et al (2008) High beta diversity of bacteria in the shallow terrestrial subsurface. Environ Microbiol 10:2537–2549

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  43. 43.

    Yamaoka K, Nakagawa T, Uno T (1978) Application of Akaikes information criterion (AIC) in evaluation of linear pharmacokinetic equations. J Pharmacokinet Pharmacodyn 6:165–175

    CAS  Article  Google Scholar 

  44. 44.

    Lawrence RL, Wood SD, Sheley RL (2006) Mapping invasive plants using hyperspectral imagery and Breiman Cutler classifications (RandomForest). Remote Sens Environ 100:356–362

    Article  Google Scholar 

  45. 45.

    Grace JB, Anderson TM, Olff H et al (2010) On the specification of structural equation models for ecological systems. Ecol Monog 80:67–87

    Article  Google Scholar 

  46. 46.

    Rosseel Y (2012) Lavaan: an R package for structural equation modeling. J Stat Softw 48:1–36

    Article  Google Scholar 

  47. 47.

    Tedersoo L, Bahram M, Polme S et al (2014) Global diversity and geography of soil fungi. Science 346:1256688

    PubMed  Article  CAS  PubMed Central  Google Scholar 

  48. 48.

    Bahram M, Hildebrand F, Forslund SK et al (2018) Structure and function of the global topsoil microbiome. Nature 560:233–237

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  49. 49.

    Zheng Y, Ji N, Wu B et al (2020) Climatic factors have unexpectedly strong impacts on soil bacterial β-diversity in 12 forest ecosystems. Soil Biol Biochem 142:107699

    CAS  Article  Google Scholar 

  50. 50.

    Looby CI, Martin PH (2020) Diversity and function of soil microbes on montane gradients: the state of knowledge in a changing world. FEMS Microbiol Ecol 96:fiaa122

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  51. 51.

    Yuan Y, Si G, Li W et al (2015) Altitudinal distribution of ammonia-oxidizing archaea and bacteria in alpine grassland soils along the south-facing slope of Nyqentangula mountains, central Tibetan Plateau. Geomicrobiol J 32:77–88

    CAS  Article  Google Scholar 

  52. 52.

    Singh D, Takahashi K, Park J et al (2016) Similarities and contrasts in the archaeal community of two Japanese mountains: Mt. Norikura compared to Mt. Fuji. Microb Ecol 71:428–441

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  53. 53.

    Shearer CA, Zelski SE, Raja HA et al (2015) Distributional patterns of freshwater ascomycetes communities along an Andes to Amazon elevational gradient in Peru. Biodivers Conserv 24:1877–1897

    Article  Google Scholar 

  54. 54.

    Wang J, Legendre P, Soininen J et al (2019) Temperature drives local contributions to beta diversity in mountain streams: stochastic and deterministic processes. Glob Ecol Biogeogr 29:420–432

    Article  Google Scholar 

  55. 55.

    Zhang Y, Cong J, Lu H et al (2015) Soil bacterial diversity patterns and drivers along an elevational gradient on Shennongjia Mountain, China. Microbiol Biotechnol 8:739–746

    Article  Google Scholar 

  56. 56.

    Sheng Y, Cong W, Yang L et al (2019) Forest soil fungal community elevational distribution pattern and their ecological assembly processes. Front Microbiol 10:02226

    Article  Google Scholar 

  57. 57.

    Brown JH (2001) Mammals on mountainsides: elevational patterns of diversity. Global Ecol Biogeogr 10:101–109

    Article  Google Scholar 

  58. 58.

    Hawkins BA, Field R, Cornell HV et al (2003) Energy, water, and broad-scale geographic patterns of species richness. Ecology 84:3105–3117

    Article  Google Scholar 

  59. 59.

    Jankowski JE, Ciecka AL, Meyer NY et al (2009) Beta diversity along environmental gradients: implications of habitat specialization in tropical montane landscapes. J Anim Ecol 78:315–327

    PubMed  Article  PubMed Central  Google Scholar 

  60. 60.

    Sundqvist MK, Sanders NJ, Wardle DA et al (2013) Community and ecosystem responses to elevational gradients: processes, mechanisms, and insights for global change. Annu Rev Ecol Evol Syst 44:261–280

    Article  Google Scholar 

  61. 61.

    Condit R, Engelbrecht BMJ, Pino D et al (2013) Species distributions in response to individual soil nutrients and seasonal drought across a community of tropical trees. Proc Natl Acad Sci USA 110:5064–5068

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  62. 62.

    Wang J, Pan F, Soininen J et al (2016) Nutrient enrichment modifies temperature-biodiversity relationships in large-scale field experiments. Nat Commun 7:13960

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  63. 63.

    Picazo F, Vilmi A, Aalto J et al (2020) Climate mediates continental scale patterns of stream microbial functional diversity. Microbiome 8:1–14

    Article  Google Scholar 

  64. 64.

    Yuan Y, Si G, Wang J et al (2014) Bacterial community in alpine grasslands along an altitudinal gradient on the Tibetan Plateau. FEMS Microbiol Ecol 87:121–132

    CAS  PubMed  Article  Google Scholar 

  65. 65.

    Shigyo N, Umeki K, Hirao T (2019) Plant functional diversity and soil properties control elevational diversity gradients of soil bacteria. FEMS Microbiol Ecol 95:fiz025

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  66. 66.

    Wang S, Bao X, Feng K et al (2021) Warming-driven migration of core microbiota indicates soil property changes at continental scale. Sci Bull 01:021

    Google Scholar 

  67. 67.

    Ma M, Collins SL, Du G (2020) Direct and indirect effects of temperature and precipitation on alpine seed banks in the Tibetan Plateau. Ecol Appl 30:e02096

    PubMed  Article  Google Scholar 

  68. 68.

    Peters MK, Hemp A, Appelhans T (2016) Predictors of elevational biodiversity gradients change from single taxa to the multi-taxa community level. Nat Commun 7:3736

    Google Scholar 

  69. 69.

    Jenerette GD, Scott RL, Huxman TE (2008) Whole ecosystem metabolic pulses following precipitation events. Funct Ecol 22:924–930

    Article  Google Scholar 

  70. 70.

    Chen Q, Niu B, Hu Y et al (2020) Warming and increased precipitation indirectly affect the composition and turnover of labile-fraction soil organic matter by directly affecting vegetation and microorganisms. Sci Total Environ 714:136787

    CAS  PubMed  Article  Google Scholar 

  71. 71.

    Rengel Z (2011) Soil pH, soil health and climate change. Springer-Verlag, Berlin

    Book  Google Scholar 

  72. 72.

    Shen C, Xiong J, Zhang H et al (2013) Soil pH drives the spatial distribution of bacterial communities along elevation on Changbai Mountain. Soil Biol Biochem 57:204–211

    CAS  Article  Google Scholar 

  73. 73.

    Shen C, Liang W, Shi Y et al (2014) Contrasting elevational diversity patterns between eukaryotic soil microbes and plants. Ecology 95:3190–3202

    Article  Google Scholar 

  74. 74.

    Siciliano SD, Palmer AS, Winsley T et al (2014) Soil fertility is associated with fungal and bacterial richness, whereas pH is associated with community composition in polar soil microbial communities. Soil Biol Biochem 78:10–20

    CAS  Article  Google Scholar 

  75. 75.

    Barcenas-Moreno G, Baath E, Rousk J (2016) Functional implications of the pH-trait distribution of the microbial community in a re-inoculation experiment across a pH gradient. Soil Biol Biochem 93:69–78

    CAS  Article  Google Scholar 

  76. 76.

    Bates ST, Berg-Lyons D, Caporaso JG et al (2011) Examining the global distribution of dominant archaeal populations in soil. ISME J 5:908–917

    CAS  PubMed  Article  Google Scholar 

  77. 77.

    Prescott CE, Grayston SJ (2013) Tree species influence on microbial communities in litter and soil: current knowledge and research needs. For Ecol Manag 309:19–27

    Article  Google Scholar 

  78. 78.

    Leff JW, Bardgett RD, Wilkinson A et al (2018) Predicting the structure of soil communities from plant community taxonomy, phylogeny, and traits. ISME J 12:1794–1805

    PubMed  PubMed Central  Article  Google Scholar 

  79. 79.

    Wang J, Wang Y, He N et al (2020) Plant functional traits regulate soil bacterial diversity across temperate deserts. Sci Total Environ 715:136976

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  80. 80.

    Delgado-Baquerizo M, Fry EL, Eldridge DJ et al (2018) Plant attributes explain the distribution of soil microbial communities in two contrasting regions of the globe. New Phytol 219:574–587

    PubMed  Article  PubMed Central  Google Scholar 

  81. 81.

    Vetaas OR, Paudel KP, Christensen M (2019) Principal factors controlling biodiversity along an elevation gradient: water, energy and their interaction. J Biogeogr 46:1652–1663

    Article  Google Scholar 

  82. 82.

    Santonja M, Rancon A, Fromin N et al (2017) Plant litter diversity increases microbial abundance, fungal diversity, and carbon and nitrogen cycling in a Mediterranean shrubland. Soil Biol Biochem 111:124–134

    CAS  Article  Google Scholar 

  83. 83.

    Delgado-Baquerizo M, Reich PB, Khachane AN et al (2017) It is elemental: soil nutrient stoichiometry drives bacterial diversity. Environ Microbiol 19:1176–1188

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  84. 84.

    Dini-Andreote F, Stegen JC, van Elsas JD et al (2015) Disentangling mechanisms that mediate the balance between stochastic and deterministic processes in microbial succession. Proc Natl Acad Sci USA 112:E1326–E1332

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  85. 85.

    Bryant JA, Lamanna C, Morlon H et al (2008) Microbes on mountainsides: contrasting elevational patterns of bacterial and plant diversity. Proc Natl Acad Sci USA 105:11505–11511

    CAS  PubMed  PubMed Central  Article  Google Scholar 

Download references

Acknowledgements

We are grateful to Conghai Han for soil sample collection.

Funding

This research was supported by grants from the Second Tibetan Plateau Scientific Expedition and Research Program (STEP) (2019QZKK0503), the National Natural Science Foundation of China (41871066, 41471055), the Strategic Priority Research Program (A) of the Chinese Academy of Sciences (XDA20050101).

Author information

Affiliations

Authors

Contributions

Xiaoqin Yang: conceptualization, investigation, validation, data analyzation, writing-original draft, writing-review & editing. Jianjun Wang: conceptualization, validation, formal analysis and methodology, writing-review & editing. Gengxin Zhang: supervision, resources, funding acquisition, conceptualization, validation, writing-review & editing. Yue Li: data analyzation. Yibo Yang: data curation, writing-review & editing. Bin Niu, Qiuyu Chen, Yilun Hu, Lili Song: writing-review & editing. All co-authors participated in discussions and revised the manuscript.

Corresponding authors

Correspondence to Jianjun Wang or Gengxin Zhang.

Ethics declarations

Conflict of Interest

The authors declare no competing interests.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 2869 KB)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Yang, X., Li, Y., Niu, B. et al. Temperature and Precipitation Drive Elevational Patterns of Microbial Beta Diversity in Alpine Grasslands. Microb Ecol (2021). https://doi.org/10.1007/s00248-021-01901-w

Download citation

Keywords

  • Soil microbes
  • Elevational gradient
  • Temperature
  • Precipitation
  • LCBD
  • Community composition