Diversity of active aerobic methanotrophs along depth profiles of arctic and subarctic lake water column and sediments

ISME Journal

Volumn 6, Issue 10, 2012, Pages 1937-1948

  He, Ruo ^a,b   Wooller, Matthew J ^b,c   Pohlman, John W ^d   Quensen, John ^e   Tiedje, James M ^e   Leigh, Mary Beth ^b  

^a ZHEJIANG UNIVERSITY   (China)

^b UNIVERSITY OF ALASKA FAIRBANKS   (United States)

^c University of Alaska Fairbanks   (United States)

^d U S GEOLOGICAL SURVEY   (United States)

^e MICHIGAN STATE UNIVERSITY   (United States)

Author keywords

Arctic lakes; CH4 oxidation potential; Methanotrophs; Stable isotope probing

Indexed keywords

BACTERIAL DNA; CARBON; METHANE;

ARCTIC ENVIRONMENT; GLACIAL LAKE; LACUSTRINE DEPOSIT; LAKE WATER; LATITUDE; METHANE; METHANOTROPHY; POLYMERASE CHAIN REACTION; SEDIMENT-WATER INTERFACE; SPECIES DIVERSITY; STABLE ISOTOPE; TUNDRA; WATER COLUMN;

ARCTIC; ARTICLE; BIODIVERSITY; CHEMISTRY; CLASSIFICATION; DNA SEQUENCE; GENETICS; LAKE; METABOLISM; METHYLOCOCCACEAE; METHYLOCYSTACEAE; MICROBIOLOGY; OXIDATION REDUCTION REACTION; PHYLOGENY; PLANKTON; RESTRICTION FRAGMENT LENGTH POLYMORPHISM; SEDIMENT; UNITED STATES;

ALASKA; ARCTIC REGIONS; BIODIVERSITY; CARBON; DNA, BACTERIAL; GEOLOGIC SEDIMENTS; LAKES; METHANE; METHYLOCOCCACEAE; METHYLOCYSTACEAE; OXIDATION-REDUCTION; PHYLOGENY; PLANKTON; POLYMORPHISM, RESTRICTION FRAGMENT LENGTH; SEQUENCE ANALYSIS, DNA;

ALASKA; UNITED STATES;

METHYLOBACTER; METHYLOCOCCACEAE; METHYLOCYSTIS; METHYLOMONAS;

EID: 84867743452     PISSN: 17517362     EISSN: 17517370     Source Type: Journal    
DOI: 10.1038/ismej.2012.34     Document Type: Article

References (57)

1. Amaral JA, Knowles R. (1995). Growth of methanotrophs in methane and oxygen counter gradients. FEMS Microbiol Lett 126: 215-220.
2. Auman AJ. (2001). Molecular analysis of methanotroph ecology in lake Washington sediment, Ph D Thesis. University of Washington: Washington.
3. 4 emissions. J Geophys Res 113: G02024.
4. Bastviken D, Tranvik LJ, Downing JA, Crill PM, Enrich-Prast A. (2011). Freshwater methane emissions offset the continental carbon sink. Science 331: 50.
5. Bender M, Conrad R. (1994). Methane oxidation activity in various soils and freshwater sediments: occurence, charateristics, vertical profiles and distribution on grain size fractions. J Geophys Res 99: 16531-16540.
6. Bowman JP, Sly LI, Nichols PD, Hayward AC (1993). Revised taxonomy of the methanotrophs: description of Methylobacter gen. nov., validation of Methylo-sinus and Methylocystis species, and a proposal that the family Methylococcaceae includes only the group I methanotrophs. Int J Syst Bacteriol 43: 735-753.
7. Bratina BJ, Brusseau GA, Hanson RS. (1992). Use of 16S r RNA analysis to investigate phylogeny of methylotrophic bacteria. Int J Syst Evol Microbiol 42: 645-648.
8. Brosius LS. (2010). Investigation controls over methane production and bubbling from interior Alaskan lakes using stable isotopes and radiocarbon ages, MS Thesis. University of Alaska Fairbanks: Fairbanks.
9. Brune A, Frenzel P, Cypionka H. (2000). Life at the oxic-anoxic interface: microbial activities and adaptations. FEMS Microbiol Rev 24: 691-710.
10. Burn CR. (2002). Tundra lakes and permafrost, Richards Island, western Arctic coast, Canada. Can J Earth Sci 39: 1281-1298.
11. Bussmann I, Pester M, Brune A, Schink B. (2004). Preferential cultivation of Type II methanotrophic bacteria from littoral sediments (Lake Constance). FEMS Microbiol Eco 47: 179-189.
12. Carini S, Bano N, Le Cleir G, Joye SB. (2005). Aerobic methane oxidation and methanotroph community composition during seasonal stratification in Mono Lake, California (USA). Environ Microbiol 7: 1127-1138.
13. Chanton JP, Powelson DK, Abichou T, Fields D, Green R. (2008). Effect of temperature and oxidation rate on carbon-isotope fractionation during methane oxida-tion by landfill cover materials. Environ Sci Technol 42: 7818-7823.
14. Clilverd H, White D, Lilly M. (2009). Chemical and physical controls on the oxygen regime of ice-covered arctic lakes and reservoirs. J Am Water Resources Ass 45: 500-511.
15. Corder RE, Johnson ER, Vega JL, Clausen EC, Gaddy JL. (1986). Biological production ofmethanol from methane. URL http://www.anl.gov/PCS/acsfuel/ preprint%20 archive/Files/33 3 LOS%20ANGELES 09-88 0469.pdf.
16. Costello AM, Lidstrom ME. (1999). Molecular character-ization of functional and phylogenetic genes from natural populations of methanotrophs in lake sedi-ments. Appl Environ Microbiol 65: 506-5074.
17. Crump BC, Kling GW, Bahr M, Hobbie JE. (2003). Bacterioplankton community shifts in an arctic lake correlate with seasonal changes in organic matter source. Appl Environ Microbiol 69: 2253-2268.
18. Duc NT, Crill P, Bastviken D. (2010). Implications of temperature and sediment characteristics on methane formation and oxidation in lake sediments. Biogeo-chemistry 100: 185-196.
19. Dumont MG, Murrell JC. (2005). Stable isotope probing-linking microbial identity to function. Nat Rev Micro-biol 3: 499-504.
20. Dunfield PF, Yuryev A, Senin P, Smirnova AV, Stott MB, Hou SB et al. (2007). Methane oxidation by an extremely acidophilic bacterium of the phylum Verru-comicrobia. Nature 450: 879-882.
21. Etheridge DM, Steele LP, Francey RJ, Langenfields RL. (1998). Atmospheric methane between 1000 A.D. and present: Evidence of anthropogenic emissions and climatic variability. J Geophys Res 103: 15979-15993.
22. Frenzel P, Thebrath B, Conrad R. (1990). Oxidation of methane in the oxic surface layer of a deep lake sediment (Lake Constance). FEMS Microbiol Lett 73: 149-158.
23. Gee GW, Bauder JW. (1986). Particle-size analysis. In: Klute A (ed) Methods of Soil Analysis, Part 1. Physical and Mineralogical Methods. American Society of Agronomy/Soil Science Society of America: Madison, pp 383-411.
24. Graham DW, Korich DG, Leblanc RP, Sinclair NA, Arnold RG. (1992). Applications of a colorimetric plate assay for soluble methane monooxygenase activity. Appl Environ Microbiol 58: 2231-2236.
25. Hammer Ø, Harper DAT, Ryan PD. (2001). PAST: Paleon-tological statistics software package for education and data analysis. Palaeontol Electron 4: 9 pp. http:// palaeo-electronica.org/2001-1/past/issue1-01.htm.
26. Hanson RS, Hanson TE. (1996). Methanotrophic bacteria. Microbiol Rev 60: 439-471.
27. He R, Wooller MJ, Pohlman JW, Catranis C, Quensen J, Tiedje JM, Leigh MB. (2012). Identification of func-tionally active aerobic methanotrophs in sediments from an arctic lake using stable isotope probing. Environ Microbiol; e-pub ahead of print 20 March 2012; doi:10.1111/j.1462-2920.2012.02725.x.
28. Henckel T, Jäckel U, Conrad R. (2001). Vertical distribu-tion of the methanotrophic community after drainage of rice field soil. FEMS Microbiol Ecol 34: 279-291.
29. 4 on presence and activity of the indigenous methanotrophic community in rice field soil. Environ Microbiol 2: 666-679.
30. Hoehler TM, Borowski WS, Alperin MJ, Rodriguez NM, Paull CK. (2000). Model, stable isotope, and radio-tracer characterization of anaerobic methane oxidation in gas hydrate-bearing sediments of the Blake Ridge. Proc ODP Sci Res 164: 79-85.
31. Intergovernmental Panel on Climate Change (IPCC) (2001). Climate change 2001: the Scientific Basis. In: Houghton JT, Ding Y, Griggs DJ, Noguer M, van der Linden PJ, Xiaos D (eds). Contribution of Working Group I to the Third Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge University Press: Cambridge.
32. Intergovernmental Panel on Climate Change (IPCC) (2007). Climate Change 2007\-The Physical Science Basis. In: Solomon S, Qin D, Manning M, Marquis M, Averyt K, Tignor MMB, Miller HL, Chen Z (eds). Contribution of Working Group I to the Fourth Assessment Report of the Intergovernmental Panel on Climate Chang. Cambridge University Press: Cambridge.
33. Islam T, Jensen S, Reigstad LJ, Larsen O, Birkeland NK. (2008). Methane oxidation at 55 °C and p H 2 by a thermoacidophilic bacterium belonging to the Verru-comicrobia phylum. Proc Natl Acad Sci USA 105: 300-304.
34. Jugnia LB, Roy R, Pacheco-Oliver M, Planas D, Miguez CB, Greer CW. (2006). Potential activity and diversity of methanotrophic bacteria in forest soil, peat, and sediments from a hydroelectric reservoir (robert-bourassa) and lakes in the Canadian Taiga. Soil Sci 171: 127-137.
35. Kightley D, Nedwell DB, Cooper M. (1995). Capacity for methane oxidation in landfill cover soils measured in laboratory scale soil microcosms. Appl Environ Micro-biol 61: 592-601.
36. Kuivila KM, Murray JW, Devol AH, Lidstrom ME, Reimers CE. (1988). Methane cycling in the sediments of Lake Washington. Limn Oceanogr 33: 571-581.
37. Lee SG, Goo JH, Kim HG, Oh JI, Kim YM, Kim SW. (2004). Optimization of methanol biosynthesis from methane using Methylosinus trichosporium OB3b. Biotechnol Lett 26: 947-950.
38. Leigh MB, Pellizari VH, Uhl?́k O, Sutka R, Rodrigues J, Ostrom NE et al. (2007). Biphenyl-utilizing bacteria and their functional genes in a pine root zone contaminated with polychlorinated biphenyls (PCBs). The ISMEJ1: 134-148.
39. Lide DR, Frederikse HPR. (1995). CRC Handbook of Chemistry and Physics, 76th edn. CRC Press, Inc: Boca Raton, FL.
40. Liebner S, Wagner D. (2007). Abundance, distribution and potential activity of methane oxidizing bacteria in permafrost soils from the Lena Delta, Siberia. Environ Microbiol 9: 107-117.
41. Martineau C, Whyte LG, Greer CW. (2010). Stable isotope probing analysis of the diversity and activity of methanotrophic bacteria in soils from the Canadian High Arctic. Appl Environ Microbiol 76: 5773-5784.
42. Mc Donald IR, Radajewski S, Murrell JC. (2005). Stable isotope probing of nucleic acids in methanotrophs and methylotrophs: a review. Org Geochem 36: 779-787.
43. Miller MC, Prentki RT, Barsdate RJ. (1980). Physics. In: Hobbie JE (ed) Limnology of Tundra Ponds: Barrow, Alaska Hutchinson and Ross Dowden, pp 76-178.
44. Mor S, Visscher AD, Ravindra K, Dahiya RP, Chandra A, Cleemput OV. (2006). Induction of enhanced methane oxidation in compost: Temperature and moisture response. Waste Manage 2006: 381-388.
45. Phelps AR, Peterson KM, Jeffries MO. (1998). Methane efflux from high-latitude lakes during spring ice melt. J Geophys Res 103: 29029-29036.
46. Pol A, Heijmans K, Harhangi HR, Tedesco D, Jetten MSM, Op den Camp HJM. (2007). Methanotrophy below p H1 by a new Verrucomicrobia species. Nature 450: 874-878.
47. Radajewski S, Mc Donald IR, Murrell JC. (2003). Stable-isotope probing of nucleic acids: a window to the function of uncultured microorganisms. Curr Opin Biotechnol 14: 296-302.
48. Radajewski S, Webster G, Reay DS, Morris SA, Ineson P, Nedwell DB et al. (2002). Identification of active methylotroph populations in an acidic forest soil by stable-isotope probing. Microbiology 148: 2331-2342.
49. Rahalkar M, Schink B. (2007). Comparison of aerobic methanotrophic communities in littoral and profundal sediments of Lake Constance by a molecular approach. Appl Environ Microbiol 73: 4389-4394.
50. Reay WG, Gallagher D, Simmons GM. (1993). Sediment-water column nutrient exchanges in Southern Chesa-peake Bay nearshore environments. Virginia Polytech-nic Institute and State University: Virginia.
51. Reeburgh WS. (2007). Oceanic methane biogeochemistry. Chem Rev 107: 486-513.
52. Treude T, Ziebis W. (2010). Methane oxidation in permeable sediments at hydrocarbon seeps in the Santa Barbara Channel, California. Biogeosciences 7: 3095-3108.
53. Vries GE, Kües U, Stahl U. (1990). Physiology and genetics of methylotrophic bacteria. FEMS Microbiol Lett 75: 57-101.
54. Walter KM, Smith LC, Chapin FS III. (2007). Methane bubbling from northern lakes: present and future contributions to the global methane budget. Phil Trans R Soc A 365: 1657-1676.
55. Wang Y, Wooller MJ. (2006). The stable isotopic (C and N) composition of modern plants and lichens from northern Iceland: with ecological and paleoenviron-mental implications. Jökull 56: 27-37.
56. Wooller MJ, Ruppel C, Pohlman JW, Leigh MB, Heintz M. (2009). Permafrost gas hydrates and climate change: Lake-based seep studies on the Alaskan north slope. Fire in the Ice 4: 6-9.
57. Zimov SA, Schuur EAG, Chapin FS III. (2006). Permafrost global carbon budget. Science 312: 1612-1613.