Diversity and stratification of archaea in a hypersaline microbial Mat

Applied and Environmental Microbiology

Volumn 75, Issue 7, 2009, Pages 1801-1810

  Robertson, Charles E ^a   Spear, John R ^b   Harris, J Kirk ^c   Pace, Norman R ^a  

^a UNIVERSITY OF COLORADO   (United States)

^b Department of Metallurgical and Materials Engineering   (United States)

^c University of Colorado Denver and Children s Hospital Colorado   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARCHAEA; ARCHAEAL; ARCHAEON; BIOGEOCHEMICAL STUDIES; BULK CONTRIBUTIONS; CALIFORNIA; CHEMICAL GRADIENTS; HYPERSALINE; ME-XICO; METABOLIC ACTIVITIES; MICROBIAL MATS; MOLECULAR SURVEYS; PACIFIC OCEANS; PCR PRIMERS; PHYLOGENETIC DISTRIBUTIONS; PHYLOTYPES; RRNA GENES; STUDY SITES; UNDER SAMPLINGS;

BACTERIOLOGY; BIODIVERSITY; BIOGEOCHEMISTRY; COSMIC RAYS; LAKES; METABOLISM; OCEAN ENGINEERING; OCEANOGRAPHY; SOLAR PONDS;

GENES;

BACTERIAL RNA; RIBOSOME RNA; SODIUM CHLORIDE;

DOMINANCE; EUKARYOTE; HYPERSALINE ENVIRONMENT; METABOLISM; MICROBIAL MAT; MOLECULAR ANALYSIS; PHOTOSYNTHESIS; PHYLOGENETICS; POLYMERASE CHAIN REACTION; POND; PROKARYOTE; RNA; SALINITY; SPECIES DIVERSITY; STRATIFICATION;

ARCHAEBACTERIUM; ARTICLE; BACTERIAL GENE; CLADISTICS; CRENARCHAEOTA; EUKARYOTE; EURYARCHAEOTA; GENE SEQUENCE; METHANOGENIC ARCHAEON; MICROBIAL DIVERSITY; MICROBIAL MAT; NONHUMAN; NUCLEOTIDE SEQUENCE; PHYLOGENY; POLYMERASE CHAIN REACTION; POND; RNA GENE; UNINDEXED SEQUENCE;

ARCHAEA; BIODIVERSITY; DNA, ARCHAEAL; DNA, RIBOSOMAL; GENES, RRNA; GEOLOGIC SEDIMENTS; MEXICO; MOLECULAR SEQUENCE DATA; PACIFIC OCEAN; PHYLOGENY; RNA, ARCHAEAL; RNA, RIBOSOMAL, 16S; SEQUENCE ANALYSIS, DNA; SEQUENCE HOMOLOGY, NUCLEIC ACID;

BAJA CALIFORNIA SUR; GUERRERO NEGRO; MEXICO [NORTH AMERICA]; NORTH AMERICA;

ARCHAEA; CRENARCHAEOTA; EURYARCHAEOTA;

EID: 63849295689     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.01811-08     Document Type: Article

References (56)

1. Ashelford, K. E., N. A. Chuzhanova, J. C. Fry, A. J. Jones, and A. J. Weightman. 2006. New screening software shows that most recent large 16S rRNA gene clone libraries contain chimeras. Appl. Environ. Microbiol. 72:5734-5741.
2. Baati, H., S. Guermazi, R. Amdouni, N. Gharsallah, A. Sghir, and E. Am-mar. 2008. Prokaryotic diversity of a Tunisian multipond solar saltern. Extremophiles 12:505-518.
3. Bebout, B. M., S. P. Carpenter, D. J. Des Marais, M. Discipulo, T. Embaye, F. Garcia-Pichel, T. M. Hoehler, M. Hogan, L. L. Jahnke, R. M. Keller, S. R. Miller, L. E. Prufert-Bebout, C. Raleigh, M. Rothrock, and K. Turk. 2002. Long-term manipulations of intact microbial mat communities in a greenhouse collaboratory: simulating earth's present and past field environments. Astrobiology 2:383-402.
4. Benson, D. A., I. Karsch-Mizrachi, D. J. Lipman, J. Ostell, and D. L. Wheeler. 2006 GenBank. Nucleic Acids Res. 34:D16-D20.
5. Biddle, J. F., J. S. Lipp, M. A. Lever, K. G. Lloyd, K. B. Sorensen, R. Anderson, H. F. Fredricks, M. Elvert, T. J. Kelly, D. P. Schrag, M. L. Sogin, J. E. Brenchley, A. Teske, C. H. House, and K. U. Hinrichs. 2006. Heterotrophic Archaea dominate sedimentary subsurface ecosystems off Peru. Proc. Natl. Acad. Sci. USA 103:3846-3851.
6. Colwell, R. K., and J. A. Coddington. 1994. Estimating terrestrial biodiversity through extrapolation. Philos. Trans. R. Soc. Lond. B Biol. Sci. 345:101-118.
7. D'Amelio D'Antoni, E., Y. Cohen, and D. J. DesMaris. 1989. Comparative functional ultrastructure of two hypersaline submerged cyanobacterial mats: Guerrero Negro, Baja California Sur, Mexico, and Solar Lake, Sinai. Egypt. In Y. Cohen and E. Rosenberg (ed.), Microbial mats: physiological ecology of benthic microbial communities. American Society for Microbiology, Washington, DC.
8. Decker, K. L, C S. Potter, B. M. Bebout, D. J. Marais, S. Carpenter, M Discipulo, T. M. Hoehler, S. R. Miller, B. Thamdrup, K A. Turk, and P. T. Visseher. 2005. Mathematical simulation of the diel O, S, and C biogeochemistry of a hypersaline microbial mat. FEMS Microbiol. Ecol. 52:377-395.
9. DeSantis, T. Z., P. Hugenholtz, N. Larsen, M. Rojas, E. L. Brodie, K. Keller, T. Huber, D. Dalevi, P, Ha, and G. L. Andersen. 2006. Greengenes, a chimera-checked 16S rRNA gene database and workbench compatible with ARB. Appl. Environ. Microbiol. 72:5069-5072.
10. DeSantis, T. Z., Jr., P. Hugenholtz, K. Keller, E. L. Brodie, N. Larsen, Y. M. Piceno, R. Phan, and G. L. Andersen. 2006. NAST: a multiple sequence alignment server for comparative analysis of 16S rRNA genes. Nucleic Acids Res. 34:W394-W399.
11. Des Marais, D. J. 2003. Biogeochemistry of hypersaline microbial mats illustrates the dynamics of modern microbial ecosystems and the early evolution of the biosphere. Biol. Bull. 204:160-167.
12. Dhillon, A., M. Lever, K. G. Lloyd, D. B. Albert, M. L. Sogin, and A. Teske. 2005. Methanogen diversity evidenced by molecular characterization of methyl coenzyme M reductase A (mcrA) genes in hydrothermal sediments of the Guaymas Basin. Appl. Environ. Microbiol. 71:4592-4601.
13. Dojka, M. A., J. K. Harris, and N. R. Pace. 2000. Expanding the known diversity and environmental distribution of an uncultured phylogenetic division of bacteria. Appl. Environ. Microbiol. 66:1617-1621.
14. Dojka, M. A., P. Hugenholtz, S. K. Haack, and N. R. Pace. 1998. Microbial diversity in a hydrocarbon- and chlorinated-solvent-contaminated aquifer undergoing intrinsic bioremediation. Appl. Environ. Microbiol. 64:3869-3877.
15. Feazel, L. M., J, R. Spear, A. B. Berger, J. K. Harris, D. N. Frank, R. E. Ley, and N. R. Pace. 2008. Eucaryotic diversity in a hypersaline microbial mat. Appl. Environ. Microbiol. 74:329-332.
16. Fike, D. A., C. L. Gammon, W. Ziebis, and V. J. Orphan. 2008. Micron-scale mapping of sulfur cycling across the oxycline of a cyanobacterial mat: a paired nanoSIMS and CARD-EISH approach. ISME J. 2:749-759.
17. Frank, D. N. 2008. XplorSeq: a software environment for integrated management and phylogenetic analysis of metagenomic sequence data. BMC Bioinformatics 9:420.
18. Goebel, B. M., and E. Stackebrandt. 1994. Cultural and phylogenetic analysis of mixed microbial populations found in natural and commercial bioleaching environments. Appl. Environ. Microbiol. 60:1614-1621.
19. Green, S. J., C. Blackford, P. Bucki, L. L. Jahnke, and L. Prufert-Bebout. 2008. A salinity and sulfate manipulation of hypersaline microbial mats reveals stasis in the cyanobacterial community structure. ISME J. 2:457-470.
20. Hoehler, T. M., B. M. Bebout, and D. J. Des Marais. 2001. The role of microbial mats in the production of reduced gases on the early Earth. Nature 412:324-327.
21. Holmer, M., and E. Kirstensen. 1994. Coexistance of sulfate reduction and methane production in an organic-rich sediment. Mar. Ecol. Prog. Ser. 107:117-184.
22. Hong, S. H., J. Bunge, S. O. Jeon, and S. S. Epstein. 2006. Predicting microbial species richness. Proc. Natl. Acad. Sci. USA 103:117-122.
23. Huber, T., G. Faulkner, and P. Hugenholtz. 2004. Bellerophon: a program to detect chimeric sequences in multiple sequence alignments. Bioinformatics 20:2317-2319.
24. Jorgensen, B. B., Y. Cohen, and D. J. Des Marais. 1987. Photosynthetic action spectra and adaptation to spectral light distribution in a benthic cyanobacterial mat. Appl. Environ. Microbiol. 53:879-886.
25. Karner, M. B., E. F. DeLong, and D. M. Karl. 2001. Archaeal dominance in the mesopelagic zone of the Pacific Ocean. Nature 409:507-510.
26. Kendall, M. M., G. D. Wardlaw, C. F. Tang, A. S. Bonin, Y. Liu, and D. L. Valentine. 2007. Diversity of Archaea in marine sediments from Skan Bay. Alaska, including cultivated methanogens, and description of Methanogenium boonei sp. nov. Appl. Environ. Microbiol. 73:407-414.
27. Knittel, K., T. Losekann, A. Boetius, R. Kort, and R. Amann. 2005. Diversity and distribution of methanotrophic archaea at cold seeps. Appl. Environ. Microbiol. 71:467-479.
28. Kunin, V., J. Raes, J. K. Harris, J. R. Spear, J. J. Walker, N. Ivanova, C. von Mering, B. M. Bebout, N. R. Pace, P. Bork, and P. Hugenholtz. 2008. Millimeter-scale genetic gradients and community-level molecular convergence in a hypersaline microbial mat. Mol. Syst. Biol. 4:198.
29. Ley, R. E., J. K. Harris, J. Wilcox, J. R. Spear, S. R. Miller, B. M. Bebout, J. A. Maresca, D. A. Bryant, M. L. Sogin, and N. R. Pace. 2006. Unexpected diversity and complexity of the Guerrero Negro hypersaline microbial mat. Appl. Environ. Microbiol. 72:3685-3695.
30. Liu, Z., C. Lozupone, M. Hamady, F. D. Bushman, and R. Knight. 2007. Short pyrosequencing reads suffice for accurate microbial community analysis. Nucleic Acids Res. 35:e120.
31. Ludwig, W., O. Strunk, R. Westram, L. Richter, H. Meier, Yadhukumar, A. Buchner, T. Lai, S. Steppi, G. Jobb, W. Forster, I Brettske, S. Gerber, A. W. Ginhart, O. Gross, S. Grumann, S. Hermann, R. Jost, A. Konig, T. Liss, R. Lussmann, M. May, B. Nonhoff, B. Reichel, R. Strehlow, A. Stamatakis, N. Stuckmann, A. Vilbig, M. Lenke, T. Ludwig, A. Bode, and K.-H. Schleifer. 2004. ARB: a software environment for sequence data. Nucleic Acids Res. 32:1363-1371.
32. Magurran, A. E. 2004. Measuring biological diversity. Blackwell Publishing Company. Maiden, MA.
33. Minz, D., S. Fishbain, S. J. Green, G. Muyzer, Y. Cohen, B. E. Rittmann, and D. A. Stahl. 1999. Unexpected population distribution in a microbial mat community: sulfate-reducing bacteria localized to the highly oxic chemocline in contrast to a eukaryotic preference for anoxia. Appl. Environ. Microbiol. 65:4659-4665.
34. Minz, D., J. L. Flax, S. J. Green, G. Muyzer, Y. Cohen, M. Wagner, B. E. Rittmann, and D. A. Stahl. 1999. Diversity of sulfate-reducing bacteria in oxic and anoxic regions of a microbial mat characterized by comparative analysis of dissimilatory sulfite reductase genes. Appl. Environ. Microbiol. 65:4666-4671.
35. Mochimaru, H., H. Yoshioka, H. Tamaki, K. Nakamura, N. Kaneko, S. Sakata, H. Imachi, Y. Sekiguchi, H. Uchiyama, and Y. Kamagata. 2007. Microbial diversity and methanogenic potential in a high temperature natural gas field in Japan. Extremophiles 11:453-461.
36. Nubel, U., M. M. Bateson, M. T. Madigan, M. Kuhl, and D. M. Ward. 2001. Diversity and distribution in hypersaline microbial mats of bacteria related to Chloroftexus spp. Appl. Environ. Microbiol. 67:4365-4371.
37. Nubel, U., F. Garcia-Pichel, M. Kuhl, and G. Muyzer. 1999. Quantifying microbial diversity: morphotypes. 16S rRNA genes, and carotenoids of oxygenic phototrophs in microbial mats. Appl. Environ. Microbiol. 65:422-430.
38. Omoregie, E. O., L. L. Crumbliss, B. M. Bebout, and J. P. Zehr. 2004. Determination of nitrogen-fixing phylotypes in Lyngbya sp. and Microcoleus chthonoplastes cyanobacterial mats from Guerrero Negro, Baja California, Mexico. Appl. Environ. Microbiol. 70:2119-2128.
39. Pruesse, E., C. Quast, K. Knittel, B. M. Fuchs, W. Ludwig, J. Peplies, and F. O. Glockner. 2007. SILVA: a comprehensive online resource for quality checked and aligned ribosomal RNA sequence data compatible with ARB. Nucleic Acids Res. 35:7188-7196.
40. Risatti, J. B., W. C. Capman, and D. A. Stahl. 1994. Community structure of a microbial mat: the phylogenetic dimension. Proc. Natl. Acad. Sci. USA 91:10173-10177.
41. ε-acetyl-β-lysine, β-glutamine, and betaine in Methanohalophilus strain FDF1 suggested by nuclear magnetic resonance analyses. J. Bacteriol. 174:6688-6693.
42. Robertson, D. E., M. C. Lai, R. P. Gunsalus, and M. F. Roberts. 1992. Composition, variation, and dynamics of major osmotic solutes in Methanohalophilus strain FDF1. Appl. Environ. Microbiol. 58:2438-2443.
43. Rouviere, P., L. Mandelco, S. Winker, and C. R. Woese. 1992. A detailed phylogeny for the Methanomicrobiales. Syst. Appl. Microbiol. 15:363-371.
44. Sahl, J. W., N. R. Pace, and J. R. Spear. 2008. A comparative molecular analysis of endoevaporatic microbial communities. Appl. Environ. Microbiol. 74:6444-6446.
45. Sakai, S., H. Imachi, Y. Sekiguchi, A. Ohashi, H. Harada, and Y. Kamagata. 2007. Isolation of key methanogens for global methane emission from rice paddy fields: a novel isolate affiliated with the clone cluster rice cluster I. Appl. Environ. Microbiol. 73:4326-4331.
46. Sinninghe Damsté, J. S., W. I. Rijpstra, E. C. Hopmans, F. G. Prahl, S. G. Wakeham, and S. Scheuten. 2002. Distribution of membrane lipids of planktonic Crenarchaeota in the Arabian Sea. Appl. Environ. Microbiol. 68:2997-3002.
47. Smith, J. M., S. J. Green, C. A. Kelley, L. Prufert-Bebout, and B. M. Bebout. 2008. Shifts in methanogen community structure and function associated with long-term manipulation of sulfate and salinity in a hypersaline microbial mat. Environ. Microbiol. 10:386-394.
48. Sorensen, K. B., D. E. Canfield, A. P. Teske, and A. Oren. 2005. Community composition of a hypersaline endoevaporitic microbial mat. Appl. Environ. Microbiol. 71:7352-7365.
49. Spear, J. R., R. E. Ley, A. B. Berger, and N. R. Pace. 2003. Complexity in natural microbial ecosystems: the Guerrero Negro experience. Biol. Bull. 204:168-173.
50. Stamatakis, A. 2006. RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22:2688-2690.
51. Summons, R. E., L. L. Jahnke, J. M. Hope, and G. A. Logan. 1999. 2-Methylhopanoids as biomarkers for cyanobacterial oxygenic photosynthesis. Nature 400:554-557.
52. Takai, K., and K. Horikoshi. 1999. Genetic diversity of archaea in deep-sea hydrothermal vent environments. Genetics 152:1285-1297.
53. Tice, M. M., and D. R. Lowe. 2004. Photosynthetic microbial mats in the 3,416-Myr-old ocean. Nature 431:549-552.
54. Valentine, D. L. 2007. Adaptations to energy stress dictate the ecology and evolution of the Archaea. Nat. Rev. Microbiol. 5:316-323.
55. Vetriani, C, H. W. Jannasch, B. J. MacGregor, D. A. Stahl, and A. L. Reysenbach. 1999. Population structure and phylogenetic characterization of marine benthic Archaea in deep-sea sediments. Appl. Environ. Microbiol. 65:4375-4384.
56. Visscher, P. T., L. K. Baumgartner, D. H. Buckley, D. R. Rogers, M. E. Hogan, C. D. Raleigh, K. A. Turk, and D. J. Des Marais. 2003. Dimethyl sulfide and methanethiol formation in microbial mats: potential pathways for biogenic signatures. Environ. Microbiol. 5:296-308.