Global biodiversity of aquatic ammonia-oxidizing archaea: Is partitioned by habitat

Frontiers in Microbiology

Volumn 3, Issue JUL, 2012, Pages

  Biller, Steven J ^a,c   Mosier, Annika C ^a,d   Wells, George F ^b,e   Francis, Christopher A ^a  

^a STANFORD UNIVERSITY   (United States)

^b Stanford University   (United States)

^c Massachusetts Institute of Technology Cambridge   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

^e SWISS FEDERAL INSTITUTE OF AQUATIC SCIENCE AND TECHNOLOGY   (Switzerland)

Author keywords

Ammonia oxidizing archaea; amoA; Biogeography; Nitrification; Thaumarchaeota

Indexed keywords

EID: 84874550637     PISSN: None     EISSN: 1664302X     Source Type: Journal    
DOI: 10.3389/fmicb.2012.00252     Document Type: Article

References (55)

1. Agogué,H.,Brink,M.,Dinasquet,J.,and Herndl, G. J. (2008). Major gradi-ents in putatively nitrifying and non-nitrifying archaea in the deep North Atlantic. Nature 456, 788-791.
2. Beman, J., Popp, B., and Francis, C. (2008). Molecular and biogeochem-ical evidence for ammonia oxidation by marine crenarchaeota in the Gulf of California. ISME J. 2, 429-441.
3. Beman, J. M., Sachdeva, R., and Fuhrman, J. A. (2010). Population ecology of nitrifying archaea and bacteria in the Southern California bight. Environ. Microbiol. 12, 1282-1292.
4. Blainey, P. C., Mosier, A. C., Potan-ina, A., Francis, C. A., and Quake, S. R. (2011). Genome of a low-salinity ammonia-oxidizing archaeon determined by single-cell and metagenomic analysis. PLoS ONE 6, e16626. doi:10.1371/journal.pone.0016626
5. Brochier-Armanet, C., Boussau, B., Gribaldo, S., and Forterre, P. (2008). Mesophilic crenarchaeota: proposal for a third archaeal phylum, the Thaumarchaeota. Nat. Rev. Microbiol. 6, 245-252.
6. Church, M. J., Wai, B., Karl, D. M., and Delong, E. F. (2010). Abundances of crenarchaeal amoA genes and transcripts in the Pacific Ocean. Environ. Microbiol. 12, 679-688.
7. De La Torre, J., Walker, C., Ingalls, A., Konneke, M., and Stahl, D. (2008). Cultivation of a thermophilic ammonia oxidizing archaeon syn-thesizing crenarchaeol. Environ. Microbiol. 10, 810-818.
8. Erguder, T. H., Boon, N., Wittebolle, L., Marzorati, M., and Verstraete, W. (2009). Environmental factors shaping the ecological niches of ammonia-oxidizing archaea. FEMS Microbiol. Rev. 33, 855-869.
9. Francis, C. A., Beman, J. M., and Kuypers, M. M. (2007). New processes and players in the nitro-gen cycle: the microbial ecology of anaerobic and archaeal ammonia oxidation. ISME J. 1, 19-27.
10. Francis, C. A., Roberts, K. J., Beman, J. M., Santoro, A. E., and Oakley, B. B. (2005). Ubiquity and diversity of ammonia-oxidizing archaea in water columns and sediments of the ocean. Proc. Natl. Acad. Sci. U.S.A. 102, 14683-14688.
11. Gubry-Rangin, C., Hai, B., Quince, C., Engel, M., Thomson, B. C., James, P., Schloter, M., Griffiths, R. I., Prosser, J. I., and Nicol, G. W. (2011). Niche specialization of terrestrial archaeal ammonia oxidizers. Proc. Natl. Acad. Sci. U.S.A. 108, 21206-21211.
12. Guindon, S., and Gascuel, O. (2003). A simple, fast, and accurate algo-rithm to estimate large phylogenies by maximum likelihood. Syst. Biol. 52, 696-704.
13. Hallam, S., Mincer, T., Schleper, C., Preston, C., Roberts, K., Richardson, P., and Delong, E. (2006). Pathways of carbon assimilation and ammonia oxidation suggested by environ-mental genomic analyses of marine crenarchaeota. PLoS Biol. 4, e95. doi:10.1371/journal.pbio.0040095
14. Hamady, M., Lozupone, C., and Knight, R. (2010). Fast uniFrac: facilitat-ing high-throughput phylogenetic analyses of microbial communities including analysis of pyrosequenc-ing and phylochip data. ISME J. 4, 17-27.
15. Hansel, C., Fendorf, S., Jardine, P., and Francis,C. (2008). Changes in bacterial and archaeal community structure and functional diversity along a geochemically variable soil pro-file. Appl. Environ. Microbiol. 74, 1620-1633.
16. Hatzenpichler, R., Lebedeva, E., Spieck, E., Stoecker, K., Richter, A., Daims, H., and Wagner, M. (2008). A moderately thermophilic ammonia-oxidizing crenarchaeote from a hot spring. Proc. Natl. Acad. Sci. U.S.A. 105, 2134-2139.
17. He, J., Shen, J., Zhang, L., Zhu, Y., Zheng, Y., Xu, M., and Di, H. (2007). Quantitative analyses of the abundance and composition of ammonia-oxidizing bacteria and ammonia-oxidizing archaea of a Chinese upland red soil under long-term fertilization practices. Environ. Microbiol. 9, 2364-2374.
18. Hu, A., Jiao, N., Zhang, R., and Yang, Z. (2011). Niche partitioning of marine group I crenarchaeota in the euphotic and upper mesopelagic zones of the East China Sea. Appl. Environ. Microbiol. 77, 7469-7478.
19. Hunt, D. E., David, L. A., Gevers, D., Preheim, S. P., Alm, E. J., and Polz, M. F. (2008). Resource parti-tioning and sympatric differentiation among closely related bacteri-oplankton. Science 320, 1081-1085
20. Jia, Z., and Conrad, R. (2009). Bacteria rather than archaea dominate microbial ammonia oxidation in an agricultural soil. Environ. Microbiol. 11, 1658-1671.
21. Jung, M. Y., Park, S. J., Min, D., Kim, J. S., Rijpstra, W. I., Sinninghe Damste, J. S., Kim, G. J., Mad-sen, E. L., and Rhee, S. K. (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.
22. Kalanetra, K. M., Bano, N., and Hollibaugh, J. T. (2009). Ammonia-oxidizing archaea in the Arctic Ocean and Antarctic coastal waters. Environ. Microbiol. 11, 2434-2445.
23. Könneke, M., Bernhard, A., De La Torre, J., Walker, C., Waterbury, J., and Stahl, D. (2005). Isolation of an autotrophic ammonia-oxidizing marine archaeon. Nature 437, 543-546.
24. Kosakovsky Pond, S. L., and Frost, S. D. W. (2005). Not so different after all: a comparison of methods for detect-ing amino acid sites under selection. Mol. Biol. Evol. 22, 1208-1222.
25. Kryazhimskiy, S., and Plotkin, J. B. (2008). The population genetics of dN/dS. PLoS Genet. 4, e1000304. doi:10.1371/journal.pgen.1000304
26. Lam, P., Lavik, G., Jensen, M., Van De Vossenberg, J., Schmid, M., Woe-bken, D., Gutierrez, D., Amann, R., Jetten, M., and Kuypers, M. (2009). Revising the nitrogen cycle in the Peruvian oxygen minimum zone. Proc. Natl. Acad. Sci. U.S.A. 106, 4752-4757.
27. Lehtovirta-Morley, L. E., Stoecker, K., Vilcinskas,A.,Prosser,J. I.,and Nicol, G. W. (2011). Cultivation of an obligate acidophilic ammonia oxi-dizer from a nitrifying acid soil. Proc. Natl. Acad. Sci. U.S.A. 108, 15892-15897.
28. Leininger, S., Urich, T., Schloter, M., Schwark, L., Qi, J., Nicol, G., Prosser, J., Schuster, S., and Schleper, C. (2006). Archaea predomi-nate among ammonia-oxidizing prokaryotes in soils. Nature 442, 806-809.
29. Letunic, I., and Bork, P. (2007). Interactive tree of life (itol): an online tool for phylogenetic tree display and annotation. Bioinformatics 23, 127-128.
30. Lozupone, C. A., and Knight, R. (2007). Global patterns in bacterial diversity. Proc. Natl. Acad. Sci.U.S.A. 104, 11436-11440.
31. Ludwig, W., Strunk, O., Westram, R., Richter, L., Meier, H., Yadhukumar, Buchner, A., Lai, T., Steppi, S., Jobb, G., Forster, W., Brettske, I., Gerber, S., Ginhart, A., Gross, O., Grumann, S., Hermann, S., Jost, R., Konig, A., Liss,T.,Lussmann,R.,May,M.,Non-hoff, B., Reichel, B., Strehlow, R.,Stamatakis, A., Stuckmann, N., Vilbig, A., Lenke, M., Ludwig, T., Bode, A., and Schleifer, K. (2004). ARB: a soft-ware environment for sequence data. Nucleic Acids Res. 32, 1363-1371.
32. Miller, M., Holder, M., Vos, R., Midford, P., Liebowitz, T., Chan, L., Hoover, P., and Warnow, T. (2009). The CIPRES Portals. Available at: http://www.phylo.org/sub_sections/ portal [Accessed: 2009-08-04]. (Archived by WebCite(r) at http:// www.webcitation.org/5imQlJeQa) [Online]. [Accessed].
33. Mincer, T. J., Church, M. J., Taylor, L. T., Preston, C., Karl, D. M., and Delong, E. F. (2007). Quantitative distribution of presumptive archaeal and bacterial nitrifiers in Monterey Bay and the North Pacific Sub-tropical Gyre. Environ. Microbiol. 9, 1162-1175.
34. Moin, N. S., Nelson, K. A., Bush, A., and Bernhard, A. E. (2009). Distribution and diversity of archaeal and bacterial ammonia oxidizers in salt marsh sediments. Appl. Environ. Microbiol. 75, 7461-7468.
35. Mosier, A. C., and Francis, C. A. (2008). Relative abundance and diversity of ammonia-oxidizing archaea and bacteria in the San Francisco Bay estuary. Environ. Microbiol. 10, 3002-3016.
36. Mosier, A. C., and Francis, C. A. (2011). Determining the distribution of marine and coastal ammonia-oxidizing archaea and bacteria using a quantitative approach. Meth. Enzymol. 486, 205-221.
37. Mosier, A. C., Lund, M. B., and Francis, C. A. (2012). Ecophysiology of an ammonia-oxidizing archaeon adapted to low-salinity habitats. Microb. Ecol. doi: 10.1007/s00248-012-0075-1
38. Mussmann, M., Brito, I., Pitcher, A., Sinninghe Damsté, J. S., Hatzen-pichler, R., Richter, A., Nielsen, J. L., Nielsen, P. H., Müller, A., Daims, H., Wagner, M., and Head, I. M. (2011). Thaumarchaeotes abundant in refinery nitrifying sludges express amoA but are not obligate autotrophic ammonia oxidizers. Proc. Natl. Acad. Sci. U.S.A. 108, 16771-16776.
39. Oksanen, J., Blanchet, F. G., Kindt, R., Legendre, P., Ohara, R. B., Simpson, G. L., Solymos, P., Henry, M., Stevens, H., and Wagner, H. (2010). Vegan: Community Ecol-ogy Package. R Package Version 1.17-3. Available at: http://CRAN.R-project.org/package=vegan
40. Park, H., Wells, G., Bae, H., Criddle, C., and Francis, C. (2006). Occurrence of ammonia-oxidizing archaea in wastewater treatment plant bioreactors. Appl. Environ. Microbiol. 72, 5643-5647.
41. Pester, M., Rattei, T., Flechl, S., Gröngröft, A., Richter, A., Over-mann, J., Reinhold-Hurek, B., Loy, A., and 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.
42. Pond, S. L., and Frost, S. D. (2005). Data-monkey: rapid detection of selec-tive pressure on individual sites of codon alignments. Bioinformatics 21, 2531-2533.
43. Pond, S. L., Frost, S. D., and Muse, S. V. (2005). HyPhy: hypothesis test-ing using phylogenies. Bioinformatics 21, 676-679.
44. Santoro, A. E., Francis, C. A., De Sieyes, N. R., and Boehm, A. B. (2008). Shifts in the relative abundance of ammonia-oxidizing bacteria and archaea across physicochemical gradients in a subterranean estuary. Environ. Microbiol. 10, 1068-1079.
45. Santoro, A. E., Casciotti, K. L., and Francis, C. A. (2010). Activity, abun-dance, and diversity of nitrifying archaea and bacteria in the central California current. Environ. Microbiol. 12, 1989-2006.
46. Schloss, P. D., Westcott, S. L., Ryabin, T., Hall, J. R., Hartmann, M., Hollister, E. B., Lesniewski, R. A., Oakley, B. B., Parks, D. H., Robinson, C. J., Sahl, J. W., Stres, B., Thallinger, G. G., Van Horn, D. J., and Weber, C. F. (2009). Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl. Environ. Microbiol. 75, 7537-7541.
47. Stamatakis, A. (2006). RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22, 2688-2690.
48. Tamura, K., Dudley, J., Nei, M., and Kumar, S. (2007). MEGA4: molec-ular evolutionary genetics analysis (mega) software version 4.0. Mol. Biol. Evol. 24, 1596-1599.
49. Tourna, M., Stieglmeier, M., Spang, A., Konneke, M., Schintlmeister, A., Urich, T., Engel, M., Schloter, M., Wagner, M., Richter, A., and Schleper, C. (2011). Nitrososphaera viennensis, an ammonia oxidizing archaeon from soil. Proc. Natl. Acad. Sci. U.S.A. 108, 8420-8425.
50. Treusch, A., Leininger, S., Kletzin, A., Schuster, S., Klenk, H., and Schleper, C. (2005). Novel genes for nitrite reductase and amo-related proteins indicate a role of uncultivated mesophilic crenarchaeota in nitrogen cycling. Environ. Microbiol. 7, 1985-1995.
51. Venter, J., Remington, K., Heidelberg, J., Halpern, A., Rusch, D., Eisen, J., Wu, D., Paulsen, I., Nelson, K., Nelson, W., Fouts, D., Levy, S., Knap, A., Lomas, M., Neal-son, K., White, O., Peterson, J., Hoffman, J., Parsons, R., Baden-Tillson, H., Pfannkoch, C., Rogers, Y., and Smith, H. (2004). Environmental genome shotgun sequenc-ing of the Sargasso Sea. Science 304, 66-74.
52. Wankel, S. D., Mosier, A. C., Hansel, C. M., Paytan, A., and Francis, C. A. (2011). Spatial variability in nitrifi-cation rates and ammonia-oxidizing microbial communities in the agri-culturally impacted Elkhorn Slough estuary, California. Appl. Environ. Microbiol. 77, 269-280.
53. Wells, G. F., Park, H.-D., Yeung, C.-H., Eggleston, B., Francis, C. A., and Criddle, C. S. (2009). Ammonia-oxidizing communities in a highly aerated full-scale activated sludge bioreactor: betaproteobacterial dynamics and low relative abun-dance of crenarchaea. Environ. Microbiol. 11, 2310-2328.
54. Yilmaz, P., Kottmann, R., Field, D., Knight, R., Cole, J. R., Amaral-Zettler, L., Gilbert, J. A., Karsch-Mizrachi, I., Johnston, A., Cochrane, G., Vaughan, R., Hunter, C., Park, J., Morrison, N., Rocca-Serra, P., Sterk, P., Arumugam, M., Bailey, M., Baumgartner, L., Birren, B. W., Blaser, M. J., Bonazzi, V., Booth, T., Bork, P., Bushman, F. D., Buttigieg, P. L., Chain, P. S. G., Charlson, E., Costello, E. K., Huot-Creasy, H., Dawyndt, P., Desantis, T., Fierer, N., Fuhrman,J. A.,Gallery,R. E.,Gevers, D.,Gibbs,R. A.,San Gil,I.,Gonzalez, A., Gordon, J. I., Guralnick, R., Hankeln,W.,Highlander, S., Hugenholtz, P., Jansson, J., Kau, A. L., Kelley, S. T., Kennedy, J., Knights, D., Koren, O., Kuczynski, J., Kyrpides, N., Larsen, R., Lauber, C. L., Legg, T., Ley, R. E., Lozupone, C. A., Ludwig, W., Lyons, D., Maguire, E., Methé, B. A., Meyer, F., Muegge, B., Nakielny, S., Nelson,K. E.,Nemergut,D.,Neufeld, J. D., Newbold, L. K., Oliver, A. E., Pace, N. R., Palanisamy, G., Peplies, J., Petrosino, J., Proctor, L., Pruesse, E., Quast, C., Raes, J., Ratnasing-ham, S., Ravel, J., Relman, D. A., Assunta-Sansone, S., Schloss, P. D., Schriml, L., Sinha, R., Smith, M. I., Sodergren, E., Spo, A., Stombaugh, J., Tiedje, J. M., Ward, D. V., Wein-stock, G. M., Wendel, D., White, O., Whiteley, A., Wilke, A., Wort-man, J. R., Yatsunenko, T., and Glöckner, F. O. (2011). Minimum information about a marker gene sequence (MIMARKS) and minimum information about any (x) sequence (MIxS) specifications. Nat. Biotechnol. 29, 415-420.
55. Zhang, L.-M., Offre, P. R., He, J.-Z., Verhamme, D. T., Nicol, G. W., and Prosser, J. I. (2010). Autotrophic ammonia oxidation by soil thaumarchaea. Proc. Natl. Acad. Sci. U.S.A. 107, 17240-17245.