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The Responses of Ammonia-Oxidizing Microorganisms to Different Environmental Factors Determine Their Elevational Distribution and Assembly Patterns

  • Soil Microbiology
  • Published:
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Abstract

The assembly mechanisms shaping the elevational patterns of diversity and community structure in ammonia-oxidizing archaea (AOA) and ammonia-oxidizing bacteria (AOB) are not well understood. We investigated the diversities, co-occurrence network patterns, key drivers, and potential activities of AOA and AOB communities along a large altitudinal gradient. The α-diversity of the AOA communities exhibited a monotonically decreasing pattern with increasing elevation, whereas a sinusoidal pattern was observed for the AOB communities. The mean annual temperature was the single factor that most strongly influenced the α-diversity of the AOA communities; however, the interactions of plant richness, soil conductivity, and total nitrogen made comparable contributions to the α-diversity of the AOB communities. Moreover, the β-diversities of the AOA and AOB communities were divided into two distinct clusters by elevation, i.e., low- (1800–2600 m) and high-altitude (2800–4100 m) sections. These patterns were attributed mainly to the soil pH, followed by variations in plant richness along the altitudinal gradient. In addition, the AOB communities were more important to the soil nitrification potential in the low-altitude section, whereas the AOA communities contributed more to the soil nitrification potential in the high-altitude section. Overall, this study revealed the key factors shaping the elevational patterns of ammonia-oxidizing communities and might predict the consequences of changes in ammonia-oxidizing communities.

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Data Availability

The data that support the findings of this study are available from the corresponding author upon reasonable request.

References

  1. Lehtovirta-Morley LE, Sayavedra-Soto LA, Gallois N, Schouten S, Stein LY, Prosser JI, Nicol GW (2016) Identifying potential mechanisms enabling acidophily in the ammonia-oxidizing archae on “Candidatus Nitrosotalea devanaterra.” Appl Environ Microb 82(9):2608–2619. https://doi.org/10.1128/aem.04031-15

    Article  CAS  Google Scholar 

  2. Kits KD, Sedlacek CJ, Lebedeva EV, Han P, Bulaev A, Pjevac P, Daebeler A, Romano S, Albertsen M, Stein LY, Daims H, Wagner M (2017) Kinetic analysis of a complete nitrifier reveals an oligotrophic lifestyle. Nature 549(7671):269–272. https://doi.org/10.1038/nature23679

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Ouyang Y, Norton JM, Stark JM, Reeve JR, Habteselassie MY (2016) Ammonia-oxidizing bacteria are more responsive than archaea to nitrogen source in an agricultural soil. Soil Biol Biochem 96:4–15. https://doi.org/10.1016/j.soilbio.2016.01.012

    Article  CAS  Google Scholar 

  4. Kozlowski JA, Stieglmeier M, Schleper C, Klotz MG, Stein LY (2016) Pathways and key intermediates required for obligate aerobic ammonia-dependent chemolithotrophy in bacteria and Thaumarchaeota. ISME J 10(8):1836–1845. https://doi.org/10.1038/ismej.2016.2

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Offre P, Kerou M, Spang A, Schleper C (2014) Variability of the transporter gene complement in ammonia-oxidizing archaea. Trends Microbiol 22(12):665–675. https://doi.org/10.1016/j.tim.2014.07.007

    Article  CAS  PubMed  Google Scholar 

  6. Hink L, Gubry-Rangin C, Nicol GW, Prosser JI (2018) The consequences of niche and physiological differentiation of archaeal and bacterial ammonia oxidisers for nitrous oxide emissions. ISME J 12(4):1084–1093. https://doi.org/10.1038/s41396-017-0025-5

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Nicol GW, Leininger S, Schleper C, Prosser JI (2008) The influence of soil pH on the diversity, abundance and transcriptional activity of ammonia oxidizing archaea and bacteria. Environ Microbiol 10(11):2966–2978. https://doi.org/10.1111/j.1462-2920.2008.01701.x

    Article  CAS  PubMed  Google Scholar 

  8. Meinhardt KA, Stopnisek N, Pannu MW, Strand SE, Fransen SC, Casciotti KL, Stahl DA (2018) Ammonia-oxidizing bacteria are the primary N2O producers in an ammonia-oxidizing archaea dominated alkaline agricultural soil. Environ Microbiol 20(6):2195–2206. https://doi.org/10.1111/1462-2920.14246

    Article  CAS  PubMed  Google Scholar 

  9. Lu XD, Nicol GW, Neufeld JD (2018) Differential responses of soil ammonia-oxidizing archaea and bacteria to temperature and depth under two different land uses. Soil Biol Biochem 120:272–282. https://doi.org/10.1016/j.soilbio.2018.02.017

    Article  CAS  Google Scholar 

  10. Bello MO, Thion C, Gubry-Rangin C, Prosser JI (2019) Differential sensitivity of ammonia oxidising archaea and bacteria to matric and osmotic potential. Soil Biol Biochem 129:184–190. https://doi.org/10.1016/j.soilbio.2018.11.017

    Article  CAS  Google Scholar 

  11. Ying JY, Zhang LM, He JZ (2010) Putative ammonia-oxidizing bacteria and archaea in an acidic red soil with different land utilization patterns. Environ Microbiol Rep 2(2):304–312. https://doi.org/10.1111/j.1758-2229.2009.00130.x

    Article  CAS  PubMed  Google Scholar 

  12. Li J, Li C, Kou Y, Yao M, He Z, Li X (2020) Distinct mechanisms shape soil bacterial and fungal co-occurrence networks in a mountain ecosystem. FEMS Microbiol Ecol 96(4):fiaa030. https://doi.org/10.1093/femsec/fiaa030

    Article  CAS  PubMed  Google Scholar 

  13. Wang YS, Li CN, Kou YP, Wang JJ, Tu B, Li H, Li XZ, Wang CT, Yao MJ (2017) Soil pH is a major driver of soil diazotrophic community assembly in Qinghai-Tibet alpine meadows. Soil Biol Biochem 115:547–555. https://doi.org/10.1016/j.soilbio.2017.09.024

    Article  CAS  Google Scholar 

  14. Berry D, Widder S (2014) Deciphering microbial interactions and detecting keystone species with co-occurrence networks. Front Microbiol 5:219. https://doi.org/10.3389/fmicb.2014.00219

    Article  PubMed  PubMed Central  Google Scholar 

  15. Meng H, Katayama Y, Gu JD (2017) More wide occurrence and dominance of ammonia-oxidizing archaea than bacteria at three Angkor sandstone temples of Bayon, Phnom Krom and Wat Athvea in Cambodia. Int Biodeterior Biodegrad 117:78–88. https://doi.org/10.1016/j.ibiod.2016.11.012

    Article  CAS  Google Scholar 

  16. Guo JJ, Ling N, Chen H, Zhu C, Kong YL, Wang M, Shen QR, Guo SW (2017) Distinct drivers of activity, abundance, diversity and composition of ammonia-oxidizers: evidence from a long-term field experiment. Soil Biol Biochem 115:403–414. https://doi.org/10.1016/j.soilbio.2017.09.007

    Article  CAS  Google Scholar 

  17. Taylor AE, Zeglin LH, Dooley S, Myrold DD, Bottomley PJ (2010) Evidence for different contributions of archaea and bacteria to the ammonia-oxidizing potential of diverse oregon soils. Appl Environ Microb 76(23):7691–7698. https://doi.org/10.1128/aem.01324-10

    Article  CAS  Google Scholar 

  18. Zhao K, Kong W, Khan A, Liu J, Guo G, Muhanmmad S, Zhang X, Dong X (2017) Elevational diversity and distribution of ammonia-oxidizing archaea community in meadow soils on the Tibetan Plateau. Appl Microbiol Biotechnol 101(18):7065–7074. https://doi.org/10.1007/s00253-017-8435-x

    Article  CAS  PubMed  Google Scholar 

  19. Li C, Tu B, Kou Y, Wang Y, Li X, Wang J, Li J (2021) The assembly of methanotrophic communities regulated by soil pH in a mountain ecosystem. Catena 196:104883. https://doi.org/10.1016/j.catena.2020.104883

    Article  CAS  Google Scholar 

  20. Li J, Shen Z, Li C, Kou Y, Wang Y, Tu B, Zhang S, Li X (2018) Stair-step pattern of soil bacterial diversity mainly driven by pH and vegetation types along the elevational gradients of Gongga Mountain, China. Front Microbiol 9:569. https://doi.org/10.3389/fmicb.2018.00569

    Article  PubMed  PubMed Central  Google Scholar 

  21. Shen ZH, Fang JY, Liu ZL (2001) Patterns of biodiversity along the vertical vegetation spectrum of the east aspect of Gongga Mountain. Chin J Plan Ecolo 25(6):721–732. https://www.plant-ecology.com/EN/Y2001/V25/I6/721. Accessed 20 Apr 2022

  22. Francis CA, Roberts KJ, Beman JM, Santoro AE, Oakley BB (2005) Ubiquity and diversity of ammonia-oxidizing archaea in water columns and sediments of the ocean. Proc Natl Acad Sci USA 102(41):14683–14688. https://doi.org/10.1073/pnas.0506625102

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Rotthauwe JH, Witzel KP, Liesack W (1997) The ammonia monooxygenase structural gene amoA as a functional marker: Molecular fine-scale analysis of natural ammonia-oxidizing populations. Appl Environ Microb 63(12):4704–4712. https://doi.org/10.1128/aem.63.12.4704-4712.1997

    Article  CAS  Google Scholar 

  24. Penton CR, Johnson TA, Quensen JF, Iwai S, Cole JR, Tiedje JM (2013) Functional genes to assess nitrogen cycling and aromatic hydrocarbon degradation: primers and processing matter. Front Microbiol 4:e00279. https://doi.org/10.3389/fmicb.2013.00279

    Article  Google Scholar 

  25. Chin CS, Alexander DH, Marks P, Klammer AA, Drake J, Heiner C, Clum A, Copeland A, Huddleston J, Eichler EE, Turner SW, Korlach J (2013) Nonhybrid, finished microbial genome assemblies from long-read SMRT sequencing data. Nat Methods 10(6):563–569. https://doi.org/10.1038/nmeth.2474

    Article  CAS  PubMed  Google Scholar 

  26. Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Pena 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, Tumbaugh PJ, Walters WA, Widmann J, Yatsunenko T, Zaneveld J, Knight R (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7(5):335–336. https://doi.org/10.1038/nmeth.f.303

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Edgar RC (2010) Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26(19):2460–2461. https://doi.org/10.1093/bioinformatics/btq461

    Article  CAS  PubMed  Google Scholar 

  28. Wang Q, Quensen JF III, Fish JA, Kwon Lee T, Sun Y, Tiedje JM, Cole JR (2013) Ecological patterns of nifH genes in four terrestrial climatic zones explored with targeted metagenomics using FrameBot, a new informatics tool. mBio 4(5):e00592-00513. https://doi.org/10.1128/mBio.00592-13

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Hou S, Ai C, Zhou W, Liang G, He P (2018) Structure and assembly cues for rhizospheric nirK-and nirS-type denitrifier communities in long-term fertilized soils. Soil Biol Biochem 119:32–40. https://doi.org/10.1016/j.soilbio.2018.01.007

    Article  CAS  Google Scholar 

  30. Fish JA, Chai BL, Wang Q, Sun YN, Brown CT, Tiedje JM, Cole JR (2013) FunGene: the functional gene pipeline and repository. Front Microbiol 4:291. https://doi.org/10.3389/fmicb.2013.00291

    Article  PubMed  PubMed Central  Google Scholar 

  31. Deng Y, Jiang YH, Yang Y, He Z, Luo F, Zhou J (2012) Molecular ecological network analyses. Bmc Bioinformatics 13:113. https://doi.org/10.1186/1471-2105-13-113

    Article  PubMed  PubMed Central  Google Scholar 

  32. Wang Y, Kou Y, Li C, Tu B, Wang J, Yao M, Li X (2019) Contrasting responses of diazotrophic specialists, opportunists, and generalists to steppe types in Inner Mongolia. Catena 182:104168. https://doi.org/10.1016/j.catena.2019.104168

    Article  Google Scholar 

  33. Shigyo N, Umeki K, Hirao T (2019) Plant functional diversity and soil properties control elevational diversity gradients of soil bacteria. FEMS Microbiol Ecol 95(4):fiz025. https://doi.org/10.1093/femsec/fiz025

    Article  CAS  PubMed  Google Scholar 

  34. Gubry-Rangin C, Novotnik B, Mandic-Mulec I, Nicol GW, Prosser JI (2017) Temperature responses of soil ammonia-oxidising archaea depend on pH. Soil Biol Biochem 106:61–68. https://doi.org/10.1016/j.soilbio.2016.12.007

    Article  CAS  Google Scholar 

  35. Tourna M, Freitag TE, Nicol GW, Prosser JI (2008) Growth, activity and temperature responses of ammonia-oxidizing archaea and bacteria in soil microcosms. Environ Microbiol 10(5):1357–1364. https://doi.org/10.1111/j.1462-2920.2007.01563.x

    Article  CAS  PubMed  Google Scholar 

  36. Peay KG, von Sperber C, Cardarelli E, Toju H, Francis CA, Chadwick OA, Vitousek PM (2017) Convergence and contrast in the community structure of Bacteria, Fungi and Archaea along a tropical elevation-climate gradient. FEMS Microbiol Ecol 93(5):219–222. https://doi.org/10.1093/femsec/fix045

    Article  CAS  Google Scholar 

  37. Pan YD, Birdsey RA, Fang JY, Houghton R, Kauppi PE, Kurz WA, Phillips OL, Shvidenko A, Lewis SL, Canadell JG, Ciais P, Jackson RB, Pacala SW, McGuire AD, Piao SL, Rautiainen A, Sitch S, Hayes D (2011) A large and persistent carbon sink in the world’s forests. Science 333(6045):988–993. https://doi.org/10.1126/science.1201609

    Article  CAS  PubMed  Google Scholar 

  38. Paul EA (2016) The nature and dynamics of soil organic matter: plant inputs, microbial transformations, and organic matter stabilization. Soil Biol Biochem 98:109–126. https://doi.org/10.1016/j.soilbio.2016.04.001

    Article  CAS  Google Scholar 

  39. Yao M, Rui J, Li J, Dai Y, Bai Y, Heděnec P, Wang J, Zhang S, Pei K, Liu C (2014) Rate-specific responses of prokaryotic diversity and structure to nitrogen deposition in the Leymus chinensis steppe. Soil Biol Biochem 79:81–90. https://doi.org/10.1016/j.soilbio.2014.09.009

    Article  CAS  Google Scholar 

  40. Gubry-Rangin C, Kratsch C, Williams TA, McHardy AC, Embley TM, Prosser JI, Macqueen DJ (2015) Coupling of diversification and pH adaptation during the evolution of terrestrial Thaumarchaeota. P Natl Acad Sci USA 112(30):9370–9375. https://doi.org/10.1073/pnas.1419329112

    Article  CAS  Google Scholar 

  41. Prosser JI, Nicol GW (2012) Archaeal and bacterial ammonia-oxidisers in soil: the quest for niche specialisation and differentiation. Trends Microbiol 20(11):523–531. https://doi.org/10.1016/j.tim.2012.08.001

    Article  CAS  PubMed  Google Scholar 

  42. Hayatsu M, Tago K, Uchiyama I, Toyoda A, Wang Y, Shimomura Y, Okubo T, Kurisu F, Hirono Y, Nonaka K, Akiyama H, Itoh T, Takami H (2017) An acid-tolerant ammonia-oxidizing gamma-proteobacterium from soil. ISME J 11(5):1130–1141. https://doi.org/10.1038/ismej.2016.191

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Abichou T, Kormi T, Yuan L, Johnson T, Francisco E (2015) Modeling the effects of vegetation on methane oxidation and emissions through soil landfill final covers across different climates. Waste Manage 36:230–240. https://doi.org/10.1016/j.wasman.2014.11.002

    Article  CAS  Google Scholar 

  44. Thoms C, Gattinger A, Jacob M, Thomas FM, Gleixner G (2010) Direct and indirect effects of tree diversity drive soil microbial diversity in temperate deciduous forest. Soil Biol Biochem 42(9):1558–1565. https://doi.org/10.1016/j.soilbio.2010.05.030

    Article  CAS  Google Scholar 

  45. Hu A, Wang JJ, Sun H, Niu B, Si GC, Wang J, Yeh CF, Zhu XX, Lu XC, Zhou JZ, Yang YP, Ren ML, Hu YL, Dong HL, Zhang GX (2020) Mountain biodiversity and ecosystem functions: interplay between geology and contemporary environments. ISME J 14(4):931–944. https://doi.org/10.1038/s41396-019-0574-x

    Article  PubMed  PubMed Central  Google Scholar 

  46. Faust K, Raes J (2012) Microbial interactions: from networks to models. Nat Rev Microbiol 10:538–550. https://doi.org/10.1038/nrmicro2832

    Article  CAS  PubMed  Google Scholar 

  47. Dohi M, Mougi A (2018) A coexistence theory in microbial communities. R Soc Open Sci 5:180476. https://doi.org/10.1098/rsos.180476

    Article  PubMed  PubMed Central  Google Scholar 

  48. Herbold CW, Lehtovirta-Morley LE, Jung MY, Jehmlich N, Hausmann B, Han P, Loy A, Pester M, Sayavedra-Soto LA, Rhee SK, Prosser JI, Nicol GW, Wagner M, Gubry-Rangin C (2017) Ammonia-oxidising archaea living at low pH: insights from comparative genomics. Environ Microbiol 19(12):4939–4952. https://doi.org/10.1111/1462-2920.13971

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Burton SAQ, Prosser JI (2001) Autotrophic ammonia oxidation at low pH through urea hydrolysis. Appl Environ Microb 67(7):2952–2957. https://doi.org/10.1128/aem.67.7.2952-2957.2001

    Article  CAS  Google Scholar 

  50. Song H, Che Z, Cao WC, Huang T, Wang JG, Dong ZR (2016) Changing roles of ammonia-oxidizing bacteria and archaea in a continuously acidifying soil caused by over-fertilization with nitrogen. Environ Sci Pollut Res 23(12):11964–11974. https://doi.org/10.1007/s11356-016-6396-8

    Article  CAS  Google Scholar 

  51. Jung MY, Park SJ, Min D, Kim JS, Rijpstra WIC, Damste JSS, Kim GJ, Madsen EL, Rhee SK (2011) Enrichment and characterization of an autotrophic ammonia-oxidizing archaeon of mesophilic crenarchaeal Group I.1a from an agricultural soil. Appl Environ Microb 77(24):8635–8647. https://doi.org/10.1128/aem.05787-11

    Article  CAS  Google Scholar 

  52. Koper TE, Stark JM, Habteselassie MY, Norton JM (2010) Nitrification exhibits Haldane kinetics in an agricultural soil treated with ammonium sulfate or dairy-waste compost. FEMS microbiol ecol 74(2):316–322. https://doi.org/10.1111/j.1574-6941.2010.00960.x

    Article  CAS  PubMed  Google Scholar 

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Funding

This work was supported by the National Natural Science Foundation of China (32171550, 31870473), the Strategic Priority Research Program of the Chinese Academy of Sciences (XDA20020401), the Youth Innovation Promotion Association, Chinese Academy of Sciences (2021371), the Second Tibetan Plateau Scientic Expedition and Research Program (2019QZKK0600), and China Biodiversity Observation Networks (Sino BON).

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  1. CAS Key Laboratory of Environmental and Applied Microbiology, Environmental Microbiology Key Laboratory of Sichuan Province, Chengdu Institute of Biology, Chinese Academy of Sciences, Chengdu, 610041, People’s Republic of China

    Yongping Kou, Chaonan Li, Bo Tu, Jiabao Li & Xiangzhen Li

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  1. Yongping Kou
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  2. Chaonan Li
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  3. Bo Tu
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  4. Jiabao Li
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Contributions

X. Z. L. and Y. P. K. planned and designed the research. Y. P. K., J. B. L., C. N. L., and B. T. performed experiments and collected data. Y. P. K. analyzed the data and wrote the manuscript. X. Z. L., J. B. L., and Y. P. K. revised the paper.

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Correspondence to Jiabao Li or Xiangzhen Li.

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Kou, Y., Li, C., Tu, B. et al. The Responses of Ammonia-Oxidizing Microorganisms to Different Environmental Factors Determine Their Elevational Distribution and Assembly Patterns. Microb Ecol 86, 485–496 (2023). https://doi.org/10.1007/s00248-022-02076-8

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