Oxic water column methanogenesis as a major component of aquatic CH4 fluxes

Nature Communications

Volumn 5, Issue , 2014, Pages

  Bogard, Matthew J ^a   Del Giorgio, Paul A ^a   Boutet, Lennie ^a   Chaves, Maria Carolina Garcia ^a   Prairie, Yves T ^a   Merante, Anthony ^a   Derry, Alison M ^a  

^a UNIVERSITÉ DU QUÉBEC À MONTRÉAL   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

LAKE WATER; METHANE; SURFACE WATER;

ALGAL COMMUNITY; AQUATIC ECOSYSTEM; FRESHWATER; GAS EXCHANGE; LAKE DYNAMICS; METHANE; METHANOGENESIS; OXIC CONDITIONS; PRIMARY PRODUCTION; WATER COLUMN;

ALGA; ARTICLE; ECOSYSTEM; METHANOGENESIS; MOLECULAR DYNAMICS; AEROBIC METABOLISM; CHEMISTRY; GREEN ALGA; GROWTH, DEVELOPMENT AND AGING; LAKE; METABOLISM; PLANKTON;

ALGAE;

AEROBIOSIS; CHLOROPHYTA; ECOSYSTEM; LAKES; METHANE; PLANKTON;

EID: 84923015306     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms6350     Document Type: Article

References (68)

1. Solomon, S. et al. in Climate Change 2007: The Physical Science Basis. Contribution of Working Group I to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change. (eds Solomon, S. et al.) (Cambridge Univ., 2007).
2. Bastviken, D., Tranvik, L. J., Downing, J. A., Crill, P. M. & Enrich-Prast, A. Freshwater methane emissions offset the continental carbon sink. Science 331, 50 (2011).
3. Michmerhuizen, C. M., Striegl, R. G. & Mcdonald, M. E. Potential methane emission from north-temperate lakes following ice melt. Limnol. Oceanogr. 41, 985-991 (1996).
4. Kirschke, S. et al. Three decades of global methane sources and sinks. Nat. Geosci. 6, 813-823 (2013).
5. Prairie, Y. T. & del Giorgio, P. A. A new pathway of freshwater methane emissions and the putative importance of microbubbles. Inl. Waters 3, 311-320 (2013).
6. Rudd, J.W. M. & Hamilton, R. D. Methane cycling in a eutrophic shield lake and its effects on whole lake metabolism. Limnol. Oceanogr. 23, 337-348 (1978).
7. Bastviken, D., Cole, J., Pace, M. & Tranvik, L. Methane emissions from lakes: dependence of lake characteristics, two regional assessments, and a global estimate. Global Biogeochem. Cycles 18, GB4009 (2004).
8. Murase, J., Sakai, Y., Sugimoto, A., Okubo, K. & Sakamoto, M. Sources of dissolved methane in Lake Biwa. Limnology 4, 91-99 (2003).
9. Schmidt, U. & Conrad, R. Hydrogen, carbon monoxide, and methane dynamics in Lake Constance. Limnol. Oceanogr. 38, 1214-1226 (1993).
10. Schulz, M., Faber, E., Hollerbach, A., Schroder, H. G. & Gude, H. The methane cycle in the epilimnion of Lake Constance. Arch. Hydrobiol. 151, 157-176 (2001).
11. Hofmann, H. Spatiotemporal distribution patterns of dissolved methane in lakes: How accurate are the current estimations of the diffusive flux path? Geophys. Res. Lett. 40, 2779-2784 (2013).
12. Schmid, M. et al. Sources and sinks of methane in Lake Baikal: A synthesis of measurements and modeling. Limnol. Oceanogr. 52, 1824-1837 (2007).
13. Scranton, M. I. & Brewer, P. G. Occurrence of methane in the near-surface waters of the western subtropical North-Atlantic. Deep. Sea Res. 24, 127-138 (1977).
14. Owens, N. J. P., Law, C. S., Mantoura, R. F. C., Burkill, P. H. & Llewellyn, C. A. Methane flux to the atmosphere from the Arabian Sea. Nature 354, 293-296 (1991).
15. Damm, E. et al. Methane production in aerobic oligotrophic surface water in the central Arctic Ocean. Biogeosciences 7, 1099-1108 (2010).
16. Karl, D. M. et al. Aerobic production of methane in the sea. Nat. Geosci. 1, 473-478 (2008).
17. Tilbrook, B. D. & Karl, D. M. Methane sources, distributions and sinks from California coastal waters to the oligotrophic North Pacific gyre. Mar. Chem. 49, 51-64 (1995).
18. Tang, K. W., McGinnis, D. G., Frindte, K., Brüchert, V. & Grossart, H.-P. Paradox reconsidered: Methane oversaturation in well-oxygenated lake waters. Limnol. Oceanogr. 59, 275-284 (2014).
19. Grossart, H.-P., Frindte, K., Dziallas, C., Eckert, W. & Tang, K. W. Microbial methane production in oxygenated water column of an oligotrophic lake. Proc. Natl Acad. Sci. USA 108, 19657-19661 (2011).
20. De Angelis, M. A. & Lee, C. Methane production during zooplankton grazing on marine phytoplankton. Limnol. Oceanogr. 39, 1298-1308 (1994).
21. Oremland, R. S. Methanogenic activity in plankton samples and fish intestines: A mechanism for in situ methanogenesis in oceanic surface waters. Limnol. Oceanogr. 24, 1136-1141 (1979).
22. Ditchfield, A. et al. Identification of putative methylotrophic and hydrogenotrophic methanogens within sedimenting material and copepod faecal pellets. Aquat. Microb. Ecol. 67, 151-160 (2012).
23. Beversdorf, L. J., White, A. E., Björkman, K. M., Letelier, L. M. & Karl, D. M. Phosphonate metabolism by Trichodesmium IMS101 and the production of greenhouse gases. Limnol. Oceanogr. 55, 1768-1778 (2010).
24. Carini, P., White, A. E., Campbell, E. O. & Giovannoni, S. J. Methane production by phosphate-starved SAR11 chemoheterotrophic marine bacteria. Nat. Commun. 5, 4346 (2014).
25. del Valle, D. A. & Karl, D. M. Aerobic production of methane from dissolved methylphosphonate in the water column and sinking particles collected in the North Pacific Subtropical Gyre. Aquat. Microb. Ecol 73, 93-105 (2014).
26. Paganin, P. et al. Vertical distribution of bacterioplankton in Lake Averno in relation to water chemistry. FEMS Microbiol. Ecol. 84, 176-188 (2013).
27. Angel, R., Matthies, D. & Conrad, R. Activation of methanogenesis in arid biological soil crusts despite the presence of oxygen. PLoS One 6, e20453 (2011).
28. Angel, R., Claus, P. & Conrad, R. Methanogenic archaea are globally ubiquitous in aerated soils and become active under wet anoxic conditions. ISME J. 6, 847-862 (2012).
29. 13C of dissolved inorganic carbon in Lake Biwa: Implications for hypolimnetic metabolism. Biogeochemistry 36, 205-221 (1997).
30. Conrad, R. Quantification of methanogenic pathways using stable carbon isotopic signatures: A review and a proposal. Org. Geochem. 36, 739-752 (2005).
31. Utsumi, M. et al. Oxidation of dissolved methane in a eutrophic, shallow lake: Lake Kasumigaura, Japan. Limnol. Oceanogr. 43, 471-480 (1998).
32. 4emissions. J. Geophys. Res. 113, G02024 (2008).
33. Wright, R. R. & Hobbie, J. E. Use of glucose and acetate by bacteria and algae in aquatic ecosystems. Ecology 47, 447-464 (1966).
34. Allen, H. L. Acetate in fresh water: Natural substrate concentrations determined by dilution bioassay. Ecology 49, 346-349 (1968).
35. Ho, T.-Y. et al. Acetate cycling in the water column of the Cariaco Basin: Seasonal and vertical variability and implication for carbon cycling. Limnol. Oceanogr. 47, 1119-1128 (2002).
36. Sepers, A. The utilization of dissolved organic compounds in aquatic environments. Hydrobiologia 52, 39-54 (1977).
37. Thauer, R. K., Möller-Zinkhan, D. & Spormann, A. M. Biochemistry of acetate catabolism in anaerobic chemotrophic bacteria. Annu. Rev. Microbiol. 43, 43-67 (1989).
38. Riemann, L. & Azam, F. Widespread N-acetyl-d-glucosamine uptake among pelagic marine bacteria and its ecological implications. Appl. Environ. Microbiol. 68, 5554-5562 (2002).
39. Alonso, C. & Pernthaler, J. Incorporation of glucose under anoxic conditions by bacterioplankton from coastal North Sea surface waters. Appl. Environ. Microbiol. 71, 1709-1716 (2005).
40. Tada, Y. & Grossart, H.-P. Community shifts of actively growing lake bacteria after N-acetyl-glucosamine addition: Improving the BrdU-FACS method. ISME J. 8, 1-14 (2013).
41. Stams, A. J. M. & Plugge, C. M. Electron transfer in syntrophic communities of anaerobic bacteria and archaea. Nat. Rev. Microbiol. 7, 568-577 (2009).
42. Finlay, K., Leavitt, P. R., Wissel, B. & Prairie, Y. T. Regulation of spatial and temporal variability of carbon flux in six hard-water lakes of the northern Great Plains. Limnol. Oceanogr. 54, 2553-2564 (2009).
43. Raymond, P. A. et al. Global carbon dioxide emissions from inland waters. Nature 503, 355-359 (2013).
44. McDonald, C. P., Stets, E. G., Striegl, R. G. & Butman, D. Inorganic carbon loading as a primary driver of dissolved carbon dioxide concentrations in the lakes and reservoirs of the contiguous United States. Global Biogeochem. Cycles 27, 285-295 (2013).
45. 4 fluxes across boreal lakes, and contribution to diffusive C emissions. Glob. Chang. Biol. (In the press).
46. Ortiz-Llorente, M. J. & Alvarez-Cobelas, M. Comparison of biogenic methane emissions from unmanaged estuaries, lakes, oceans, rivers and wetlands. Atmos. Environ. 59, 328-337 (2012).
47. Schindler, D. W. Recent advances in the understanding and management of eutrophication. Limnol. Oceanogr. 51, 356-363 (2006).
48. Moss, B. Cogs in the endless machine: Lakes, climate change and nutrient cycles: a review. Sci. Total Environ. 434, 130-142 (2012).
49. Carpenter, S. R. et al. Nonpoint pollution of surface waters with phosphorus and nitrogen. Ecol. Appl. 8, 559-568 (1998).
50. Monteith, D. T. et al. Dissolved organic carbon trends resulting from changes in atmospheric deposition chemistry. Nature 450, 537-540 (2007).
51. Schindler, D. W. et al. Climate-induced changes in the dissolved organic carbon budgets of boreal lakes. Biogeochemistry 36, 9-28 (1997).
52. Taranu, Z. E., Zurawell, R. W., Pick, F. & Gregory-Eaves, I. Predicting cyanobacterial dynamics in the face of global change: The importance of scale and environmental context. Glob. Chang. Biol. 18, 3477-3490 (2012).
53. Carpenter, S. R., Cole, J. J., Kitchel, J. F. & Pace, M. L. Impact of dissolved organic carbon, phosphorus, and grazing on phytoplankton biomass and production in experimental lakes. Limnol. Oceanogr. 43, 73-80 (1998).
54. Jones, R. I. The influence of humic substances on lacustrine planktonic food chains. Hydrobiologia 229, 73-91 (1992).
55. Den Heyer, C. & Kalff, J. Organic matter mineralization rates in sediments: A within- and among-lake study. Limnol. Oceanogr. 43, 695-705 (1998).
56. Lennon, J. T. et al. A source of terrestrial organic carbon to investigate the browning of aquatic ecosystems. PLoS One 8, e75771 (2013).
57. Bouvier, T. C. & del Giorgio, P. A. Compositional changes in free-living bacterial communities along a salinity gradient in two temperate estuaries. Limnol. Oceanogr. 47, 453-470 (2002).
58. Vachon, D., Prairie, Y. T. & Cole, J. J. The relationship between near-surface turbulence and gas transfer velocity in freshwater systems and its implications for floating chamber measurements of gas exchange. Limnol. Oceanogr. 55, 1723-1732 (2010).
59. Jahne, B. et al. On the parameters influencing air-water gas exchange. J. Geophys. Res. 92, 1937-1949 (1987).
60. Wanninkhof, R. Relationship between wind speed and gas exchange over the ocean. J. Geophys. Res. 97, 7373-7382 (1992).
61. Quiñones-Rivera, Z. J., Wissel, B. & Justić, D. Development of productivity models for the northern Gulf of Mexico based on oxygen concentrations and stable isotopes. Estuaries Coasts 32, 436-446 (2009).
62. Bastviken, D., Ejlertsson, J. & Tranvik, L. Measurement of methane oxidation in lakes: A comparison of methods. Environ. Sci. Technol. 36, 3354-3361 (2002).
63. Stumm, W. & Morgan, J. J. Aquatic Chemistry: Chemical Equilibria and Rates in Natural Waters (Wiley, 1996).
64. Mook, K. A., Bommerson, J. C. & Staverman, W. H. Carbon isotope fractionation between dissolved bicarbonate and gaseous carbon dioxide. Earth Planet. Sci. Lett. 22, 169-176 (1974).
65. Fry, B. Stable Isotope Ecology (Springer, 2006).
66. 2. J. Geophys. Res. 97, 335-343 (1992).
67. Livingstone, D. M. & Imboden, D. M. The prediction of hypolimnetic oxygen profiles: a plea for a deductive approach. Can. J. Fish. Aquat. Sci. 53, 924-932 (1996).
68. Carignan, R Station de biologie des Laurentides-Université de Montreál http://www.sbl.umontreal.ca/territoire-cartes/cartes/index.html (2010).