Trends in Taxonomic and Functional Composition of Soil Microbiome Along a Precipitation Gradient in Israel

Abstract

The soil microbiome is important for the functioning of terrestrial ecosystems. However, the impacts of climate on taxonomic and functional diversity of soil microbiome are not well understood. A precipitation gradient along regional scale transects may offer a model setting for understanding the effect of climate on the composition and function of the soil microbiome. Here, we compared taxonomic and functional attributes of soil microorganisms in arid, semiarid, Mediterranean, and humid Mediterranean climatic conditions of Israel using shotgun metagenomic sequencing. We hypothesized that there would be a distinct taxonomic and functional soil community for each precipitation zone, with arid environments having lower taxonomic and functional diversity, greater relative abundance of stress response and sporulation-related genes, and lower relative abundance of genes related to nutrient cycling and degradation of complex organic compounds. As hypothesized, our results showed a distinct taxonomic and functional community in each precipitation zone, revealing differences in soil taxonomic and functional selection in the different climates. Although the taxonomic diversity remained similar across all sites, the functional diversity was—as hypothesized—lower in the arid environments, suggesting that functionality is more constrained in “extreme” environments. Also, with increasing aridity, we found a significant increase in genes related to dormancy/sporulation and a decrease in those related to nutrient cycling (genes related to nitrogen, potassium, and sulfur metabolism), respectively. However, relative abundance of genes related to stress response were lower in arid soils. Overall, these results indicate that climatic conditions play an important role in shaping taxonomic and functional attributes of soil microbiome. These findings have important implications for understanding the impacts of climate change (e.g., precipitation change) on structure and function of the soil microbiome.

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

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

References

  1. 1.

    Torsvik V, Ovreas L (2002) Microbial diversity and function in soil: from genes to ecosystems. Curr. Opin. Microbiol. 5:240–245

    CAS  Article  PubMed  Google Scholar 

  2. 2.

    Zeller B, Liu J, Buchmann N, Richter A (2008) Tree girdling increases soil N mineralisation in two spruce stands. Soil Biol. Biochem. 40(5):1155–1166

    CAS  Article  Google Scholar 

  3. 3.

    Herman DJ, Firestone MK, Nuccio E, Hodge A (2012) Interactions between an arbuscular mycorrhizal fungus and a soil microbial community mediating litter decomposition. FEMS Microbiol. Ecol. 80(1):236–247

    CAS  Article  PubMed  Google Scholar 

  4. 4.

    Cotrufo MF, Wallenstein MD, Boot CM, Denef K, Paul E (2013) The Microbial Efficiency-Matrix Stabilization (MEMS) framework integrates plant litter decomposition with soil organic matter stabilization: do labile plant inputs form stable soil organic matter? Glob Change Biol 19(4):988–995

    Article  Google Scholar 

  5. 5.

    Staddon WJ, Trevors JT, Duchesne LC (1998) Soil microbial diversity and community structure across a climatic gradient in western Canada. Biodivers. Conserv. 7(8):1081–1092

    Article  Google Scholar 

  6. 6.

    Smith JL, Halvorson JJ, Bolton H (2002) Soil properties and microbial activity across a 500 m elevation gradient in a semi-arid environment. Soil Biol. Biochem. 34(11):1749–1757

    CAS  Article  Google Scholar 

  7. 7.

    Habekost M, Eisenhauer N, Scheu S, Steinbeiss S, Weigelt A, Gleixner G (2008) Seasonal changes in the soil microbial community in a grassland plant diversity gradient four years after establishment. Soil Biol. Biochem. 40(10):2588–2595

    CAS  Article  Google Scholar 

  8. 8.

    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 

  9. 9.

    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

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  10. 10.

    Burke C, Steinberg P, Rusch D, Kjelleberg S, Thomas T (2011) Bacterial community assembly based on functional genes rather than species. Proc. Natl. Acad. Sci. U. S. A. 108(34):14288–14293

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  11. 11.

    Krause S, Le Roux X, Niklaus PA, Van Bodegom PM, Lennon JT, Bertilsson S, Grossart HP, Philippot L, Bodelier PL (2014) Trait-based approaches for understanding microbial biodiversity and ecosystem functioning. Front. Microbiol. 5:251

    Article  PubMed  PubMed Central  Google Scholar 

  12. 12.

    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. U. S. A. 109(52):21390–21395

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  13. 13.

    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

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  14. 14.

    Tripathi BM, Kim M, Tateno R, Kim W, Wang J, Lai-Hoe A, Shukor NAA, Rahim RA, Go R, Adams JM (2015) Soil pH and biome are both key determinants of soil archaeal community structure. Soil Biol. Biochem. 88:1–8

    CAS  Article  Google Scholar 

  15. 15.

    Tripathi BM, Edwards DP, Mendes LW, Kim M, Dong K, Kim H, Adams JM (2016) The impact of tropical forest logging and oil palm agriculture on the soil microbiome. Mol. Ecol. 25(10):2244–2257

    CAS  Article  PubMed  Google Scholar 

  16. 16.

    Navarrete AA, Tsai SM, Mendes LW, Faust K, de Hollander M, Cassman NA, Raes J, van Veen JA, Kuramae EE (2015) Soil microbiome responses to the short-term effects of Amazonian deforestation. Mol. Ecol. 24(10):2433–2448

    CAS  Article  PubMed  Google Scholar 

  17. 17.

    Mendes LW, Tsai SM, Navarrete AA, de Hollander M, van Veen JA, Kuramae EE (2015) Soil-borne microbiome: linking diversity to function. Microb. Ecol. 70(1):255–265

    CAS  Article  PubMed  Google Scholar 

  18. 18.

    Le Houérou HN (1996) Climate change, drought and desertification. J. Arid Environ. 34(2):133–185

    Article  Google Scholar 

  19. 19.

    Fleischer A, Sternberg M (2006) The economic impact of global climate change on Mediterranean rangeland ecosystems: a space-for-time approach. Ecol. Econ. 59(3):287–295

    Article  Google Scholar 

  20. 20.

    Sternberg M, Fleischer A, Holzapfel C, Jeltsch F, Lavee H, Kigel J, Tielbörger K, Köchy M, Sarah P (2011) The use and misuse of climatic gradients for evaluating climate impact on dryland ecosystems—an example for the solution of conceptual problems. In: Blanco J, Kheradmand H (eds) Climate change-geophysical foundations and ecological effects. InTech, Rijeka, pp. 361–374

    Google Scholar 

  21. 21.

    Kleidon A, Mooney HA (2000) A global distribution of biodiversity inferred from climatic constraints: results from a process-based modelling study. Glob Change Biol 6(5):507–523

    Article  Google Scholar 

  22. 22.

    Manzoni S, Schimel JP, Porporato A (2012) Responses of soil microbial communities to water stress: results from a meta-analysis. Ecology 93(4):930–938

    Article  PubMed  Google Scholar 

  23. 23.

    Grandy AS, Neff JC (2008) Molecular C dynamics downstream: the biochemical decomposition sequence and its impact on soil organic matter structure and function. Sci. Total Environ. 404(2):297–307

    CAS  Article  PubMed  Google Scholar 

  24. 24.

    Evenari M, Shanan L, Tadmor N (1982) The Negev: the challenge of a desert. Harvard University Press, Cambridge

    Google Scholar 

  25. 25.

    Rowell DL (2014) Soil science: methods and applications. Routledge, New York, USA

    Google Scholar 

  26. 26.

    Meyer F, Paarmann D, D’Souza M, Olson R, Glass EM, Kubal M, Paczian T, Rodriguez A, Stevens R, Wilke A (2008) The metagenomics RAST server—a public resource for the automatic phylogenetic and functional analysis of metagenomes. BMC Bioinformatics 9(1):386

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  27. 27.

    Oksanen J, Blanchet F, Kindt R, Legendre P, O’Hara R, Simpson G, Solymos P, Stevens M, Wagner H (2013) Vegan: community ecology package. R package version 2:3–2 Available at http://cran.r-project.org/web/packages/vegan/index.html

    Google Scholar 

  28. 28.

    R Development CoreTeam (2008) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria

  29. 29.

    Sherman C, Steinberger Y (2012) Microbial functional diversity associated with plant litter decomposition along a climatic gradient. Microbial Ecol 64(2):399–415

    CAS  Article  Google Scholar 

  30. 30.

    Sherman C, Grishkan I, Barness G, Steinberger Y (2014) Fungal community-plant litter decomposition relationships along a climate gradient. Pedosphere 24(4):437–449

    Article  Google Scholar 

  31. 31.

    Oren A, Steinberger Y (2008) Catabolic profiles of soil fungal communities along a geographic climatic gradient in Israel. Soil Biol. Biochem. 40(10):2578–2587

    CAS  Article  Google Scholar 

  32. 32.

    Bell CW, Acosta-Martinez V, McIntyre NE, Cox S, Tissue DT, Zak JC (2009) Linking microbial community structure and function to seasonal differences in soil moisture and temperature in a Chihuahuan desert grassland. Microb. Ecol. 58(4):827–842

    CAS  Article  PubMed  Google Scholar 

  33. 33.

    Brockett BF, Prescott CE, Grayston SJ (2012) Soil moisture is the major factor influencing microbial community structure and enzyme activities across seven biogeoclimatic zones in western Canada. Soil Biol. Biochem. 44(1):9–20

    CAS  Article  Google Scholar 

  34. 34.

    Schimel J, Balser TC, Wallenstein M (2007) Microbial stress-response physiology and its implications for ecosystem function. Ecology 88(6):1386–1394

    Article  PubMed  Google Scholar 

  35. 35.

    Onyenwoke RU, Brill JA, Farahi K, Wiegel J (2004) Sporulation genes in members of the low G+ C Gram-type-positive phylogenetic branch (Firmicutes). Arch. Microbiol. 182(2–3):182–192

    CAS  PubMed  Google Scholar 

  36. 36.

    Davis KE, Sangwan P, Janssen PH (2011) Acidobacteria, Rubrobacteridae and Chloroflexi are abundant among very slow-growing and mini-colony-forming soil bacteria. Environ. Microbiol. 13(3):798–805

    Article  PubMed  Google Scholar 

  37. 37.

    Sutcliffe IC (2010) A phylum level perspective on bacterial cell envelope architecture. Trends Microbiol. 18(10):464–470

    CAS  Article  PubMed  Google Scholar 

  38. 38.

    Wu D, Raymond J, Wu M, Chatterji S, Ren Q, Graham JE, Bryant DA, Robb F, Colman A, Tallon LJ (2009) Complete genome sequence of the aerobic CO-oxidizing thermophile Thermomicrobium roseum. PLoS One 4(1):e4207

    Article  PubMed  PubMed Central  Google Scholar 

  39. 39.

    Barnard RL, Osborne CA, Firestone MK (2013) Responses of soil bacterial and fungal communities to extreme desiccation and rewetting. ISME J 7(11):2229–2241

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  40. 40.

    Bachar A, Al-Ashhab A, Soares MIM, Sklarz MY, Angel R, Ungar ED, Gillor O (2010) Soil microbial abundance and diversity along a low precipitation gradient. Microb. Ecol. 60(2):453–461

    Article  PubMed  Google Scholar 

  41. 41.

    Elbert W, Weber B, Burrows S, Steinkamp J, Büdel B, Andreae MO, Pöschl U (2012) Contribution of cryptogamic covers to the global cycles of carbon and nitrogen. Nat. Geosci. 5(7):459–462

    CAS  Article  Google Scholar 

  42. 42.

    Locey KJ, Lennon JT (2016) Scaling laws predict global microbial diversity. Proc. Natl. Acad. Sci. 113(21):5970–5975

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  43. 43.

    Cornforth DM, Foster KR (2013) Competition sensing: the social side of bacterial stress responses. Nat Rev Microbiol 11(4):285–293

    CAS  Article  PubMed  Google Scholar 

Download references

Acknowledgements

This work was supported by the Korea Research Fellowship Program through the National Research Foundation of Korea (NRF) funded by the Ministry of Science, ICT and Future Planning (2015H1D3A1066568). This research was conducted under the financial support from the NRF funded by the Korean Government, Ministry of Education, Science and Technology (MEST) (NRF-0409-20150076).

Author information

Affiliations

Authors

Corresponding authors

Correspondence to Jonathan M. Adams or Yosef Steinberger.

Additional information

Binu M. Tripathi and Itumeleng Moroenyane equally contributed to the work

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Tripathi, B.M., Moroenyane, I., Sherman, C. et al. Trends in Taxonomic and Functional Composition of Soil Microbiome Along a Precipitation Gradient in Israel. Microb Ecol 74, 168–176 (2017). https://doi.org/10.1007/s00248-017-0931-0

Download citation

Keywords

  • Taxonomic and functional composition
  • Soil microbiome
  • Israel