Plant-driven niche differentiation of ammonia-oxidizing bacteria and archaea in global drylands

Abstract

Under controlled laboratory conditions, high and low ammonium availability are known to favor soil ammonia-oxidizing bacteria (AOB) and archaea (AOA) communities, respectively. However, whether this niche segregation is maintained under field conditions in terrestrial ecosystems remains unresolved, particularly at the global scale. We hypothesized that perennial vegetation might favor AOB vs. AOA communities compared with adjacent open areas devoid of perennial vegetation (i.e., bare soil) via several mechanisms, including increasing the amount of ammonium in soil. To test this niche-differentiation hypothesis, we conducted a global field survey including 80 drylands from 6 continents. Data supported our hypothesis, as soils collected under plant canopies had higher levels of ammonium, as well as higher richness (number of terminal restriction fragments; T-RFs) and abundance (qPCR amoA genes) of AOB, and lower richness and abundance of AOA, than those collected in open areas located between plant canopies. Some of the reported associations between plant canopies and AOA and AOB communities can be a consequence of the higher organic matter and available N contents found under plant canopies. Other aspects of soils associated with vegetation including shading and microclimatic conditions might also help explain our results. Our findings provide strong evidence for niche differentiation between AOA and AOB communities in drylands worldwide, advancing our understanding of their ecology and biogeography at the global scale.

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References

  1. 1.

    Prosser JI. Autotrophic Nitrification in Bacteria. In: Advances in Microbial Physiology. 1990;30:125–81.

  2. 2.

    Hatzenpichler R. Diversity, physiology, and niche differentiation of ammonia-oxidizing archaea. Appl Environ Microbiol. 2012;78:7501–10.

  3. 3.

    Kowalchuk GA, Stephen JR. Ammonia-oxidizing bacteria: a model for molecular microbial ecology. Annu Rev Microbiol. 2001;55:485–529.

  4. 4.

    Hawkes CV, Wren IF, Herman DJ, Firestone MK. Plant invasion alters nitrogen cycling by modifying the soil nitrifying community. Ecol Lett. 2005;8:976–85.

  5. 5.

    Gruber N, Galloway JN. An Earth-system perspective of the global nitrogen cycle. Nature. 2008;451:293–6.

  6. 6.

    LeBauer DS, Treseder KK. Nitrogen limitation of net primary productivity in terrestrial ecosystems is globally distributed. Ecology. 2008;89:371–9.

  7. 7.

    Parker SS, Schimel JP. Soil nitrogen availability and transformations differ between the summer and the growing season in a California grassland. Appl Soil Ecol. 2011;48:185–92.

  8. 8.

    Schlesinger W, Bernhardt E. Biogeochemistry: an analysis of global change. 2013;3:688.

  9. 9.

    Yang WH, Ryals RA, Cusack DF, Silver WL. Cross-biome assessment of gross soil nitrogen cycling in California ecosystems. Soil Biol Biochem. 2017;107:144–55.

  10. 10.

    Venter JC, Remington K, Heidelberg JF, Halpern AL, Rusch D, Eisen JA, et al. Environmental genome shotgun sequencing of the Sargasso Sea. Science. 2004;304:66–74.

  11. 11.

    Könneke M, Bernhard AE, de la Torre JR, Walker CB, Waterbury JB, Stahl DA. Isolation of an autotrophic ammonia-oxidizing marine archaeon. Nature. 2005;437:543.

  12. 12.

    Treusch AH, Leininger S, Kletzin A, Schuster SC, Klenk HP, Schleper C. Novel genes for nitrite reductase and Amo-related proteins indicate a role of uncultivated mesophilic crenarchaeota in nitrogen cycling. Environ Microbiol. 2005;7:1985–95.

  13. 13.

    Maire V, Gross N, Börger L, Proulx R, Wirth C, Pontes LDS, Soussana JF, Louault F. Habitat filtering and niche differentiation jointly explain species relative abundance within grassland communities along fertility and disturbance gradients. New Phytol. 2012;196:497–509.

  14. 14.

    Prosser JI, Nicol GW. Archaeal and bacterial ammonia-oxidisers in soil: The quest for niche specialisation and differentiation. Trends Microbiol. 2012;20:523–31.

  15. 15.

    Verhamme DT, Prosser JI, Nicol GW. Ammonia concentration determines differential growth of ammonia-oxidising archaea and bacteria in soil microcosms. ISME J. 2011;5:1067–71.

  16. 16.

    Hink L, Gubry-Rangin C, Nicol GW, Prosser JI. The consequences of niche and physiological differentiation of archaeal and bacterial ammonia oxidisers for nitrous oxide emissions. ISME J. 2018;12:1084–93.

  17. 17.

    Di HJ, Cameron KC, Shen CS, Winefield CS, O'Callaghan M, Bowatte S, He JZ. Nitrification driven by bacteria and not archaea in nitrogen-rich grassland soils. Nat Geosci. 2009;2:621–4.

  18. 18.

    He JZ, Hu HW, Zhang LM. Current insights into the autotrophic thaumarchaeal ammonia oxidation in acidic soils. Soil Biol Biochem. 2012;55:146–54.

  19. 19.

    Nazaries L, Karunaratne SB, Delgado-Baquerizo M, Campbell CD, Singh BK. Environmental drivers of the geographical distribution of methanotrophs: Insights from a national survey. Soil Biol Biochem. 2018;127:264–79.

  20. 20.

    Reich PB. The world-wide ‘fast-slow’ plant economics spectrum: A traits manifesto. J Ecol. 2014;102:275–301.

  21. 21.

    Poorter L, Bongers L, Bongers F. Architecture of 54 moist‐forest tree species: traits, trade‐offs, and functional groups. Ecology. 2006;87:1289–301.

  22. 22.

    Sendall KM, Lusk CH, Reich PB. Trade-offs in juvenile growth potential vs. shade tolerance among subtropical rain forest trees on soils of contrasting fertility. Funct Ecol. 2016;30:845–55.

  23. 23.

    Sterck FJ, Poorter L, Schieving F. Leaf traits are good predictors of plant performance across 53 rain forest species. Ecology. 2006;87:1733–43.

  24. 24.

    Moreau D, Pivato B, Bru D, Busset H, Deau F, Faivre C, et al. Plant traits related to nitrogen uptake influence plant‐microbe competition. Ecology. 2015;96:2300–10.

  25. 25.

    Thion CE, Poirel JD, Cornulier T, De Vries FT, Bardgett RD, Prosser JI. Plant nitrogen-use strategy as a driver of rhizosphere archaeal and bacterial ammonia oxidiser abundance. FEMS Microbiol Ecol. 2016;92:fiw091.

  26. 26.

    Delgado-Baquerizo M, Morillas L, Maestre FT, Gallardo A. Biocrusts control the nitrogen dynamics and microbial functional diversity of semi-arid soils in response to nutrient additions. Plant Soil. 2013;372:643–54.

  27. 27.

    Ochoa-Hueso R, Eldridge DJ, Delgado-Baquerizo M, Soliveres S, Bowker MA, Gross N, et al. Soil fungal abundance and plant functional traits drive fertile island formation in global drylands. J Ecol. 2018;106:242–53.

  28. 28.

    Pravalie R. Drylands extent and environmental issues. A global approach. Earth-Science Rev. 2016;161:259–78.

  29. 29.

    Reynolds JF, Smith DMS, Lambin EF, Turner BL II, Mortimore M, et al. Global desertification: building a science for dryland development. Science. 2007;316:847–51.

  30. 30.

    Valentin C, D’Herbès JM, Poesen J. Soil and water components of banded vegetation patterns. Catena. 1999;37:1–24.

  31. 31.

    Delgado‐Baquerizo M, Maestre F. Human impacts and aridity differentially alter soil N availability in drylands worldwide. Glob Ecol. 2016;25:36-45.

  32. 32.

    Gubry-Rangin C, Hai B, Quince C, Engel M, Thomson BC, James P, et al. Niche specialization of terrestrial archaeal ammonia oxidizers. Proc Natl Acad Sci USA. 2011;108:21206–11.

  33. 33.

    Hu HW, Zhang LM, Dai Y, Di HJ, He JZ. pH-dependent distribution of soil ammonia oxidizers across a large geographical scale as revealed by high-throughput pyrosequencing. J Soils Sediments. 2013;13:1439–49.

  34. 34.

    Oton EV, Quince C, Nicol GW, Prosser JI, Gubry-Rangin C. Phylogenetic congruence and ecological coherence in terrestrial Thaumarchaeota. ISME J. 2016;10:85–96.

  35. 35.

    Hu HW, Chen D, He JZ. Microbial regulation of terrestrial nitrous oxide formation: understanding the biological pathways for prediction of emission rates. FEMS Microbiol Rev. 2015;39:729–49.

  36. 36.

    Bernhard AE, Landry ZC, Blevins A, José R, Giblin AE, Stahl DA. Abundance of ammonia-oxidizing archaea and bacteria along an estuarine salinity gradient in relation to potential nitrification rates. Appl Environ Microbiol. 2010;76:1285–9.

  37. 37.

    Bello MO, Thion C, Gubry-Rangin C, Prosser JI. Differential sensitivity of ammonia oxidising archaea and bacteria to matric and osmotic potential. Soil Biol Biochem. 2019;129:184–90.

  38. 38.

    Valencia E, Maestre FT, Le Bagousse-Pinguet Y, Quero JL, Tamme R, Börger L, et al. Functional diversity enhances the resistance of ecosystem multifunctionality to aridity in Mediterranean drylands. New Phytol. 2015;206:660–71.

  39. 39.

    Maestre FT, Delgado-Baquerizo M, Jeffries TC, Eldridge DJ, Ochoa V, Gozalo B, et al. Increasing aridity reduces soil microbial diversity and abundance in global drylands. Proc Natl Acad Sci USA. 2015;112:15684–9.

  40. 40.

    Carini P, Delgado-Baquerizo M, Hinckley EL, Brewer TE, Rue G, Vanderburgh C, et al. Unraveling the effects of spatial variability and relic DNA on the temporal dynamics of soil microbial communities. BioRxiv. 2018;402438.

  41. 41.

    Delgado-Baquerizo M, Covelo F, Maestre FT, Gallardo A. Biological soil crusts affect small-scale spatial patterns of inorganic N in a semiarid Mediterranean grassland. J Arid Environ. 2013;91:147–50.

  42. 42.

    Tourna M, Freitag TE, Nicol GW, Prosser JI. Growth, activity and temperature responses of ammonia-oxidizing archaea and bacteria in soil microcosms. Environ Microbiol. 2008;10:1357–64.

  43. 43.

    Rotthauwe JH, Witzel KP, Liesack W. The ammonia monooxygenase structural gene amoA as a functional marker: molecular fine-scale analysis of natural ammonia-oxidizing populations. Appl Environ Microbiol. 1997;63:4702–12.

  44. 44.

    Hu HW, Macdonald CA, Trivedi P, Holmes B, Bodrossy L, He JZ, Singh BK. Water addition regulates the metabolic activity of ammonia oxidizers responding to environmental perturbations in dry subhumid ecosystems. Environ Microbiol. 2015;17:444–61.

  45. 45.

    Delgado-Baquerizo M, Maestre FT, Eldridge DJ, Singh BK. Microsite differentiation drives the abundance of soil ammonia oxidizing bacteria along aridity gradients. Front Microbiol. 2016;7:505.

  46. 46.

    Culman SW, Bukowski R, Gauch HG, Cadillo-Quiroz H, Buckley DH. T-REX: software for the processing and analysis of T-RFLP data. BMC Bioinformatics. 2009;10:171.

  47. 47.

    van Dorst J, Bissett A, Palmer AS, Brown M, Snape I, Stark JS, et al. Community fingerprinting in a sequencing world. FEMS Microbiol Ecol. 2014;89:316–30.

  48. 48.

    Stralis-Pavese N, Sessitsch A, Weilharter A, Reichenauer T, Riesing J, Csontos J, et al. Optimization of diagnostic microarray for application in analysing landfill methanotroph communities under different plant covers. Environ Microbiol. 2004;6:347–63.

  49. 49.

    Singh BK, Nazaries L, Munro S, Anderson IC, Campbell CD. Use of multiplex terminal restriction fragment length polymorphism for rapid and simultaneous analysis of different components of the soil microbial community. Appl Environ Microbiol. 2006;72:7278–85.

  50. 50.

    Zomer RJ, Trabucco A, Bossio DA, Verchot LV. Climate change mitigation: A spatial analysis of global land suitability for clean development mechanism afforestation and reforestation. Agric Ecosyst Environ. 2008;126:67–8.

  51. 51.

    Hijmans RJ, Cameron SE, Parra JL, Jones PG, Jarvis A. Very high resolution interpolated climate surfaces for global land areas. Int J Climatol. 2005;7568:201.

  52. 52.

    Sanderson EW, Jaiteh M, Levy MA, Redford KH, Wannebo AV, Woolmer G. The Human Footprint and the Last of the Wild: The human footprint is a global map of human influence on the land surface, which suggests that human beings are stewards of nature, whether we like it or not. Bioscience. 2002;52:891–904.

  53. 53.

    Crowther TW, Glick HB, Covey KR, Bettigole C, Bettigole C, Maynard DS, et al. Mapping tree density at a global scale. Nature. 2015;525:201–5.

  54. 54.

    Anderson JM, Ingram JSI. Tropical Soil Biology and Fertility: A Handbook of Methods. Soil Sci. 1994;157:265.

  55. 55.

    Delgado-Baquerizo M, Gallardo A. Depolymerization and mineralization rates at 12 Mediterranean sites with varying soil N availability. A test for the Schimel and Bennett model. Soil Biol Biochem. 2011;43:693–6.

  56. 56.

    Maestre FT, Quero JL, Gotelli NJ, Escudero A, Ochoa V, Delgado-Baquerizo M, et al. Plant species richness and ecosystem multifunctionality in global drylands. Science. 2012;335:279–91.

  57. 57.

    Clarke KR, Gorley RN. PRIMER V6: User Manual-tutorial. 2006.

  58. 58.

    Maestre FT, Bautista S, Cortina J, Bellot J. Potential for using facilitation by grasses to establish shrubs on a semiarid degraded steppe. Ecol Appl. 2001;11:1641–55.

  59. 59.

    Maestre FT, Bautista S, Cortina J. Positive, negative, and net effects in Grass-Shrub interaction in Mediterranean Semiarid Grassland. Ecology. 2003;84:3186–97.

  60. 60.

    Valentine DL. Opinion: Adaptations to energy stress dictate the ecology and evolution of the archaea. Nat Rev. 2007;5:316.

  61. 61.

    Bates ST, Berg-Lyons D, Caporaso JG, Walters WA, Knight R, Fierer N. Examining the global distribution of dominant archaeal populations in soil. ISME J. 2011;5:908–17.

  62. 62.

    Zhalnina K, Dörr de Quadros P, AO Camargo F, Triplett EW. Drivers of archaeal ammonia-oxidizing communities in soil. Front Microbiol. 2012;3:210.

  63. 63.

    Carini P, Marsden PJ, Leff JW, Morgan EE, Strickland MW, Fierer N. Relic DNA is abundant in soil and obscures estimates of soil microbial diversity. Nat Microbiol. 2016;2:16242.

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Acknowledgements

We acknowledge the help of Victoria Ochoa and Beatriz Gozalo with laboratory analyses, and of all the colleagues that collected soil samples in global drylands. This research is supported by the Australian Research Council projects (DP170104634 and DP190103714), by the European Research Council (BIOCOM project, ERC Grant agreement n°242658) and by the Spanish Ministerio de Economía y Competitividad (BIOMOD project, ref. CGL2013-44661-R). M.D-B. acknowledges support from the Marie Sklodowska-Curie Actions of the Horizon 2020 Framework Programme H2020-MSCA-IF-2016 under REA grant agreement n°702057. FTM acknowledges support from the European Research Council (BIODESERT project, ERC Grant agreement n°647038).

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Statement of authorship: M.D.-B. conceived the idea of this study. F.T.M. designed and coordinated field surveys. Laboratory analyses were done by C.T. and F.T.M. in consultation with B.K.S. and M.D.B. Data analyses were done by C.T., B.K.S. and H.-W.H; interpretation was done by all authors. Statistical modeling was done by M.D.B. The manuscript was written by M.D.-B. and C.T., edited by P.B.R., B.K.S. and F.T.M., and all authors contributed to the final draft.

Correspondence to Brajesh K. Singh or Manuel Delgado-Baquerizo.

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Trivedi, C., Reich, P.B., Maestre, F.T. et al. Plant-driven niche differentiation of ammonia-oxidizing bacteria and archaea in global drylands. ISME J 13, 2727–2736 (2019). https://doi.org/10.1038/s41396-019-0465-1

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