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Functional dominance and community compositions of ammonia-oxidizing archaea in extremely acidic soils of natural forests

  • Ruo-Nan Wu
  • Han Meng
  • Yong-Feng Wang
  • Ji-Dong GuEmail author
Environmental biotechnology
  • 107 Downloads

Abstract

Extremely acidic soils of natural forests in Nanling National Nature Reserve have been previously investigated and revisited in two successive years to reveal the active ammonia oxidizers. Ammonia-oxidizing archaea (AOA) rather than ammonia-oxidizing bacteria (AOB) were found more functionally important in the extremely acidic soils of the natural forests in Nanling National Nature Reserve. The relative abundances of Nitrosotalea, Nitrososphaera sister group, and Nitrososphaera lineages recovered by ammonia monooxygenase subunit A (amoA) transcripts were reassessed and compared to AOA communities formerly detected by genomic DNA. Nitrosotalea, previously found the most abundant AOA, were the second-most-active lineage after Nitrososphaera sister group. Our field study results, therefore, propose the acidophilic AOA, Nitrosotalea, can better reside in extremely acidic soils while they may not contribute to nitrification proportionately according to their abundances or they are less functionally active. In contrast, the functional importance of Nitrososphaera sister group may be previously underestimated and the functional dominance further extends their ecological distribution as little has been reported. Nitrososphaera gargensis–like AOA, the third abundant lineage, were more active in summer. The analyses of AOA community composition and its correlation with environmental parameters support the previous observations of the potential impact of organic matter on AOA composition. Al3+, however, did not show a strong adverse correlation with the abundances of functional AOA unlike in the DNA-based study. The new data further emphasize the functional dominance of AOA in extremely acidic soils, and unveil the relative contributions of AOA lineages to nitrification and their community transitions under the environmental influences.

Keywords

Ammonia-oxidizing archaea (AOA) Ammonia monooxygenase subunit a (amoAOrganic matter Aluminum Nitrososphaera sister group Nitrosotalea 

Notes

Acknowledgments

We would like to thank the comments and revision of Miss Jennifer Li, and the reviewers and editor for their assistance in the publication process.

Funding information

This research was supported by a PhD graduate studentship (RW) from The University of Hong Kong Graduate School and a research grant (Yong-Feng Wang) from National Natural Science Foundation of China (31470562).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

This article does not contain any studies with human participants or animals performed by any of the authors.

Supplementary material

253_2019_9721_MOESM1_ESM.pdf (437 kb)
ESM 1 (PDF 437 kb)

References

  1. Beman JM, Francis CA (2006) Diversity of ammonia-oxidizing archaea and bacteria in the sediments of a hypernutrified subtropical estuary: Bahia del Tobari, Mexico. Appl Environ Microbiol 72:7767–7777.  https://doi.org/10.1128/AEM.00946-06 CrossRefGoogle Scholar
  2. Beman JM, Roberts KJ, Wegley L, Rohwer F, Francis CA (2007) Distribution and diversity of archaeal ammonia monooxygenase genes associated with corals. Appl Environ Microbiol 73:5642–5647.  https://doi.org/10.1128/AEM.00461-07 CrossRefGoogle Scholar
  3. Booth MS, Stark JM, Rastetter E (2005) Controls on nitrogen cycling in terrestrial ecosystems: a synthetic analysis of literature data. Ecol Monogr 75:139–157.  https://doi.org/10.1890/04-0988 CrossRefGoogle Scholar
  4. De Boer W, Kowalchuk GA (2001) Nitrification in acid soils: micro-organisms and mechanisms. Soil Biol Biochem 33:853–866.  https://doi.org/10.1016/S0038-0717(00)00247-9 CrossRefGoogle Scholar
  5. De Boer W, Gunnewiek PK, Veenhuis M, Bock E, Laanbroek H (1991) Nitrification at low pH by aggregated chemolithotrophic bacteria. Appl Environ Microbiol 57:3600–3604Google Scholar
  6. de la Torre JR, Walker CB, Ingalls AE, Konneke M, Stahl DA (2008) Cultivation of a thermophilic ammonia oxidizing archaeon synthesizing crenarchaeol. Environ Microbiol 10:810–818.  https://doi.org/10.1111/j.1462-2920.2007.01506.x CrossRefGoogle Scholar
  7. Fish JA, Chai B, Wang Q, Sun Y, Brown CT, Tiedje JM, Cole JR (2013) FunGene: the functional gene pipeline and repository. Front Microbiol 4:291CrossRefGoogle Scholar
  8. Francis C, Roberts K, Beman J, Santoro A, Oakley B, (2005) Ubiquity and diversity of ammonia-oxidizing archaea in water columns and sediments of the ocean. Proc Natl Acad Sci 102 (41):14683-14688Google Scholar
  9. 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. Proc Natl Acad Sci U S A 112:9370–9375.  https://doi.org/10.1073/pnas.1419329112 CrossRefGoogle Scholar
  10. Hatzenpichler R, Lebedeva EV, Spieck E, Stoecker K, Richter A, Daims H, Wagner M (2008) A moderately thermophilic ammonia-oxidizing crenarchaeote from a hot spring. Proc Natl Acad Sci U S A 105:2134–2139.  https://doi.org/10.1073/pnas.0708857105 CrossRefGoogle Scholar
  11. Herndl GJ, Reinthaler T, Teira E, van Aken H, Veth C, Pernthaler A, Pernthaler J (2005) Contribution of archaea to total prokaryotic production in the deep Atlantic Ocean. Appl Environ Microbiol 71:2303–2309.  https://doi.org/10.1128/AEM.71.5.2303-2309.2005 CrossRefGoogle Scholar
  12. Horz HP, Barbrook A, Field CB, Bohannan BJM (2004) Ammonia-oxidizing bacteria respond to multifactorial global change. Proc Natl Acad Sci U S A 101:15136–15141.  https://doi.org/10.1073/pnas.0406616101 CrossRefGoogle Scholar
  13. Huang Y, Niu BF, Gao Y, Fu LM, Li WZ (2010) CD-HIT suite: a web server for clustering and comparing biological sequences. Bioinformatics 26:680–682.  https://doi.org/10.1093/bioinformatics/btq003 CrossRefGoogle Scholar
  14. Jung MY, Park SJ, Min D, Kim JS, Rijpstra WI, Damsté JS, 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 Microbiol 77:8635–8647.  https://doi.org/10.1128/Aem.05787-11 CrossRefGoogle Scholar
  15. Karner MB, DeLong EF, Karl DM (2001) Archaeal dominance in the mesopelagic zone of the Pacific Ocean. Nature 409:507–510.  https://doi.org/10.1038/35054051 CrossRefGoogle Scholar
  16. Kim JG, Jung MY, Park SJ, Rijpstra WI, Sinninghe Damsté JS, Madsen EL, Min D, Kim JS, Kim GJ, Rhee SK (2012) Cultivation of a highly enriched ammonia-oxidizing archaeon of thaumarchaeotal group I. 1b from an agricultural soil. Environ Microbiol 14:1528–1543CrossRefGoogle Scholar
  17. Konneke M, Bernhard AE, de la Torre JR, Walker CB, Waterbury JB, Stahl DA (2005) Isolation of an autotrophic ammonia-oxidizing marine archaeon. Nature 437:543–546.  https://doi.org/10.1038/nature03911 CrossRefGoogle Scholar
  18. Lehtovirta-Morley LE, Stoecker K, Vilcinskas A, Prosser JI, Nicol GW (2011) Cultivation of an obligate acidophilic ammonia oxidizer from a nitrifying acid soil. Proc Natl Acad Sci U S A 108:15892–15897.  https://doi.org/10.1073/pnas.1107196108 CrossRefGoogle Scholar
  19. Lehtovirta-Morley LE, Ge CR, Ross J, Yao HY, Nicol GW, Prosser JI (2014) Characterisation of terrestrial acidophilic archaeal ammonia oxidisers and their inhibition and stimulation by organic compounds. FEMS Microbiol Ecol 89:542–552.  https://doi.org/10.1111/1574-6941.12353 CrossRefGoogle Scholar
  20. Lehtovirta-Morley LE, Ross J, Hink L, Weber EB, Gubry-Rangin C, Thion C, Prosser JI, Nicol GW (2016) Isolation of ‘Candidatus Nitrosocosmicus franklandus’, a novel ureolytic soil archaeal ammonia oxidiser with tolerance to high ammonia concentration. FEMS Microbiol Ecol 92:fiw057.  https://doi.org/10.1093/femsec/fiw057 CrossRefGoogle Scholar
  21. Leininger S, Urich T, Schloter M, Schwark L, Qi J, Nicol GW, Prosser JI, Schuster SC, Schleper C (2006) Archaea predominate among ammonia-oxidizing prokaryotes in soils. Nature 442:806CrossRefGoogle Scholar
  22. Loscher CR, Kock A, Konneke M, LaRoche J, Bange HW, Schmitz RA (2012) Production of oceanic nitrous oxide by ammonia-oxidizing archaea. Biogeosciences 9:2419–2429.  https://doi.org/10.5194/bg-9-2419-2012 CrossRefGoogle Scholar
  23. Lu R (2000) Agricultural chemical analysis methods of soil. China Agriculture Science and Technology Press, Beijing, pp 107–108Google Scholar
  24. Martens-Habbena W, Berube PM, Urakawa H, de la Torre JR, Stahl DA (2009) Ammonia oxidation kinetics determine niche separation of nitrifying archaea and bacteria. Nature 461:976–979.  https://doi.org/10.1038/nature08465 CrossRefGoogle Scholar
  25. Nelson DW, Sommers LE (1996) Total carbon, organic carbon, and organic matter. Methods of soil analysis: part 3 - chemical methods: 961–1010Google Scholar
  26. NNNR (2015, 2016) Nanling National Nation Reserve. http://www.gdnl.org. Accessed 12th Aug 2015 and 15th Jan 2016
  27. Park H-D, Wells GF, Bae H, Criddle CS, Francis CA (2006) Occurrence of ammonia-oxidizing archaea in wastewater treatment plant bioreactors. Appl Environ Microbiol 72:5643–5647CrossRefGoogle Scholar
  28. Pester MRT, Flechl S, Gröngröft A, Richter A, Overmann J, Reinhold-Hurek B, Loy A, Wagner M (2012) amoA-based consensus phylogeny of ammonia-oxidizing archaea and deep sequencing of amoA genes from soils of four different geographic regions. Environ Microbiol 14:525–539.  https://doi.org/10.1111/j.1462-2920.2011.02666.x CrossRefGoogle Scholar
  29. Rotthauwe J-H, Witzel K-P, 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):4704–4712Google Scholar
  30. Santoro AE, Buchwald C, McIlvin MR, Casciotti KL (2011) Isotopic signature of N2O produced by marine ammonia-oxidizing archaea. Science 333:1282–1285.  https://doi.org/10.1126/science.1208239 CrossRefGoogle Scholar
  31. Schleper C, Jurgens G, Jonuscheit M (2005) Genomic studies of uncultivated archaea. Nat Rev Microbiol 3:479–488.  https://doi.org/10.1038/nrmicro1159 CrossRefGoogle Scholar
  32. Schloss PDWS, Ryabin T, Hall JR, Hartmann M, Hollister EB, Lesniewski RA, Oakley BB, Parks DH, Robinson CJ, Sahl JW (2009) Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 75:7537–7541.  https://doi.org/10.1128/Aem.01541-09 CrossRefGoogle Scholar
  33. Spang A, Poehlein A, Offre P, Zumbrägel S, Haider S, Rychlik N, Nowka B, Schmeisser C, Lebedeva EV, Rattei T, Böhm C (2012) The genome of the ammonia-oxidizing Candidatus Nitrososphaera gargensis: insights into metabolic versatility and environmental adaptations. Environ Microbiol 14:3122–3145CrossRefGoogle Scholar
  34. Steger D, Ettinger-Epstein P, Whalan S, Hentschel U, de Nys R, Wagner M, Taylor MW (2008) Diversity and mode of transmission of ammonia-oxidizing archaea in marine sponges. Environ Microbiol 10:1087–1094.  https://doi.org/10.1111/j.1462-2920.2007.01515.x CrossRefGoogle Scholar
  35. Stieglmeier M, Mooshammer M, Kitzler B, Wanek W, Zechmeister-Boltenstern S, Richter A, Schleper C (2014) Aerobic nitrous oxide production through N-nitrosating hybrid formation in ammonia-oxidizing archaea. ISME J 8:1135–1146.  https://doi.org/10.1038/ismej.2013.220 CrossRefGoogle Scholar
  36. Stopnisek N, Gubry-Rangin C, Hofferle S, Nicol GW, Mandic-Mulec I, Prosser JI (2010) Thaumarchaeal ammonia oxidation in an acidic forest peat soil is not influenced by ammonium amendment. Appl Environ Microbiol 76:7626–7634.  https://doi.org/10.1128/AEM.00595-10 CrossRefGoogle Scholar
  37. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729.  https://doi.org/10.1093/molbev/mst197 CrossRefGoogle Scholar
  38. Ter Braak CJ, Smilauer P (2002) CANOCO reference manual and CanoDraw for windows user’s guide: software for canonical community ordination (version 4.5). http://www.canoco.com. Accessed 1st Feb 2016 
  39. Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680CrossRefGoogle Scholar
  40. Tourna M, Stieglmeier M, Spang A, Könneke M, Schintlmeister A, Urich T, Engel M, Schloter M, Wagner M, Richter A, Schleper C (2011) Nitrososphaera viennensis, an ammonia oxidizing archaeon from soil. Proc Natl Acad Sci U S A 108:8420–8425.  https://doi.org/10.1073/pnas.1013488108 CrossRefGoogle Scholar
  41. Van Hoek A, Van Alen T, Sprakel V, Hackstein J, Vogels G, (1998) Evolution of anaerobic ciliates from the gastrointestinal tract: phylogenetic analysis of the ribosomal repeat from Nyctotherus ovalis and its relatives. Mol Biol Evol 15(9):1195-1206Google Scholar
  42. Venter JC, Remington K, Heidelberg JF, Halpern AL, Rusch D, Eisen JA, Wu D, Paulsen I, Nelson KE, Nelson W, Fouts DE (2004) Environmental genome shotgun sequencing of the Sargasso Sea. Science 304:66–74.  https://doi.org/10.1126/science.1093857 CrossRefGoogle Scholar
  43. Wang YF, Gu J-D (2013) Higher diversity of ammonia/ammonium-oxidizing prokaryotes in constructed freshwater wetland than natural coastal marine wetland. Appl Microbiol Biotechnol 97:7015–7033.  https://doi.org/10.1007/s00253-012-4430-4 CrossRefGoogle Scholar
  44. Weidler GW, Dornmayr-Pfaffenhuemer M, Gerbl FW, Heinen W, Stan-Lotter H (2007) Communities of archaea and bacteria in a subsurface radioactive thermal spring in the Austrian Central Alps, and evidence of ammonia-oxidizing Crenarchaeota. Appl Environ Microbiol 73:259–270.  https://doi.org/10.1128/AEM.01570-06 CrossRefGoogle Scholar
  45. Wu Y, Conrad R (2014) Ammonia oxidation-dependent growth of group I.1b Thaumarchaeota in acidic red soil microcosms. FEMS Microbiol Ecol 89:127–134.  https://doi.org/10.1111/1574-6941.12340 CrossRefGoogle Scholar
  46. Wu R-N, Meng H, Wang Y-F, Lan W, Gu J-D (2017) A more comprehensive community of ammonia-oxidizing archaea (AOA) revealed by genomic DNA and RNA analyses of amoA gene in subtropical acidic forest soils. Microb Ecol 74(4):910–922.  https://doi.org/10.1007/s00248-017-1045-4 CrossRefGoogle Scholar
  47. Wuchter C, Abbas B, Coolen MJ, Herfort L, van Bleijswijk J, Timmers P, Strous M, Teira E, Herndl GJ, Middelburg JJ, Schouten S (2006) Archaeal nitrification in the ocean. Proc Natl Acad Sci U S A 103:12317–12322.  https://doi.org/10.1073/pnas.0600756103 CrossRefGoogle Scholar
  48. Yin B, Crowley D, Sparovek G, De Melo WJ, Borneman J (2000) Bacterial functional redundancy along a soil reclamation gradient. Appl Environ Microbiol 66:4361–4365.  https://doi.org/10.1128/Aem.66.10.4361-4365.2000 CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Laboratory of Environmental Microbiology and Toxicology, School of Biological Sciences, Faculty of ScienceThe University of Hong KongHong KongPeople’s Republic of China
  2. 2.Department of Biology, Hong Kong Baptist UniversityHong KongPeople’s Republic of China
  3. 3.Laboratory of Microbial Ecology and Toxicology, Guangdong Academy of ForestryGuangzhouPeople’s Republic of China

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