Vertical distribution of microbial communities in a perennially stratified Arctic lake with saline, anoxic bottom waters

Scientific Reports

Volumn 2, Issue , 2012, Pages

  Comeau, André M ^a   Harding, Tommy ^b   Galand, Pierre E ^c,d   Vincent, Warwick F ^a,b   Lovejoy, Connie ^a  

^a UNIVERSITÉ LAVAL   (Canada)

^b CENTRE D ÉTUDES NORDIQUES   (Canada)

^c SORBONNE UNIVERSITÉ   (France)

^d Observatoire Océanologique de Banyuls sur Mer   (France)

Author keywords

[No Author keywords available]

Indexed keywords

OXYGEN; RNA 16S;

ARCHAEON; ARCTIC; ARTICLE; BACTERIUM; BIODIVERSITY; CANADA; CHEMISTRY; CLASSIFICATION; ECOSYSTEM; GENETICS; GEOGRAPHY; LAKE; MICROBIOLOGY; PHYLOGENY; SALINITY;

ARCHAEA; ARCTIC REGIONS; BACTERIA; BIODIVERSITY; CANADA; ECOSYSTEM; GEOGRAPHY; LAKES; OXYGEN; PHYLOGENY; RNA, RIBOSOMAL, 16S; SALINITY; WATER MICROBIOLOGY;

EID: 84866134935     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep00604     Document Type: Article

References (72)

1. Coolen, M. J. L. et al. Evolution of the methane cycle in Ace Lake (Antarctica) during the Holocene: Response of methanogens and methanotrophs to environmental change. Org. Geochem. 35, 1151-1167 (2004). (Pubitemid 39204619)
2. Canfield, D. E. & Green, W. J. The cycling of nutrients in a closed-basin Antarctic Lake: Lake Vanda. Biogeochem. 1, 233-256 (1984).
3. Green, W. J., Canfield, D. E., Lee, G. F. & Jones, R. A. Mn, Cu and Cd distributions and residence times in closed basin Lake Vanda (Wright Valley, Antarctica). Hydrobiologia 134, 237-248 (1986).
4. Lee, P. A. et al. Elevated levels of dimethylated-sulfur compounds in Lake Bonney, a poorly ventilated Antarctic lake. Limnol. Oceanogr. 49, 1044-1055 (2004). (Pubitemid 39040341)
5. Priscu, J. C. The biogeochemistry of nitrous oxide in permanently ice-covered lakes of the McMurdo Dry Valleys, Antarctica. Glob. Change Biol. 3, 301-315 (1997).
6. Vincent, W. F., Downes, M. T. & Vincent, C. L. Nitrous oxide cycling in Lake Vanda, Antarctica. Nature 292, 618-620 (1981).
7. Tomkins, J. D., Lamoureux, S. F., Antoniades, D. & Vincent, W. F. Sedimentology of perennial ice-covered, meromictic Lake A, Ellesmere Island, at the northern extreme of Canada. Can. J. Earth Sci. 46, 83-100 (2009).
8. Vincent, A. C., Mueller, D. R. & Vincent, W. F. Simulated heat storage in a perennially ice-covered high Arctic lake: Sensitivity to climate change. J. Geophy. Res. 113, C04036 (2008).
9. Van Hove, P., Vincent, W. F., Galand, P. E. & Wilmotte, A. Abundance and diversity of picocyanobacteria in High Arctic lakes and fjords. Algo. Stud. 126, 209-227 (2008).
10. Pouliot, J., Galand, P. E., Lovejoy, C. & Vincent, W. F. Vertical structure of archaeal communities and the distribution of ammonia monooxygenase A gene variants in two high Arctic lakes. Environ. Microbiol. 11, 687-699 (2009).
11. Antoniades, D. et al. Bacterial dominance of phototrophic communities in a High Arctic lake and its implications for paleoclimate analysis. Polar Sci. 3, 147-161 (2009).
12. Lauro, F. M. et al. An integrative study of a meromictic lake ecosystem in Antarctica. ISME J. 5, 879-895 (2011).
13. Comeau, A. M., Li, W. K. W., Tremblay, J.-E., Carmack, E. C. & Lovejoy, C. Changes in Arctic Ocean microbial community structure following the 2007 record sea ice minimum. PLoS ONE 6, e27492 (2011).
14. Veillette, J., Martineau, M.-J., Antoniades, D., Sarrazin, D.& Vincent, W. F. Effects of loss of perennial lake ice on mixing and phytoplankton dynamics: Insights from High Arctic Canada. Ann. Glaciol. 51, 56-70 (2010).
15. Prowse, T. et al. Past and future changes in lake and river ice. Ambio 40, 53-62 (2011).
16. Galand, P. E., Casamayor, E. O., Kirchman, D. L., Potvin,M. & Lovejoy, C. Unique archaeal assemblages in the Arctic Ocean unveiled by massively parallel tag sequencing. ISME J. 3, 860-869 (2009).
17. DeLong, E. F. & Pace, N. R. Environmental diversity of Bacteria and Archaea. Syst. Biol. 50, 470-478 (2001).
18. Gibson, J. A. E. et al. Geochemistry of ice-covered meromictic Lake A in the Canadian High Arctic. Aquat. Geochem. 8, 1-23 (2002).
19. Yurkov, V. V. in The Prokaryotes: A Handbook on the Biology of Bacteria. Volume 5: Proteobacteria: Alpha and Beta Subclasses (eds M. M. Dworkin, S. Falkow, E. Rosenberg, K.-H. Schleifer & E. Stackebrandt) (Springer, 2006).
20. Martinez-Romero, E. in The Prokaryotes: A Handbook on the Biology of Bacteria. Volume 2: Ecophysiology and Biochemistry (eds M. M. Dworkin, S. Falkow, E. Rosenberg, K.-H. Schleifer & E. Stackebrandt) (Springer, 2006).
21. Overmann, J. in The Prokaryotes: A Handbook on the Biology of Bacteria. Volume 7: Proteobacteria: Delta and Epsilon Subclasses, Deeply Rooting Bacteria (eds M. M. Dworkin, S. Falkow, E. Rosenberg, K.-H. Schleifer & E. Stackebrandt) (Springer, 2006).
22. Lovley, D. in The Prokaryotes: A Handbook on the Biology of Bacteria. Volume 2: Ecophysiology and Biochemistry (eds M. M. Dworkin, S. Falkow, E. Rosenberg, K.-H. Schleifer & E. Stackebrandt) (Springer, 2006).
23. Heising, S., Richter, L., Ludwig,W. & Schink, B. Chlorobium ferrooxidans sp. nov., a phototrophic green sulfur bacterium that oxidizes ferrous iron in coculture with a ''Geospirillum'' sp. strain. Arch. Microbiol. 172, 116-124 (1999). (Pubitemid 29362074)
24. Rankin, L. M., Gibson, J. A. E., Franzmann, P. D. & Burton, H. R. The chemical stratification and microbial communities of Ace Lake, Antarctica: A review of the characteristics of a marine-derived meromictic lake. Polarforschung 66, 33-52 (1999). (Pubitemid 126431288)
25. Lentini, V., Gugliandolo, C. & Maugeri, T. L. Vertical distribution of Archaea and Bacteria in a meromictic lake as determined by fluorescent in situ hybridization. Curr. Microbiol. 64, 66-74 (2012).
26. Mincer, T. J. et al. Quantitative distribution of presumptive archaeal and bacterial nitrifiers in Monterey Bay and the North Pacific Subtropical Gyre. Environ. Microbiol. 9, 1162-1175 (2007). (Pubitemid 46697272)
27. Barberán, A., Fernández-Guerra, A., Auguet, J.-C., Galand, P. E. & Casamayor, E. O. Phylogenetic ecology of widespread uncultured clades of the Kingdom Euryarchaeota. Mol. Ecol. 20, 1988-1996 (2011).
28. Dimitriu, P. A., Pinkart, H. C., Peyton, B. M. & Mormile, M. R. Spatial and temporal patterns in the microbial diversity of a meromictic soda lake in Washington State. Appl. Environ. Microbiol. 74, 4877-4888 (2008).
29. Gibson, J. A. E. The meromictic lakes and stratified marine basins of the Vestfold Hills, East Antarctica. Antarct. Sci. 11, 175-192 (1999). (Pubitemid 29496660)
30. Gregersen, L.H. et al.Dominance of a clonal green sulfur bacterial population in a stratified lake. FEMS Microbiol. Ecol. 70, 30-41 (2009).
31. Koizumi, Y., Kojima, H. & Fukui, M. Dominant microbial composition and its vertical distribution in saline meromictic Lake Kaiike (Japan) as revealed by quantitative oligonucleotide probe membrane hybridization. Appl. Environ. Microbiol. 70, 4930-4940 (2004). (Pubitemid 39095523)
32. Galand, P. E. et al. Phylogenetic and functional diversity of Bacteria and Archaea in a unique stratified lagoon, the Clipperton atoll (N Pacific). FEMS Microbiol. Ecol. 79, 203-217 (2012).
33. Humayoun, S. B., Bano, N. & Hollibaugh, J. T. Depth distribution of microbial diversity in Mono Lake, a meromictic soda lake in California. Appl. Environ. Microbiol. 69, 1030-1042 (2003). (Pubitemid 36204832)
34. Lehours, A.-C., Evans, P., Bardot, C., Joblin, K. & Gérard, F. Phylogenetic diversity of Archaea and Bacteria in the anoxic zone of a meromictic lake (Lake Pavin, France). Appl. Environ. Microbiol. 73, 2016-2019 (2007). (Pubitemid 46449089)
35. Murray, A. E., Peng, V., Tyler, C. & Wagh, P. Marine bacterioplankton biomass, activity and community structure in the vicinity of Antarctic icebergs. Deep Sea Res. II 58, 1407-1421 (2011).
36. Clingenpeel, S. et al. Yellowstone Lake: High-energy geochemistry and rich bacterial diversity. Environ. Microbiol. 13, 2172-2185 (2011).
37. van den Wyngaert, S., Salcher, M. M., Pernthaler, J., Zeder, M. & Posch, T. Quantitative dominance of seasonally persistent filamentous cyanobacteria (Planktothrix rubescens) in the microbial assemblages of a temperate lake. Limnol. Oceanogr. 56, 97-109 (2011).
38. Shaw, A. K. et al. It's all relative: Ranking the diversity of aquatic bacterial communities. Environ. Microbiol. 10, 2200-2210 (2008).
39. Salcher, M. M, Pernthaler, J. & Posch, T. Seasonal bloom dynamics and ecophysiology of the freshwater sister clade of SAR11 bacteria 'that rule the waves' (LD12). ISME J. 5, 1242-1252 (2011).
40. Walsh, D. A. et al. Metagenome of a versatile chemolithoautotroph from expanding oceanic dead zones. Science 326, 578-582 (2009).
41. Schmidtova, J., Hallam, S. J. & Baldwin, S. A. Phylogenetic diversity of transition and anoxic zone bacterial communities within a near-shore anoxic basin: Nitinat Lake. Environ. Microbiol. 11, 3233-3251 (2009).
42. Madrid, V. M., Taylor, G. T., Scranton, M. I. & Chistoserdov, A. Y. Phylogenetic diversity of bacterial and archaeal communities in the anoxic zone of the Cariaco Basin. Appl. Environ. Microbiol. 67, 1663-1674 (2001). (Pubitemid 33644937)
43. Santelli, C. M. et al. Abundance and diversity of microbial life in ocean crust. Nature 453, 653-656 (2008). (Pubitemid 351769297)
44. Bauer, M. et al. Whole genome analysis of the marine Bacteroidetes 'Gramella forsetii' reveals adaptations to degradation of polymeric organic matter. Environ. Microbiol. 8, 2201-2213 (2006). (Pubitemid 44730250)
45. Grossart,H.-P., Levold, F., Allgaier, M., Simon, M. & Brinkhoff, T. Marine diatom species harbour distinct bacterial communities. Environ. Microbiol. 7, 860-873 (2005). (Pubitemid 40697644)
46. Pereira, S. et al. Complexity of cyanobacterial exopolysaccharides: Composition, structures, inducing factors and putative genes involved in their biosynthesis and assembly. FEMS Microbiol. Rev. 33, 917-941 (2009).
47. Borin, S. et al. DNA is preserved and maintains transforming potential after contact with brines of the deep anoxic hypersaline lakes of the Eastern Mediterranean Sea. Saline Systems. 4, 10 (2008).
48. Pei, A. Y. et al. Diversity of 16S rRNA genes within individual prokaryotic genomes. Appl. Environ. Microbiol. 76, 3886-3897 (2010).
49. VanHove, P., Belzile, C.,Gibson, J. A. E.& Vincent, W. F. Coupled landscape-lake evolution in High Arctic Canada. Can. J. Earth Sci. 43, 533-546 (2006). (Pubitemid 44151093)
50. Meyer, K. M. et al. Carotenoid biomarkers as an imperfect reflection of the anoxygenic phototrophic community in meromictic Fayetteville Green Lake. Geobiol. 9, 321-329 (2011).
51. Ng, C. et al. Metaproteogenomic analysis of a dominant green sulfur bacterium from Ace Lake, Antarctica. ISME J. 4, 1002-1019 (2010).
52. Halm, H. et al. Co-occurrence of denitrification and nitrogen fixation in a meromictic lake, Lake Cadagno (Switzerland). Environ. Microbiol. 11, 1945-1958 (2009).
53. Ovreas, L., Forney, L., Daae, F. L.& Torsvik, V. Distribution of bacterioplankton in meromictic Lake Saelenvannet, as determined by denaturing gradient gel electrophoresis of PCR-amplified gene fragments coding for 16S rRNA. Appl. Environ. Microbiol. 63, 3367-3373 (1997). (Pubitemid 27383123)
54. van Gemerden, H. & Mas, J. in Anoxygenic Photosynthetic Bacteria (eds RE Blankenship, MT Madigan & CE Bauer) (Springer, 1995).
55. Hamersley, M. R. et al. Water column anammox and denitrification in a temperate permanently stratified lake (Lake Rassnitzer, Germany). Syst. Appl. Microbiol. 32, 571-582 (2009).
56. Bratina, B., Stevenson, B., Green, W. & Schmidt, T. Manganese reduction by microbes from oxic regions of the Lake Vanda (Antarctica) water column. Appl. Environ. Microbiol. 64, 3791-3797 (1998). (Pubitemid 28462974)
57. Vincent, W. F. et al. Extreme ecosystems and geosystems in the Canadian High Arctic: Ward Hunt Island and vicinity. Ecoscience 18, 236-261 (2011).
58. Harding, T., Jungblut, A., Lovejoy, C. & Vincent, W. F. Microbes in High Arctic snow and implications for the cold biosphere. Appl. Environ. Microbiol. 77, 3234-3243 (2011).
59. Huse, S. M., Huber, J. A.,Morrison, H. G., Sogin, M. L. & Welch, D. M. Accuracy and quality of massively parallel DNA pyrosequencing. Genome Biol. 8, R143 (2007).
60. Quince, C. et al. Accurate determination of microbial diversity from 454 pyrosequencing data. Nature Meth. 6, 639-641 (2009).
61. Behnke, A. et al. Depicting more accurate pictures of protistan community complexity using pyrosequencing of hypervariable SSU rRNA gene regions. Environ. Microbiol. 13, 340-349 (2010).
62. Schloss, P. D. et al. Introducing mothur: Open source, platform-independent, community-supported software for describing and comparing microbial communities. Appl. Environ. Microbiol. 75, 7537-7541 (2009).
63. Schloss, P. D. A high-throughput DNA sequence aligner for microbial ecology studies. PLoS ONE 4, e8230 (2009).
64. Fraser, C., Alm, E. J., Polz, M. F., Spratt, B. G. & Hanage, W. P. The bacterial species challenge: Making sense of genetic and ecological diversity. Science. 323, 741-746 (2009).
65. Werner, J. J. et al. Impact of training sets on classification of high-throughput bacterial 16S rRNA gene surveys. ISME J. 6, 94-103 (2012).
66. Claesson, M. J. et al. Comparative analysis of pyrosequencing and a phylogenetic microarray for exploring microbial community structures in the human distal intestine. PLoS ONE 4, e6669 (2009).
67. Sundquist, A. et al. Bacterial flora-typing with targeted, chip-based Pyrosequencing. BMC Microbiol 7, 108 (2007).
68. Jeraldo, P., Chia, N.& Goldenfeld, N. On the suitability of short reads of 16S rRNA for phylogeny-based analyses in environmental surveys. Environ. Microbiol. 13, 3000-3009 (2011).
69. Liu, Z., Lozupone, C., Hamady, M., Bushman, F. D. & Knight, R. Short pyrosequencing reads suffice for accurate microbial community analysis. Nucl. Acids Res. 35, e120 (2007).
70. Youssef, N., Sheik, C. S., Krumholz, L. R., Najar, F. Z., Roe, B. A. & Elshahed, M. S. Comparison of species richness estimates obtained using nearly complete fragments and simulated pyrosequencing-generated fragments in 16S rRNA gene-based environmental surveys. Appl. Environ. Microbiol. 75, 5227-5236 (2009).
71. Cole, J. R. et al. The Ribosomal Database Project: Improved alignments and new tools for rRNA analysis. Nucl. Acids Res. 37, D141-145 (2009).
72. Brochier-Armanet, C., Boussau, B., Gribaldo, S. & Forterre, P. Mesophilic Crenarchaeota: Proposal for a third archaeal phylum, the Thaumarchaeota. Nat. Rev. Microbiol. 6, 245-252 (2008). (Pubitemid 351256319)