amoA ‐based consensus phylogeny of ammonia‐oxidizing archaea and deep sequencing of amoA genes from soils of four different geographic regions

Abstract

Summary Ammonia‐oxidizing archaea (AOA) play an important role in nitrification and many studies exploit their amoA genes as marker for their diversity and abundance. We present an archaeal amoA consensus phylogeny based on all publicly available sequences (status June 2010) and provide evidence for the diversification of AOA into four previously recognized clusters and one newly identified major cluster. These clusters, for which we suggest a new nomenclature, harboured 83 AOA species‐level OTU (using an inferred species threshold of 85% amoA identity). 454 pyrosequencing of amoA amplicons from 16 soils sampled in Austria, Costa Rica, Greenland and Namibia revealed that only 2% of retrieved sequences had no database representative on the species‐level and represented 30–37 additional species‐level OTUs. With the exception of an acidic soil from which mostly amoA amplicons of the Nitrosotalea cluster were retrieved, all soils were dominated by amoA amplicons from the Nitrososphaera cluster (also called group I.1b), indicating that the previously reported AOA from the Nitrosopumilus cluster (also called group I.1a) are absent or represent minor populations in soils. AOA richness estimates on the species level ranged from 8–83 co‐existing AOAs per soil. Presence/absence of amoA OTUs (97% identity level) correlated with geographic location, indicating that besides contemporary environmental conditions also dispersal limitation across different continents and/or historical environmental conditions might influence AOA biogeography in soils.

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References 73

1. 1.

   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;5:908-917.

   Not in our library10.1038/ismej.2010.171

2. 2.

   Benson DA, Karsch-Mizrachi I, Lipman DJ, Ostell J, Sayers EW. GenBank. Nucleic Acids Res. 2011;39:D32-D37.

   Not in our library10.1093/nar/gkq1079

3. 3.
   Genome of a Low-Salinity Ammonia-Oxidizing Archaeon Determined by Single-Cell and Metagenomic Analysis · 2011

   No notice
4. 4.

   Brochier-Armanet C, Boussau B, Gribaldo S, Forterre P. Mesophilic crenarchaeota: proposal for a third archaeal phylum, the Thaumarchaeota. Nat Rev Microbiol. 2008;6:245-252.

   Not in our library10.1038/nrmicro1852

5. 5.
   BLAST+: architecture and applications · 2009

   No notice
6. 6.

   Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, et al. QIIME allows analysis of high-throughput community sequencing data. Nat Methods. 2010;7:335-336.

   Not in our library10.1038/nmeth.f.303

7. 7.

   Chou H-H, Holmes MH. DNA sequence quality trimming and vector removal. Bioinformatics. 2001;17:1093-1104.

   Not in our library10.1093/bioinformatics/17.12.1093

8. 8.

   De Caceres M, Legendre P. Associations between species and groups of sites: indices and statistical inference. Ecology. 2009;90:3566-3574.

   Not in our library10.1890/08-1823.1

9. 9.

   Delong EF. Archaea in coastal marine environments. Proc Natl Acad Sci USA. 1992;89:5685-5689.

   Not in our library10.1073/pnas.89.12.5685

10. 10.

    DeLong EF. Everything in moderation: Archaea as ‘non-extremophiles’. Curr Opin Genet Dev. 1998;8:649-654.

    Not in our library10.1016/s0959-437x(98)80032-4

11. 11.

    Di HJ, Cameron KC, Shen JP, Winefield CS, O'Callaghan M, Bowatte S, He JZ. Ammonia-oxidizing bacteria and archaea grow under contrasting soil nitrogen conditions. FEMS Microbiol Ecol. 2010;72:386-394.

    Not in our library10.1111/j.1574-6941.2010.00861.x

12. 12.

    Edgar RC. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 2004;32:1792-1797.

    Not in our library10.1093/nar/gkh340

13. 13.

    Erguder TH, Boon N, Wittebolle L, Marzorati M, Verstraete W. Environmental factors shaping the ecological niches of ammonia-oxidizing archaea. FEMS Microbiol Rev. 2009;33:855-869.

    Not in our library10.1111/j.1574-6976.2009.00179.x

14. 14.

    Felsenstein J. PHYLIP-phylogeny inference package. Cladistics. 1989;5:164-166.

    Not in our library

15. 15.

    Francis CA, Roberts KJ, Beman JM, Santoro AE, Oakley BB. Ubiquity and diversity of ammonia-oxidizing archaea in water columns and sediments of the ocean. Proc Natl Acad Sci USA. 2005;102:14683-14688.

    Not in our library10.1073/pnas.0506625102

16. 16.

    Frijlink MJ, Abee T, Laanbroek HJ, Deboer W, Konings WN. The bioenergetics of ammonia and hydroxylamine oxidation in Nitrosomonas europaea at acid and alkaline pH. Arch Microbiol. 1992;157:194-199.

    Not in our library

17. 17.

    Fuhrman JA, McCallum K, Davis AA. Novel major archaebacterial group from marine plankton. Nature. 1992;356:148-149.

    Not in our library10.1038/356148a0

18. 18.

    Gomez-Alvarez V, Teal TK, Schmidt TM. Systematic artifacts in metagenomes from complex microbial communities. ISME J. 2009;3:1314-1317.

    Not in our library10.1038/ismej.2009.72

19. 19.

    Good IJ. The population frequencies of species and the estimation of population parameters. Biometrika. 1953;40:237-264.

    Not in our library

20. 20.

    Goslee SC, Urban DL. The ecodist package for dissimilarity-based analysis of ecological data. J Stat Softw. 2007;22:1-19.

    Not in our library

21. 21.

    Gubry-Rangin C, Nicol GW, Prosser JI. Archaea rather than bacteria control nitrification in two agricultural acidic soils. FEMS Microbiol Ecol. 2010;74:566-574.

    Not in our library10.1111/j.1574-6941.2010.00971.x

22. 22.
    Pathways of Carbon Assimilation and Ammonia Oxidation Suggested by Environmental Genomic Analyses of Marine Crenarchaeota · 2006

    Corrected
23. 23.

    Hatzenpichler R, Lebedeva EV, Spieck E, Stoecker K, Richter A, Daims H, Wagner M. A moderately thermophilic ammonia-oxidizing crenarchaeote from a hot spring. Proc Natl Acad Sci USA. 2008;105:2134-2139.

    Not in our library10.1073/pnas.0708857105

24. 24.

    Herndl GJ, Reinthaler T, Teira E, van Aken H, Veth C, Pernthaler A, Pernthaler J. Contribution of archaea to total prokaryotic production in the deep Atlantic Ocean. Appl Environ Microbiol. 2005;71:2303-2309.

    Not in our library10.1128/aem.71.5.2303-2309.2005

25. 25.

    Hong S-H, Bunge J, Jeon S-O, Epstein SS. Predicting microbial species richness. Proc Natl Acad Sci USA. 2006;103:117-122.

    Not in our library10.1073/pnas.0507245102

26. 26.

    Huang Y, Niu B, Gao Y, Fu L, Li W. CD-HIT Suite: a web server for clustering and comparing biological sequences. Bioinformatics. 2010;26:680-682.

    Not in our library10.1093/bioinformatics/btq003

27. 27.

    Ingalls AE, Shah SR, Hansman RL, Aluwihare LI, Santos GM, Druffel ERM, Pearson A. Quantifying archaeal community autotrophy in the mesopelagic ocean using natural radiocarbon. Proc Natl Acad Sci USA. 2006;103:6442-6447.

    Not in our library10.1073/pnas.0510157103

28. 28.

    Jia Z, Conrad R. Bacteria rather than archaea dominate microbial ammonia oxidation in an agricultural soil. Environ Microbiol. 2009;11:1658-1671.

    Not in our library10.1111/j.1462-2920.2009.01891.x

29. 29.

    Kemnitz D, Kolb S, Conrad R. High abundance of Crenarchaeota in a temperate acidic forest soil. FEMS Microbiol Ecol. 2007;60:442-448.

    Not in our library10.1111/j.1574-6941.2007.00310.x

30. 30.

    Kim BK, Jung M-Y, Yu DS, Park S-J, Oh TK, Rhee S-K, Kim JF. Genome sequence of an ammonia-oxidizing soil archaeon, ‘Candidatus Nitrosoarchaeum koreensis’ MY1. J Bacteriol. 2011;193:5539-5540.

    Not in our library10.1128/jb.05717-11

31. 31.

    Kip N, Dutilh BE, Pan Y, Bodrossy L, Neveling K, Kwint MP, et al. Ultra-deep pyrosequencing of pmoA amplicons confirms the prevalence of Methylomonas and Methylocystis in Sphagnum mosses from a Dutch peat bog. Environ Microbiol Rep. 2011;3:667-673.

    Not in our library10.1111/j.1758-2229.2011.00260.x

32. 32.

    Könneke M, Bernhard AE, Torre JR, Walker CB, Waterbury JB, Stahl DA. Isolation of an autotrophic ammonia-oxidizing marine archaeon. Nature. 2005;437:543-546.

    Not in our library10.1038/nature03911

33. 33.

    Kunin V, Engelbrektson A, Ochman H, Hugenholtz P. Wrinkles in the rare biosphere: pyrosequencing errors can lead to artificial inflation of diversity estimates. Environ Microbiol. 2009;12:118-123.

    Not in our library10.1111/j.1462-2920.2009.02051.x

34. 34.

    Lehtovirta-Morley LE, Stoecker K, Vilcinskas A, Prosser JI, Nicol GW. Cultivation of an obligate acidophilic ammonia oxidizer from a nitrifying acid soil. Proc Natl Acad Sci USA. 2011;108:15892-15897.

    Not in our library10.1073/pnas.1107196108

35. 35.

    Leininger S, Urich T, Schloter M, Schwark L, Qi J, Nicol GW, et al. Archaea predominate among ammonia-oxidizing prokaryotes in soils. Nature. 2006;442:806-809.

    Not in our library10.1038/nature04983

36. 36.

    Ludwig W, Strunk O, Klugbauer S, Klugbauer N, Weizenegger M, Neumaier J, et al. Bacterial phylogeny based on comparative sequence analysis. Electrophoresis. 1998;19:554-568.

    Not in our library10.1002/elps.1150190416

37. 37.

    Ludwig W, Strunk O, Westram R, Richter L, Meier H, et al. ARB: a software environment for sequence data. Nucleic Acids Res. 2004;32:1363-1371.

    Not in our library10.1093/nar/gkh293

38. 38.

    Lüke C, Frenzel P. Potential of pmoA amplicon pyrosequencing for methanotroph diversity studies. Appl Environ Microbiol. 2011;77:6305-6309.

    Not in our library10.1128/aem.05355-11

39. 39.

    Markowitz VM, Ivanova NN, Szeto E, Palaniappan K, Chu K, Dalevi D, et al. IMG/M: a data management and analysis system for metagenomes. Nucleic Acids Res. 2008;36:D534-D538.

    Not in our library10.1093/nar/gkm869

40. 40.

    Martens-Habbena W, Berube PM, Urakawa H, Torre JR, Stahl DA. Ammonia oxidation kinetics determine niche separation of nitrifying Archaea and Bacteria. Nature. 2009;461:976-979.

    Not in our library10.1038/nature08465

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