Seasonal changes of freshwater ammonia-oxidizing archaeal assemblages and nitrogen species in oligotrophic alpine lakes

Applied and Environmental Microbiology

Volumn 77, Issue 6, 2011, Pages 1937-1945

  Auguet, Jean Christophe ^a   Nomokonova, Natalya ^a   Camarero, Lluis ^a   Casamayor, Emilio O ^a  

^a CENTRE D ESTUDIS AVANÇATS DE BLANES CEAB CSIC   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

16S RRNA; 16S RRNA GENE; 16S RRNA GENE SEQUENCE; ALPINE LAKES; AMMONIA OXIDATION; ANNUAL CHANGE; ARCHAEA; ARCHAEAL; ASSEMBLAGE STRUCTURE; BIOLOGICAL DATA; COPY NUMBER; CRENARCHAEOTA; ECOLOGICAL NICHE; ENVIRONMENTAL VARIABLES; FRESHWATER HABITATS; GENE SEQUENCES; GENE SEQUENCING; GENETIC DIVERGENCE; HIGH MOUNTAINS; MONOOXYGENASES; NITROGEN SPECIES; NORTHEAST SPAIN; PHYLOTYPES; PYRENEES; QUANTITATIVE PCR; SEASONAL CHANGES; STRUCTURAL CHANGE; TEMPORAL CHANGE; WATER TEMPERATURES;

AMINO ACIDS; AMMONIA; AMMONIUM COMPOUNDS; LAKES; OXIDATION; POLYMERASE CHAIN REACTION; RNA;

GENES;

AMMONIA; AMMONIA MONOOXYGENASE; FRESH WATER; NITROGEN; OXIDOREDUCTASE; RNA 16S;

ABUNDANCE; ALPINE ENVIRONMENT; AMMONIA; BACTERIUM; CLUSTER ANALYSIS; COMMUNITY COMPOSITION; DIVERGENCE; ECOLOGICAL APPROACH; ECOTYPE; FRESHWATER ENVIRONMENT; GENE EXPRESSION; GENETIC ANALYSIS; LAKE; LIMNOLOGY; MOUNTAIN REGION; NITROGEN; OLIGOTROPHIC ENVIRONMENT; OXIDATION; PHYLOGENETICS; POLYMERASE CHAIN REACTION; QUANTITATIVE ANALYSIS; SEASONAL VARIATION; SURFACE WATER; WATER TEMPERATURE;

ARCHAEBACTERIUM; ARTICLE; BIODIVERSITY; CLASSIFICATION; GENETICS; METABOLISM; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PHYLOGENY; POLYMERASE CHAIN REACTION; SEASON; SPAIN;

AMMONIA; ARCHAEA; BIODIVERSITY; FRESH WATER; MOLECULAR SEQUENCE DATA; NITROGEN; OXIDOREDUCTASES; PHYLOGENY; POLYMERASE CHAIN REACTION; RNA, RIBOSOMAL, 16S; SEASONS; SPAIN;

PYRENEES;

ARCHAEA; CRENARCHAEOTA;

EID: 79953221862     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.01213-10     Document Type: Article

References (68)

1. Agogue, H., et al. 2004. Comparison of samplers for the biological characterization of the sea surface microlayer. Limnol. Oceanogr. Methods 2:213-225.
2. Altschul, S. F., W. Gish, W. Miller, E. W. Myers, and D. J. Lipman. 1990. Basic local alignment search tool. J. Mol. Biol. 215:403-410.
3. Auguet, J.-C., A. Barberan, and E. O. Casamayor. 2010. Global ecological patterns in uncultured Archaea. ISME J. 4:182-190.
4. Auguet, J. C., and E. O. Casamayor. 2008. A hotspot for cold crenarchaeota in the neuston of high mountain lakes. Environ. Microbiol. 10:1080-1086.
5. Barberan, A., and E. O. Casamayor. 2010. Global phylogenetic community structure and beta-diversity patterns of surface bacterioplankton metacommunities. Aquat. Microb. Ecol. 59:1-10.
6. Beman, J. M., B. N. Popp, and C. A. Francis. 2008. Molecular and biogeochemical evidence for ammonia oxidation by marine Crenarchaeota in the Gulf of California. ISME J. 2:429-441.
7. Beman, J. M., R. Sachdeva, and J. A. Fuhrman. 2010. Population ecology of nitrifying Archaea and Bacteria in the southern California bight. Environ. Microbiol. 12:1282-1292.
8. Bollmann, A., M. J. Bar-Gilissen, and H. J. Laanbroek. 2002. Growth at low ammonium concentrations and starvation response as potential factors involved in niche differentiation among ammonia-oxidizing bacteria. Appl. Environ. Microbiol. 68:4751-4757.
9. Bothe, H., G. Jost, M. Schloter, B. B. Ward, and K. P. Witzel. 2000. Molecular analysis of ammonia oxidation and denitrification in natural environments. FEMS Microbiol. Rev. 24:673-690.
10. Camarero, L., and J. Catalan. 1993. Chemistry of bulk precipitation in the central and eastern pyrenees, northeast spain. Atmos. Environ. A Gen. Topics 27:83-94.
11. Campanella, J. J., L. Bitincka, and J. Smalley. 2003. MatGAT: an application that generates similarity/identity matrices using protein or DNA sequences. BMC Bioinformatics 4:29.
12. Casamayor, E. O., G. Muyzer, and C. Pedros Alio. 2001. Composition and temporal dynamics of planktonic archaeal assemblages from anaerobic sulfurous environments studied by 16S rDNA denaturing gradient gel electrophoresis and sequencing. Aquat. Microb. Ecol. 25:237-246.
13. Casamayor, E. O., H. Schafer, L. Baneras, C. Pedros-Alio, and G. Muyzer. 2000. Identification of and spatio-temporal differences between microbial assemblages from two neighboring sulfurous lakes: comparison by microscopy and denaturing gradient gel electrophoresis. Appl. Environ. Microbiol. 66:499-508.
14. Castresana, J. 2000. Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Mol. Biol. Evol. 17:540-552.
15. Catalan, J., L. Camarero, E. Gacia, E. Ballesteros, and M. Felip. 1994. Nitrogen in the Pyrenean lakes (Spain). Hydrobiologia 274:17-27.
16. Catalan, J., et al. 2002. Lake Redó ecosystem response to an increasing warming the Pyrenees during the twentieth century. J. Paleolimnol. 28:129-145.
17. Church, M. J., B. Wai, D. M. Karl, and E. F. DeLong. 2010. Abundances of crenarchaeal amoA genes and transcripts in the Pacific Ocean. Environ. Microbiol. 12:679-688.
18. DeLong, E. 1992. Archaea in coastal marine environments. Proc. Natl. Acad. Sci. U. S. A. 89:5685-5689.
19. DeSantis, T. Z., et al. 2006. Greengenes, a chimera-checked 16S rRNA gene database and workbench compatible with ARB. Appl. Environ. Microbiol. 72:5069-5072.
20. Dumestre, J. F., E. O. Casamayor, R. Massana, and C. Pedros-Alio. 2002. Changes in bacterial and archaeal assemblages in an equatorial river induced by the water eutrophication of Petit Saut dam reservoir (French Guiana). Aquatic Microb. Ecol. 26:209-221.
21. Erguder, T. H., N. Boon, L. Wittebolle, M. Marzorati, and W. Verstraete. 2009. Environmental factors shaping the ecological niches of ammoniaoxidizing archaea. FEMS Microbiol. Rev. 33:855-869.
22. Faith, D. P. 1992. Conservation evaluation and phylogenetic diversity. Biol. Conserv. 61:1-10.
23. Ferrera, I., et al. 2004. High-diversity biofilm for the oxidation of sulfidecontaining effluents. Appl. Microbiol. Biotechnol. 64:726-734.
24. Francis, C. A., J. M. Beman, and M. M. M. Kuypers. 2007. New processes and players in the nitrogen cycle: the microbial ecology of anaerobic and archaeal ammonia oxidation. ISME J. 1:19-27.
25. Francis, C. A., K. J. Roberts, J. M. Beman, A. E. Santoro, and B. B. Oakley. 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.
26. Galand, P. E., C. Lovejoy, and W. F. Vincent. 2006. Remarkably diverse and contrasting archaeal communities in a large arctic river and the coastal Arctic Ocean. Aquat. Microb. Ecol. 44:115-126.
27. Hall, T. A. 1999. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp. Ser. 41:95-98.
28. 2O in the Cariaco Trench. Deep-Sea Res. A Oceanogr. Res. Papers 30:575-590.
29. He, J. Z., et al. 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.
30. Helmus, M. R., T. J. Bland, C. K. Williams, and A. R. Ives. 2007. Phylogenetic measures of biodiversity. Am. Nat. 169:E68-E83.
31. Herfort, L., et al. 2009. Diversity of Archaea and detection of crenarchaeotal amoA genes in the rivers Rhine and Tet. Aquat. Microb. Ecol. 55:189-201.
32. Herfort, L., et al. 2007. Variations in spatial and temporal distribution of Archaea in the North Sea in relation to environmental variables. FEMS Microbiol. Ecol. 62:242-257.
33. Herrmann, M., A. M. Saunders, and A. Schramm. 2009. Effect of lake trophic status and rooted macrophytes on community composition and abundance of ammonia-oxidizing prokaryotes in freshwater sediments. Appl. Environ. Microbiol. 75:3127-3136.
34. Hervàs, A., L. Camarero, I. Reche, and E. O. Casamayor. 2009. Viability and potential for immigration of airborne bacteria from Africa that reach high mountain lakes in Europe. Environ. Microbiol. 11:1612-1623.
35. Katoh, K., G. Asimenos, and H. Toh. 2009. Multiple alignment of DNA sequences with MAFFT, p. 39-64. In D. Posada (ed.), Bioinformatics for DNA sequence analysis. Springer, New York, NY.
36. Kemp, P. F., and J. Y. Aller. 2004. Estimating prokaryotic diversity: when are 16S rDNA libraries large enough? Limnol. Oceanogr. Methods 2:114-125.
37. Könneke, M., et al. 2005. Isolation of an autotrophic ammonia-oxidizing marine archaeon. Nature 437:543-546.
38. Koops, H. P., and A. Pommerening-Roser. 2001. Distribution and ecophysiology of the nitrifying bacteria emphasizing cultured species. FEMS Microbiol. Ecol. 37:1-9.
39. Lam, P., et al. 2007. Linking crenarchaeal and bacterial nitrification to anammox in the Black Sea. Proc. Natl. Acad. Sci. U. S. A. 104:7104-7109.
40. Leininger, S., et al. 2006. Archaea predominate among ammonia-oxidizing prokaryotes in soils. Nature 442:806-809.
41. Letunic, I., and P. Bork. 2007. Interactive tree of life (iTOL): an online tool for phylogenetic tree display and annotation. Bioinformatics 23:127-128.
42. Li, W., and A. Godzik. 2006. Cd-hit: a fast program for clustering and comparing large sets of protein or nucleotide sequences. Bioinformatics 22:1658-1659.
43. Llirós, M., E. O. Casamayor, and C. M. Borrego. 2008. High archaeal richness in the water column of a freshwater sulfurous karstic lake along an interannual study. FEMS Microbiol. Ecol. 66:331-342.
44. Llirós, M., et al. Vertical distribution of ammonia-oxidizing crenarchaeota and methanogens in the epipelagic waters of Lake Kivu. Appl. Environ. Microbiol. 76:6853-6863.
45. Lozupone, C., M. Hamady, and R. Knight. 2006. UniFrac-an online tool for comparing microbial community diversity in a phylogenetic context. BMC Bioinformatics 7:371.
46. Ludwig, W., et al. 2004. ARB: a software environment for sequence data. Nucleic Acids Res. 32:1363-1371.
47. Martens-Habbena, W., P. M. Berube, H. Urakawa, J. R. de la Torre, and D. A. Stahl. 2009. Ammonia oxidation kinetics determine niche separation of nitrifying Archaea and Bacteria. Nature 461:U976-U234.
48. McArdle, B. 2001. Fitting multivariate models to community data: a comment on distance-based redundancy analysis. Ecology 82:290-297.
49. Mosier, A. C., and C. A. Francis. 2008. Relative abundance and diversity of ammonia-oxidizing archaea and bacteria in the San Francisco Bay estuary. Environ. Microbiol. 10:3002-3016.
50. Muyzer, G., E. C. De Waal, and A. G. Uitterlinden. 1993. Profiling of complex microbial populations by denaturing gradient gel electrophoresis analysis of polymerase chain reaction-amplified genes coding for 16S rRNA. Appl. Environ. Microbiol. 59:695-700.
51. Nicol, G. W., S. Leininger, C. Schleper, and J. I. Prosser. 2008. The influence of soil pH on the diversity, abundance and transcriptional activity of ammonia oxidizing archaea and bacteria. Environ. Microbiol. 10:2966-2978.
52. Olson, R. J. 1981. 15N tracer studies of the primary nitrite maximum. J. Mar. Res. 39:203-226.
53. Pernthaler, A., J. Pernthaler, and R. Amann. 2002. Fluorescence in situ hybridization and catalyzed reporter deposition for the identification of marine bacteria. Appl. Environ. Microbiol. 68:3094-3101.
54. Pernthaler, J., et al. 1998. Seasonal community and population dynamics of pelagic bacteria and archaea in a high mountain lake. Appl. Environ. Microbiol. 64:4299-4306.
55. Pouliot, J., P. E. Galand, C. Lovejoy, and W. F. Vincent. 2009. Vertical structure of archaeal communities and the distribution of ammonia monooxygenase A gene variants in two meromictic high arctic lakes. Environ. Microbiol. 11:687-699.
56. Prosser, J. I., and G. W. Nicol. 2008. Relative contributions of archaea and bacteria to aerobic ammonia oxidation in the environment. Environ. Microbiol. 10:2931-2941.
57. Reed, D. W., J. M. Smith, C. A. Francis, and Y. Fujita. 2010. Responses of ammonia-oxidizing bacterial and archaeal populations to organic nitrogen amendments in low-nutrient groundwater. Appl. Environ. Microbiol. 76: 2517-2523.
58. Sahan, E. 2008. Diversity and spatio-temporal distribution of ammoniaoxidizing Archaea and Bacteria in sediments of the Westerschelde estuary. FEMS Microbiol. Ecol. 64:175-186.
59. Santoro, A. E., K. L. Casciotti, and C. A. Francis. 2010. Activity, abundance and diversity of nitrifying archaea and bacteria in the central California current. Environ. Microbiol. 12:1989-2006.
60. Shaw, A. 2008. It's all relative: ranking the diversity of aquatic bacterial communities. Environ. Microbiol. 10:2200-2210.
61. Shen, J. P., L. M. Zhang, Y. G. Zhu, J. B. Zhang, and J. Z. He. 2008. Abundance and composition of ammonia-oxidizing bacteria and ammoniaoxidizing archaea communities of an alkaline sandy loam. Environ. Microbiol. 10:1601-1611.
62. Solórzano, L. 1969. Determination of ammonia in natural waters by the phenolhypochlorite method. Limnol. Oceanogr. 14:799-801.
63. Stamatakis, A., P. Hoover, and J. Rougemont. 2008. A rapid bootstrap algorithm for the RAxML web-servers. Syst. Biol. 75:758-771.
64. Takai, K., et al. 2004. Spatial distribution of marine crenarchaeota group I in the vicinity of deep-sea hydrothermal systems. Appl. Environ. Microbiol. 70:2404-2413.
65. Treusch, A. H., et al. 2005. Novel genes for nitrite reductase and Amorelated proteins indicate a role of uncultivate mesophilic crenarchaeota in nitrogen cycling. Environ. Microbiol. 7:1985-1995.
66. van der Wielen, P., S. Voost, and D. van der Kooij. 2009. Ammonia-oxidizing bacteria and archaea in groundwater treatment and drinking water distribution systems. Appl. Environ. Microbiol. 75:4687-4695.
67. Venter, J. C., et al. 2004. Environmental genome shotgun sequencing of the Sargasso Sea. Science 304:66-74.
68. Wuchter, C., et al. 2006. Archaeal nitrification in the ocean. Proc. Natl. Acad. Sci. U. S. A. 103:12317-12322.