Environmental controls on intragroup diversity of the uncultured benthic archaea of the miscellaneous Crenarchaeotal group lineage naturally enriched in anoxic sediments of the White Oak River estuary (North Carolina, USA)

Environmental Microbiology

Volumn 17, Issue 7, 2015, Pages 2228-2238

  Lazar, Cassandre Sara ^a,b,d   Biddle, Jennifer F ^c   Meador, Travis B ^b   Blair, Nic ^a   Hinrichs, Kai Uwe ^b   Teske, Andreas P ^a  

^a University of North Carolina at Chapel Hill   (United States)

^b UNIVERSITY OF BREMEN   (Germany)

^c UNIVERSITY OF DELAWARE   (United States)

^d FRIEDRICH SCHILLER UNIVERSITY JENA   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ARCHAEA; QUERCUS ALBA;

ARCHAEAL DNA; RNA 16S;

ADAPTATION; BIODIVERSITY; CLASSIFICATION; CRENARCHAEOTA; ESTUARY; GENETICS; MICROBIOLOGY; NORTH CAROLINA; PHYLOGENY; RIVER; SEDIMENT;

ADAPTATION, PHYSIOLOGICAL; BIODIVERSITY; CRENARCHAEOTA; DNA, ARCHAEAL; ESTUARIES; GEOLOGIC SEDIMENTS; NORTH CAROLINA; PHYLOGENY; RIVERS; RNA, RIBOSOMAL, 16S;

EID: 84937042918     PISSN: 14622912     EISSN: 14622920     Source Type: Journal    
DOI: 10.1111/1462-2920.12659     Document Type: Article

References (57)

1. Biddle, J.F., Lipp, J.S., Lever, M.A., Llyod, K.G., Sorensen, K.B., Anderson, R., etal. (2006) Heterotrophic Archaea dominate sedimentary subsurface ecosystems off Peru. PNAS 103: 3846-3851.
2. Clarke, K.R. (1993) Non-parametric multivariate analyses of changes in community structure. Austral Ecol 18: 117-143.
3. Clarke, K.R., and Gorley, R.M. (2001) Changes in Marine Communities: An Approach to Statistical Analysis and Interpretation, 2nd edn. Plymouth, UK: PRIMER-E, p. 172.
4. Clarke, K.R., and Gorley, R.M. (2006) PRIMER v6: User Manual/Tutorial. Plymouth, UK: PRIMER-E.
5. Clarke, K.R., and Green, R.H. (1988) Statistical design and analysis for a 'biological effects' study. Mar Ecol Prog Ser 46: 213-226.
6. Clarke, K.R., Somerfield, P.J., and Gorley, R.N. (2008) Testing of null hypotheses in exploratory community analyses: similarity profiles and biota-environment linkage. J Exp Mar Biol Ecol 366: 56-69.
7. Cline, J.D. (1969) Spectrophotometric determination of hydrogen sulfide in natural waters. Limnol Oceanogr 14: 454-458.
8. Collins, G., O'Connor, L., Mahony, T., Gieseke, A., de Beer, D., and O'Flaherty, V. (2005) Distribution, localization, and phylogeny of abundant populations of crenarchaeota in anaerobic granular sludge. Appl Environ Microbiol 71: 7523-7527.
9. DeSantis, T.Z., Hugenholtz, P., Larsen, N., Rojas, M., Brodie, E.L., Keller, K., etal. (2006) Greengenes, a chimera-checked 16S rRNA gene database and workbench compatible with ARB. Appl Environ Microbiol 72: 5069-5072.
10. Durand, L., Zbinden, M., Cueff-Gauchard, V., Duperron, S., Roussel, E.G., Shillito, B., and Cambon-Bonavita, M.-A. (2010) Microbial diversity associated with the hydrothermal shrimp Rimicaris exoculata gut and occurrence of a resident microbial community. FEMS Microbiol Ecol 71: 291-303.
11. Gagen, E.J., Huber, H., Meador, T., Hinrichs, K.-U., and Thomm, M. (2013) A novel cultivation-based approach for understanding the miscellaneous crenarchaeotic group (MCG) Archaea from sedimentary ecosystems. Appl Environ Microbiol 79: 6400-6406.
12. 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.
13. Hershberger, K.L., Barns, S.M., Reysenbach, A.-L., Dawson, S.C., and Pace, N.R. (1996) Wide diversity of Crenarchaeota. Nature 384: 420.
14. Hinrichs, K.-U., Hayes, J.M., Sylva, S.P., Brewert, P.G., and DeLong, E.F. (1999) Methane-consuming archaebacteria in marine sediments. Nature 398: 802-805.
15. Huang, L.-N., Chen, Y.-Q., Zhou, H., Luo, S., Lan, C.-Y., and Qu, L.-H. (2003) Characterization of methanogenic Archaea in the leachate of a closed municipal solid waste landfall. FEMS Microbiol Ecol 46: 171-177.
16. Inagaki, F., Suzuki, M., Takai, K., Oida, H., Sakamoto, T., Aoki, K., etal. (2003) Microbial communities associated with geological horizons in coastal subseafloor sediments from the Sea of Okhotsk. Appl Environ Microbiol 69: 7224-7235.
17. Inagaki, F., Nunoura, T., Satoshi, N., Teske, A., Lever, M., Lauer, A., etal. (2006) Biogeographical distribution and diversity of microbes in methane hydrate-bearing deep marine sediments on the Pacific Ocean Margin. PNAS 103: 2815-2820.
18. Jiang, L., Zheng, Y., Chen, J., Xiao, X., and Wang, F. (2011) Stratification of Archaeal communities in shallow sediments of the Pearl River Estuary, Southern China. Antonie Van Leeuwenhoek 99: 739-751.
19. Jurgens, G., Glöckner, F.-O., Amann, R., Saano, A., Montonen, L., Likolammi, M., and Münster, U. (2000) Identification of novel Archaea in bacterioplankton of a boreal forest lake by phylogenetic analysis and fluorescent in situ hybridization. FEMS Microbiol Ecol 34: 45-56.
20. Kasai, Y., Takahata, Y., Hoaki, T., and Watanabe, K. (2005) Physiological and molecular characterization of a microbial community established in unsaturated, petroleum-contaminated soil. Environ Microbiol 7: 806-818.
21. Kelley, C.A., Martens, C.S., and Chanton, J.P. (1990) Variations in sedimentary carbon remineralization rates in the White Oak River Estuary, North Carolina. Limnol Oceanogr 35: 372-383.
22. Kelley, C.A., Martens, C.S., and Ussler, W., III (1995) Methane dynamics across a tidally flooded Riverbank Margin. Limnol Oceanogr 40: 1112-1129.
23. Kogan, I., and Paull, C.K. (2005) Coastal seismic wipe-outs: distribution controlled by pore water salinity. Mar Geol 217: 161-175.
24. Kubo, K., Lloyd, K.G., Biddle, J.F., Amann, R., Teske, A., and Knittel, K. (2012) Archaea of the Miscellaneous Crenarchaeotal Group are abundant, diverse and widespread in marine sediments. ISME J 6: 1949-1965.
25. Land, L.A., and Paull, C.K. (2001) Thermal gradients as a tool for estimating groundwater advective rates in a coastal estuary: White Oak River, North Carolina, USA. J Hydrol (Amst) 248: 198-215.
26. Lazar, C.S., Dinasquet, J., Pignet, P., Prieur, D., and Toffin, L. (2010) Active Archaeal communities at cold seep sediments populated by Siboglinidae tubeworms from the Storegga Slide. Microb Ecol 60: 516-527.
27. Letunic, I., and Bork, P. (2011) Interactive Tree of Life v2: online annotation and display of phylogenetic trees made easy. Nucleic Acids Res 39: W475-W478.
28. Li, P.-Y., Xie, B.-B., Zhang, X.-Y., Qin, Q.-L., Dang, H.-Y., Wang, X.-M., etal. (2011) Genetic structure of three fosmid-fragments encoding 16S rRNA genes of the Miscellaneous Crenarchaeotic Group (MCG): implications for physiology and evolution of marine sedimentary archaea. Environ Microbiol 14: 467-479.
29. Lipp, J.S., Morono, Y., Inagaki, F., and Hinrichs, K.-U. (2008) Significant contribution of Archaea to extant biomass in marine subsurface sediments. Nature 454: 991-994.
30. Llobet-Brossa, E., Rossello-Mora, R., and Amann, R. (1998) Microbial community composition of Wadden Sea sediments as revealed by fluorescence in situ hybridization. Appl Environ Microbiol 64: 2691-2696.
31. Lloyd, K.G., Alperin, M.J., and Teske, A. (2011) Environmental evidence for net methane production and oxidation in putative ANaerobic MEthanotrophic (ANME) archaea. Environ Microbiol 13: 2548-2564.
32. Lloyd, K.G., Schreiber, L., Petersen, D.G., Kjeldsen, K.U., Lever, M.A., Steen, A.D., etal. (2013) Predominant archaea in marine sediments degrade detrital proteins. Nature 496: 215-218.
33. Ludwig, W., Strunk, O., Westram, R., Richter, L., Meier, H., Yadhukumar, etal. (2004) ARB: a software environment for sequence data. Nucleic Acids Res 32: 1363-1371.
34. Martens, C.S., and Goldhaber, M.B. (1978) Early diagenesis in transitional sedimentary environments of the White Oak River Estuary, North Carolina. Limnol Oceanogr 23: 428-441.
35. Martens, C.S., Albert, D.B., and Alperin, M.J. (1998) Biogeochemical processes controlling methane in gassy coastal sediments-Part 1. A model coupling organic matter flux to gas production, oxidation and transport. Cont Shelf Res 18: 1741-1770.
36. Meng, J., Wang, F., Wang, F., Zheng, Y., Peng, X., Zhou, H., and Xiao, X. (2009) An uncultivated crenarchaeota contains functional bacteriochlorophyll a synthase. ISME J 3: 106-116.
37. Meng, J., Xu, J., Qin, D., He, Y., Xiao, X., and Wang, F. (2014) Genetic and functional properties of uncultivated MCG archaea assessed by metagenome and gene expression analyses. ISME J 8: 650-659.
38. Morono, Y., Terada, T., Masui, N., and Inagaki, F. (2009) Discriminative detection and enumeration of microbial life in marine subsurface sediments. ISME J 3: 503-511.
39. Ochsenreiter, T., Selezi, D., Quaiser, A., Bonch-Osmolovskaya, L., and Schleper, C. (2003) Diversity and abundance of Crenarchaeota in terrestrial habitats studied by 16S RNA surveys and real time PCR. Environ Microbiol 5: 787-797.
40. Parkes, R.J., Cragg, B.A., and Wellsbury, P. (2000) Recent studies on bacterial populations and processes in subseafloor sediments: a review. Hydrogeol J 8: 11-28.
41. Parkes, R.J., Webster, G., Cragg, B.A., Weightman, A.J., Newberry, C.J., Ferdelman, T.G., etal. (2005) Deep sub-seafloor prokaryotes stimulated at interfaces aver geological times. Nature 436: 390-394.
42. Plasencia, A., Baneras, L., Lliros, M., Casamayor, E.O., and Borrego, C. (2011) Maintenance of previously uncultured freshwater archaea from anoxic waters under laboratory conditions. Antonie Van Leeuwenhoek 99: 403-408.
43. Pruesse, E., Peplies, J., and Glöckner, F.O. (2012) SINA: accurate high-throughput multiple sequence alignment of ribosomal RNA genes. Bioinformatics 28: 1823-1829.
44. Raiswell, R., and Canfield, D.E. (1996) Rates of reaction between silicate iron and dissolved sulfide in Peru Margin sediments. Geochim Cosmochim Acta 60: 2777-2787.
45. Ramette, A. (2007) Multivariate analyses in microbial ecology. FEMS Microbiol Ecol 62: 142-160.
46. Reeburgh, W.S. (2007) Oceanic methane biogeochemistry. Chem Rev 107: 486-513.
47. Reed, D.W., Fujita, Y., Delwiche, M.E., Blackwelder, D.B., Sheridan, P.P., Uchida, T., and Colwell, F.S. (2002) Microbial communities from methane hydrate-bearing deep marine sediments in a forearc basin. Appl Environ Microbiol 68: 3759-3770.
48. Sahm, K., MacGregor, B.J., Jørgensen, B.B., and Stahl, D.A. (1999) Sulphate reduction and vertical distribution of sulphate-reducing bacteria quantified by rRNA slot-blot hybridization in a coastal marine sediment. Environ Microbiol 1: 65-74.
49. Seyler, L.M., McGuinness, L.M., and Kerkhof, L.J. (2014) Crenarchaeal heterotrophy in salt marsh sediments. ISME J 8: 1534-1543.
50. Sorensen, K.B., and Teske, A. (2006) Stratified communities of active Archaea in deep marine subsurface sediments. Appl Environ Microbiol 72: 4596-4603.
51. Stahl, D.A., and Amann, R. (1991) Development and application of nucleic acid probes. In Nucleic Acid Techniques in Bacterial Systematics. Stackebrandt, E., and Goodfellow, M. (eds). Chichester, UK: John Wiley & Sons, pp. 205-248.
52. Stein, L.Y., Jones, G., Alexander, B., Elmund, K., Wright-Jones, C., and Nealson, K.H. (2002) Intriguing microbial diversity associated with metal-rich particles from a freshwater reservoir. FEMS Microbiol Ecol 42: 431-440.
53. Takai, K., Moser, D.P., DeFlaun, M., Onstott, T.C., and Frederickson, J.K. (2001) Archaeal diversity in Waters from Deep South African gold mines. Appl Environ Microbiol 67: 5750-5760.
54. Teske, A., and Sorensen, K.B. (2008) Uncultured archaea in deep marine subsurface sediments: have we caught them all? ISME J 2: 3-18.
55. Teske, A.P. (2006) Microbial communities of deep marine subsurface sediments: molecular and cultivation surveys. Geomicrobiol J 23: 357-368.
56. Vetriani, C., Jannasch, H.W., MacGregor, B.J., Stahl, D.A., and Reysenbach, A.-L. (1999) Population structure and phylogenetic characterization of marine benthic Archaea in deep-sea sediments. Appl Environ Microbiol 65: 4375-4384.
57. Webster, G., Sass, H., Cragg, B.A., Gorra, R., Knab, N.J., Green, C.J., etal. (2011) Enrichment and cultivation of prokaryotes associated with the sulphate-methane transition zone of diffusion-controlled sediments of Aarhus Bay, Denmark, under heterotrophic conditions. FEMS Microbiol Ecol 77: 248-263.