Methane oxidation coupled to oxygenic photosynthesis in anoxic waters

ISME Journal

Volumn 9, Issue 9, 2015, Pages 1991-2002

  Milucka, Jana ^a   Kirf, Mathias ^b   Lu, Lu ^a,c,d   Krupke, Andreas ^a   Lam, Phyllis ^a,e   Littmann, Sten ^a   Kuypers, Marcel M M ^a   Schubert, Carsten J ^b  

^a MAX PLANCK INSTITUTE FOR MARINE MICROBIOLOGY   (Germany)

^b SWISS FEDERAL INSTITUTE OF AQUATIC SCIENCE AND TECHNOLOGY   (Switzerland)

^c INSTITUTE OF SOIL SCIENCE   (China)

^d UNIVERSITY OF CHINESE ACADEMY OF SCIENCES   (China)

^e UNIVERSITY OF SOUTHAMPTON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ABUNDANCE; ALGA; ANOXIC CONDITIONS; CARBON EMISSION; LAKE ECOSYSTEM; LIGHT EFFECT; METHANE; METHANOTROPHY; MICROBIAL COMMUNITY; PHOTOSYNTHESIS;

LAKE CADAGNO; SWITZERLAND; TICINO;

ALGAE; BACTERIA (MICROORGANISMS); PROTEOBACTERIA;

CARBON; METHANE; NITRITE; OXYGEN; SULFATE;

ATMOSPHERE; CHEMISTRY; GAMMAPROTEOBACTERIA; LAKE; METABOLISM; MICROBIOLOGY; OXIDATION REDUCTION REACTION; PHOTOSYNTHESIS;

ATMOSPHERE; CARBON ISOTOPES; GAMMAPROTEOBACTERIA; LAKES; METHANE; NITRITES; OXIDATION-REDUCTION; OXYGEN; PHOTOSYNTHESIS; SULFATES; WATER MICROBIOLOGY;

EID: 84939564088     PISSN: 17517362     EISSN: 17517370     Source Type: Journal    
DOI: 10.1038/ismej.2015.12     Document Type: Article

References (68)

1. Auman AJ, Lidstrom ME. (2002). Analysis of sMMOcontaining Type I methanotrophs in Lake Washington sediment. Environ Microbiol 4: 517-524.
2. Bahr M, Stams AJM, De la Rosa F, Garcia-Encina PA, Munoz R. (2011). Assessing the influence of carbon oxidation-reduction in algal-bacterial photobioreactos. Appl Microbiol Biotechnol 90: 1527-1536.
3. Bastviken D, Cole J, Pace M, Tranvik L. (2004). Methane emissions from lakes: dependence of lake characteristics, two regional assessments, and a global estimate. Global Biogeochem Cyc 18: 1-12.
4. Beal EJ, House CH, Orphan VJ. (2009). Manganese-and iron-dependent marine methane oxidation. Science 325: 184-187.
5. Biderre-Petit C, Jezequel D, Dugat-Bony E, Lopes F, Kuever J, Borrel G et al. (2011). Identification of microbial communities involved in the methane cycle of a freshwater meromictic lake. FEMS Microbiol Ecol 77: 533-545.
6. Blees J, Niemann H, Wenk CB, Zopfi J, Schubert CJ, Kirf MK et al. (2014). Micro-aerobic bacterial methane oxidation in the chemocline and anoxic water column of deep south-Alpine Lake Lugano (Switzerland). Limnol Oceanogr 59: 311-324.
7. Bodelier PLE, Meima-Franke M, Hordijk CA, Steenbergh AK, Hefting MM, Bodrossy L et al. (2013). Microbial minorities modulate methane consumption through niche partitioning. ISME J 7: 2214-2228.
8. Bossard P, Gammeter S, Lehmann C, Schanz F, Bachofen R, Burgi HR et al. (2001). Limnological description of the Lakes Zurich, Lucerne, and Cadagno. Aquat Sci 63: 225-249.
9. Bowman JP. (2006). The methanotrophs-the families Methylococcacae and Methylocystaceae. In: Balows AT, Truper HG, Dworkin M, Harder W, Schleifer KH (eds) The Prokaryotes. Springer: Berlin, Heidelberg, Germany; New York, NY, USA, pp 266-289.
10. Bussmann I, Pester M, Brune A, Schink B. (2004). Preferential cultivation of type II methanotrophic bacteria from littoral sediments (Lake Constance). FEMS Microbiol Ecol 47: 179-189.
11. Camacho A, Erez J, Chicote A, Florin M, Squires MM, Lehmann C et al. (2001). Microbial microstratification, inorganic carbon photoassimilation and dark carbon fixation at the chemocline of the meromictic Lake Cadagno (Switzerland) and its relevance to the food web. Aquat Sci 63: 91-106.
12. Chen Y, Dumont MG, Cebron A, Murrell JC. (2007). Identification of active methanotrophs in a landfill cover soil through detection of expression of 16S rRNA and functional genes. Environ Microbiol 9: 2855-2869.
13. Cline JD. (1969). Spectrophotometric determination of hydrogen sulfide in natural waters. Limnol Oceanogr 14: 454-458.
14. Costello AM, Lidstrom ME. (1999). Molecular characterization of functional and phylogenetic genes from natural populations of methanotrophs in lake sediments. Appl Environ Microbiol 65: 5066-5074.
15. Ettwig KF, Shima S, van de Pas-Schoonen KT, Kahnt J, Medema MH, op den Camp HJM et al. (2008). Denitrifying bacteria anaerobically oxidize methane in the absence of Archaea. Environ Microbiol 10: 3164-3173.
16. Ettwig KF, Butler MK, Le Paslier D, Pelletier E, Mangenot S, Kuypers MMM et al. (2010). Nitrite-driven anaerobic methane oxidation by oxygenic bacteria. Nature 464: 543-548.
17. Habicht KS, Miller M, Cox RP, Frigaard NU, Tonolla M, Peduzzi S et al. (2011). Comparative proteomics and activity of a green sulfur bacterium through the water column of Lake Cadagno, Switzerland. Environ Microbiol 13: 203-215.
18. Hales BA, Edwards C, Ritchie DA, Hall G, Pickup RW, Saunders JR. (1996). Isolation and identification of methanogen-specific DNA from blanket bog feat by PCR amplification and sequence analysis. Appl Environ Microbiol 62: 668-675.
19. Halm H, Musat N, Lam P, Langlois R, Musat F, Peduzzi S et al. (2009). Co-occurrence of denitrification and nitrogen fixation in a meromictic lake, Lake Cadagno (Switzerland). Environ Microbiol 11: 1945-1958.
20. Hanson RS, Hanson TE. (1996). Methanotrophic bacteria. Microbiol Rev 60: 439-471.
21. Haroon MF, Hu S, Shi Y, Imelfort M, Keller J, Hugenholtz P et al. (2013). Anaerobic oxidation of methane coupled to nitrate reduction in a novel archaeal lineage. Nature 500: 567-570.
22. Hinrichs KU, Boetius A. (2002). The anaerobic oxidation of methane: new insights in microbial ecology and biogeochemistry. In: Wefer G, Hebbeln DB, Jørgensen BB, Schluter M, van Weering TCE (eds). Ocean Margin Systems. Springer-Verlag: Berlin, Germany, pp 457-477.
23. Holland HD. (2006). The oxygenation of the atmosphere and oceans. Phil Trans R Soc B 361: 903-915.
24. Holler T, Wegener G, Knittel K, Boetius A, Brunner B, Kuypers MMM et al. (2009). Substantial 13C/12C and D/H fractionation during anaerobic oxidation of methane by marine consortia enriched in vitro. Environ Microbiol Rep 1: 370-376.
25. Holmes AJ, Costello A, Lidstrom ME, Murrell JC. (1995). Evidence that particulate methane monooxygenase and ammonia monooxygenase may be evolutionarily related. FEMS Microbiol Lett 132: 203-208.
26. Holmes RM, Aminot A, Kerouel R, Hooker BA, Peterson BJ. (1999). A simple and precise method for measuring ammonium in marine and freshwater ecosystems. Can J Fish Aquat Sci 56: 1801-1808.
27. Holtappels M, Lavik G, Jensen MM, Kuypers MMM. (2011). 15 N-Labeling experiments to dissect the contributions of heterotrophic denitrification and anammox to nitrogen removal in the OMZ waters of the Ocean. In: Klotz MG (ed). Methods in Enzymology (Research on Nitrification and Related Processes, Part ). Academic Press: Burlington, NJ, USA, pp 223-251.
28. Hutchens E, Radajewski S, Dumont MG, Mcdonald IR, Murrell JC. (2004). Analysis of methanotrophic bacteria in Movile Cave by stable isotope probing. Environ Microbiol 6: 111-120.
29. Knittel K, Boetius A. (2009). Anaerobic oxidation of methane: progress with an unknown process. Ann Rev Microbiol 63: 311-334.
30. King GM. (1990). Regulation by light of methane emissions from a wetland. Nature 345: 513-515.
31. Kirf MK, Dinkel C, Schubert CJ, Wehrli B. (2014). Submicromolar oxygen profiles at the oxic-anoxic boundary of temperate lakes. Aquat Geochem 20: 39-57.
32. Lidstrom ME, Somers L. (1984). Seasonal study of methane oxidation in Lake Washington. Appl Environ Microbiol 47: 1255-1260.
33. Luesken FA, Zhu BL, van Alen TA, Butler MK, Diaz MR, Song B et al. (2011). pmoA primers for detection of anaerobic methanotrophs. Appl Environ Microbiol 77: 3877-3880.
34. McDonald IR, Kenna EM, Murrell JC. (1995). Detection of methanotrophic bacteria in environmental samples with the PCR. Appl Environl Microbiol 61: 116-121.
35. Milucka J, Ferdelman TG, Polerecky L, Franzke D, Wegener G, Schmid M et al. (2012). Zero-valent sulphur is a key intermediate in marine methane oxidation. Nature 491: 541-546.
36. Musat N, Halm H, Winterholler B, Hoppe P, Peduzzi S, Hillion F et al. (2008). A single-cell view on the ecophysiology of anaerobic phototrophic bacteria. Proc Natl Acad Sci USA 105: 17861-17866.
37. Nercessian O, Noyes E, Kalyuzhnaya MG, Lidstrom ME, Chistoserdova L. (2005). Bacterial populations active in metabolism of C-1 compounds in the sediment of Lake Washington, a freshwater lake. Appl Environ Microbiol 71: 6885-6899.
38. Noll M, Frenzel P, Conrad R. (2008). Selective stimulation of type I methanotrophs in a rice paddy soil by urea fertilization revealed by RNA-based stable isotope probing. FEMS Microbiol Ecol 65: 125-132.
39. Patel RN, Hoare DS. (1971). Physiological studies of methane and methanol-oxidizing bacteria-oxidation of C-1 compounds by Methylococcus capsulatus. J Bacteriol 107: 187-192.
40. Peduzzi S, Tonolla M, Hahn D. (2003). Vertical distribution of sulfate-reducing bacteria in the chemocline of Lake Cadagno, Switzerland, over an annual cycle. Aquat Microb Ecol 30: 295-302.
41. Polerecky L, Adam B, Milucka J, Musat N, Vagner T, Kuypers MMM. (2012). Look@NanoSIMS-a tool for the analysis of nanoSIMS data in environmental microbiology. Environ Microbiol 14: 1009-1023.
42. Powell T, Jassby A. (1974). The estimation of vertical eddy diffusivities below the thermocline in lakes. Water Resour Res 10: 191-198.
43. Qiu QF, Noll M, Abraham WR, Lu YH, Conrad R. (2008). Applying stable isotope probing of phospholipid fatty acids and rRNA in a Chinese rice field to study activity and composition of the methanotrophic bacterial communities in situ. ISME J 2: 602-614.
44. Raghoebarsing AA, Pol A, van de Pas-Schoonen KT, Smolders AJP, Ettwig KF, Rijpstra WIC et al. (2006). A microbial consortium couples anaerobic methane oxidation to denitrification. Nature 440: 918-921.
45. Rasigraf O, Vogt C, Richnow HH, Jetten MSM, Ettwig KF. (2012). Carbon and hydrogen isotope fractionation during nitrite-dependent anaerobic methane oxidation by Methylomirabilis oxyfera. Geochim Cosmochim Acta 89: 256-264.
46. Reeburgh WS, Tyler SC, Carroll J. (2006). Stable carbon and hydrogen isotope measurements on Black Sea water-column methane. Deep-Sea Res Pt II 53: 1893-1900.
47. Reeburgh WS. (2007). Oceanic methane biogeochemistry. Chem Rev 107: 486-513.
48. Rhee TS, Kettle AJ, Andreae MO. (2009). Methane and nitrous oxide emissions from the ocean: a reassessment using basin-wide observations in the Atlantic. J Geophys Res 114: 1-20.
49. Roslev P, King GM. (1995). Aerobic and anaerobic starvation metabolism in methanotrophic bacteria. Appl Environ Microbiol 61: 1563-1570.
50. Scheller S, Goenrich M, Boecher R, Thauer RK, Jaun B. (2010). The key nickel enzyme of methanogenesis catalyses the anaerobic oxidation of methane. Nature 465: 606-608.
51. Schubert CJ, Diem T, Eugster W. (2012). Methane emissions from a small wind shielded lake determined by Eddy covariance, flux chambers, anchored funnels, and boundary model calculations: a comparison. Environ Sci Technol 46: 4515-4522.
52. Schubert CJ, Lucas FS, Durisch-Kaiser E, Stierli R, Diem T, Scheidegger O et al. (2010). Oxidation and emission of methane in a monomictic lake (Rotsee, Switzerland). Aquat Sci 72: 455-466.
53. Sivan O, Adler M, Pearson A, Gelman F, Bar-Or I, John SG et al. (2011). Geochemical evidence for iron-mediated anaerobic oxidation of methane. Limnol Oceanogr 56: 1536-1544.
54. Springer E, Sachs MS, Woese CR, Boone DR. (1995). Partial gene sequences for the a subunit of methylcoenzyme M reductase (McrI) as a phylogenetic tool for the family Methanosarcinaceae. Int J Syst Bacteriol 45: 554-559.
55. Stookey LL. (1970). Ferrozine-A new spectrophotometric reagent for iron. Anal Chem 42: 779-781.
56. Storelli N, Peduzzi S, Saad MM, Frigaard NU, Perret X, Tonolla M. (2013). CO2 assimilation in the chemocline of Lake Cadagno is dominated by a few types of phototrophic purple sulfur bacteria. FEMS Microbiol Ecol 84: 421-432.
57. Tamas I, Smirnova AV, He Z, Dunfield PF. (2014). The (d)evolution of methanotrophy in the Beijerinckiaceae-A comparative genomics analysis. ISME J 8: 369-382.
58. Templeton AS, Chu KH, Alvarez-Cohen L, Conrad ME. (2006). Variable carbon isotope fractionation expressed by aerobic CH4-oxidizing bacteria. Geochim Cosmochim Acta 70: 1739-1752.
59. Tonolla M, Peduzzi R, Hahn D. (2005). Long-term population dynamics of phototrophic sulfur bacteria in the chemocline of Lake Cadagno, Switzerland. Appl Environ Microbiol 71: 3544-3550.
60. Trotsenko Y, Murrell JC. (2008). Metabolic aspects of aerobic obligate methanotrophy. In: Laskin AI, Sariaslani S, Gadd G (eds). Advances in Applied Microbiology. Elsevier: Amsterdam, the Netherlands, pp 183-229.
61. Uhde MAC. (1992). Mischungsprozesse im hypolimnion des meromiktischen Lago di Cadagno: eine untersuchung mit hilfe naturlicher und kunstlicher tracer. Unpublished MSc Thesis, Albert Ludwigs Universitat Freiburg. Library Eawag: Duebendorf, Switzerland, p 90.
62. van der Ha D, Bundervoet B, Verstraete W, Boon N. (2011). A sustainable, carbon neutral methane oxidation by a partnership of methane oxidizing communities and microalgae. Water Res 45: 2845-2854.
63. van der Ha D, Nachtergaele L, Kerckhof M, Rameiyant D, Bossier P, Verstraete W et al. (2012). Conversion of biogas to bioproducts by algae and methane oxidizing bacteria. Environ Sci Technol 46: 13425-13431.
64. Wagener S, Schulz S, Hanselmann K. (1990). Abundance and distribution of anaerobic protozoa and their contribution to methane production in Lake Cadagno (Switzerland). FEMS Microbiol Ecol 74: 39-48.
65. Wang P, Wang F, Xu M, Xiao X. (2004). Molecular phylogeny of methylotrophs in a deep-sea sediment from a tropical west Pacific warm pool. FEMS Microbiol Ecol 47: 77-84.
66. Wankel SD, Adams MM, Johnston DT, Hansel CM, Joye SB, Girguis PR. (2012). Anaerobic methane oxidation in metalliferous hydrothermal sediments: influence on carbon flux and decoupling from sulfate reduction. Environ Microbiol 14: 2726-2740.
67. Wiesenburg DA, Guinasso NL. (1979). Equilibrium solubilities of methane, carbon monoxide, and hydrogen in water and sea-water. J Chem Eng Data 24: 356-360.
68. Wuest A. (1994). Interactions in lakes: biology as source of dominant physical forces. Limnologica 24: 93-104.