Microbial minorities modulate methane consumption through niche partitioning

ISME Journal

Volumn 7, Issue 11, 2013, Pages 2214-2228

  Bodelier, Paul L E ^a   Meima Franke, Marion ^a   Hordijk, Cornelis A ^a   Steenbergh, Anne K ^a   Hefting, Mariet M ^b   Bodrossy, Levente ^c   Von Bergen, Martin ^d,e   Seifert, Jana ^d,f  

^a NETHERLANDS INSTITUTE OF ECOLOGY NIOO KNAW   (Netherlands)

^b UTRECHT UNIVERSITY   (Netherlands)

^c CSIRO   (Australia)

^d HELMHOLTZ CENTRE FOR ENVIRONMENTAL RESEARCH UFZ   (Germany)

^e AALBORG UNIVERSITY   (Denmark)

^f UNIVERSITY OF HOHENHEIM   (Germany)

Author keywords

biodiversity ecosystem functioning; methane oxidation; proteomics; stable isotope labeling; wetlands

Indexed keywords

CARBON; METHANE;

COMMUNITY COMPOSITION; ECOSYSTEM FUNCTION; FLOODING; FLOODPLAIN; METHANE; MICROBIAL COMMUNITY; NICHE PARTITIONING; PROTEOMICS; RELATIVE ABUNDANCE; STABLE ISOTOPE; WETLAND;

ARTICLE; BACTERIUM; BIODIVERSITY; CHEMISTRY; GENETICS; METABOLISM; MICROBIOLOGY; MOLECULAR GENETICS; OXIDATION REDUCTION REACTION; SOIL; WETLAND;

BACTERIA; BIODIVERSITY; CARBON ISOTOPES; METHANE; MOLECULAR SEQUENCE DATA; OXIDATION-REDUCTION; SOIL; SOIL MICROBIOLOGY; WETLANDS;

BACTERIA (MICROORGANISMS); PROTEOBACTERIA;

EID: 84886718646     PISSN: 17517362     EISSN: 17517370     Source Type: Journal    
DOI: 10.1038/ismej.2013.99     Document Type: Article

References (80)

1. Bell T, Gessner MO, Griffiths RI, McLaren J, Morin PJ, van der Heijden M et al. (2009). Microbial biodiversity and ecosystem functioning under controlled conditions and in the wild. In: Naeem SB, Bunker DE, Hector A, Loreau M, Perrings C (eds) Biodiversity, Ecosystem Functioning, and Human Wellbeing: An Ecological and Economic Perspective. Oxford University Press: Oxford, pp 121-133.
2. Belova SE, Baani M, Suzina NE, Bodelier PLE, Liesack W, Dedysh SN. (2011). Acetate utilization as a survival strategy of peat-inhabiting Methylocystis spp. Environ Microbiol Rep 3: 36-46.
3. Benndorf D, Balcke GU, Harms H, von Bergen M. (2007). Functional metaproteome analysis of protein extracts from contaminated soil and groundwater. ISME J 1: 224-234.
4. Benndorf D, Vogt C, Jehmlich N, Schmidt Y, Thomas H, Woffendin G et al. (2009). Improving protein extraction and separation methods for investigating the metaproteome of anaerobic benzene communities within sediments. Biodegradation 20: 737-750.
5. Bloom AA, Palmer PI, Fraser A, Reay DS, Frankenberg C. (2010). Large-scale controls of methanogenesis inferred from methane and gravity spaceborne data. Science 327: 322-325.
6. Bodelier PLE, Hahn AP, Arth IR, Frenzel P. (2000). Effects of ammonium-based fertilisation on microbial processes involved in methane emission from soils planted with rice. Biogeochemistry 51: 225-257.
7. Bodelier PLE. (2011). Toward understanding, managing, and protecting microbial ecosystems. Front Microbiol 2: 80.
8. Bodelier PLE, Bar-Gilissen MJB, Meima-Franke M, Hordijk K. (2012). Structural and functional response of methane-consuming microbial communities to different flooding regimes in riparian soils. Ecol Evol 2: 106-127.
9. Bodelier PLE, Bar-Gillisen MJB, Hordijk K, Sinninghe Damsté JSS, Rijpstra WIC, Geenevasen JAJ et al. (2009). A reanalysis of phospholipid fatty acids as ecological biomarkers for methanotrophic bacteria. ISME J 3: 606-616.
10. Boden R, Cunliffe M, Scanlan J, Moussard H, Kits KD, Klotz MG et al. (2011). Complete genome sequence of the aerobic marine methanotroph methylomonas methanica MC09. J Bacteriol 193: 7001-7002.
11. Boschker HTS, Nold SC, Wellsbury P, Bos D, de Graaf W, Pel R et al. (1998). Direct linking of microbial populations to specific biogeochemical processes by C-13-labelling of biomarkers. Nature 392: 801-805.
12. Bousquet P, Ciais P, Miller JB, Dlugokencky EJ, Hauglus-taine DA, Prigent C et al. (2006). Contribution of anthropogenic and natural sources to atmospheric methane variability. Nature 443: 439-443.
13. Caliman A, Pires AF, Esteves FA, Bozelli RL, Farjalla VF. (2010). The prominence of and biases in biodiversity and ecosystem functioning research. Biodivers Con-serv 19: 651-664.
14. Cardinale BJ, Srivastava DS, Duffy JE, Wright JP, Downing AL, Sankaran M et al. (2006). Effects of biodiversity on the functioning of trophic groups and ecosystems. Nature 443: 989-992.
15. Cardinale BJ. (2011). Biodiversity improves water quality through niche partitioning. Nature 472: 86-89.
16. Cardinale BJ, Duffy JE, Gonzalez A, Hooper DU, Perrings C, Venail P et al. (2012). Biodiversity loss and its impact on humanity. Nature 486: 59-67.
17. 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.
18. Chourey K, Jansson J, VerBerkmoes N, Shah M, Chavarria KL, Tom LM et al. (2010). Direct cellular lysis/protein extraction protocol for soil metaproteomics. J Proteome Res 9: 6615-6622.
19. Cockell CS, Jones HL. (2009). Advancing the case for microbial conservation. Oryx 43: 520-526.
20. Conrad R. (2007). Microbial ecology of methanogens and methanotrophs. Adv Agron 96: 1-63.
21. Dam B, Dam S, Kube M, Reinhardt R, Liesack W. (2012). Complete genome sequence of Methylocystis sp strain SC2, an aerobic methanotroph with high-affinity methane oxidation potential. J Bacteriol 194: 6008-6009.
22. Daniell TJ, Davidson J, Alexander CJ, Caul S, Roberts DM. (2012). Improved real-time PCR estimation of gene copy number in soil extracts using an artificial reference. J Microbiol Methods 91: 38-44.
23. Dedysh SN, Knief C, Dunfield PF. (2005). Methylocella species are facultatively methanotrophic. J Bacteriol 187: 4665-4670.
24. Dedysh SN, Belova SE, Bodelier PLE, Smirnova KV, Khmelenina VN, Chidthaisong A et al. (2007). Methy-locystis heyeri sp nov., a novel type II methanotrophic bacterium possessing 'signature' fatty acids of type I methanotrophs. Int J Syst Evol Microbiol 57: 472-479.
25. del Cerro C, Garcia JM, Rojas A, Tortajada M, Ramon D, Galan B et al. (2012). Genome sequence of the methanotrophic poly-beta-hydroxybutyrate producer Methylocystis parvus OBBP. J Bacteriol 194: 5709-5710.
26. Dumont MG, Pommerenke B, Casper P, Conrad R. (2011). DNA-, rRNA-and mRNA-based stable isotope probing of aerobic methanotrophs in lake sediment. Environ Microbiol 13: 1153-1167.
27. 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 Verrucomicrobia. Nature 450: 879-882.
28. 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.
29. Falkowski PG, Fenchel T, Delong EF. (2008). The micro-bial engines that drive Earth's biogeochemical cycles. Science 320: 1034-1039.
30. Freitag TE, Toet S, Ineson P, Prosser JI. (2010). Links between methane flux and transcriptional activities of methanogens and methane oxidizers in a blanket peat bog. FEMS Microbiol Ecol 73: 157-165.
31. Gans J, Wolinsky M, Dunbar J. (2005). Computational improvements reveal great bacterial diversity and high metal toxicity in soil. Science 309: 1387-1390.
32. Graef C, Hestnes AG, Svenning MM, Frenzel P. (2011). The active methanotrophic community in a wetland from the High Arctic. Environ Microbiol Rep 3: 466-472.
33. Griffith GW. (2012). Do we need a global strategy for microbial conservation? Trends Ecol Evol 27: 1-2.
34. Hillebrand H, Matthiessen B. (2009). Biodiversity in a complex world: consolidation and progress in functional biodiversity research. Ecol Lett 12: 1405-1419.
35. Ho A, Lüke C, Cao ZH, Frenzel P. (2011). Ageing well: methane oxidation and methane oxidizing bacteria along a chronosequence of 2000 years. Environ Microbiol Rep 3: 738-743.
36. Ho A, Kerckhof FM, Lüke C, Reim A, Krause SMB, Boon N et al. (2013). Conceptualizing functional traits and ecological characteristics of methane-oxidizing bacteria as life strategies. Environ Microbiol Rep 5: 335-345.
37. Holmes AJ, Costello A, Lidstrom ME, Murrell JC. (1995). Evidence that particulate methane monooxygenase and ammonia monooxygenase may be evolutionary related. FEMS Microbiol Lett 132: 203-208.
38. Jahnke LL, Summons RE, Hope JM, des Marais DJ. (1999). Carbon isotopic fractionation in lipids from methano-trophic bacteria II: the effects of physiology and environmental parameters on the biosynthesis and isotopic signatures of biomarkers. Geochim Cosmo-chim Acta 63: 79-93.
39. Jehmlich N, Schmidt F, Taubert M, Seifert J, Bastida F, von Bergen M et al. (2010). Protein-based stable isotope probing. Nat Protoc 5: 1957-1966.
40. Kai FM, Tyler SC, Randerson JT, Blake DR. (2011). Reduced methane growth rate explained by decreased Northern Hemisphere microbial sources. Nature 476: 194-197.
41. Keiblinger KM, Wilhartitz IC, Schneider T, Roschitzki B, Schmid E, Eberl L et al. (2012). Soil metaproteomics-comparative evaluation of protein extraction protocols. Soil Biol Biochem 54: 14-24.
42. Kemnitz D, Chin KJ, Bodelier P, Conrad R. (2004). Community analysis of methanogenic archaea within a riparian flooding gradient. Environ Microbiol 6: 449-461.
43. Khadem AF, Pol A, Wieczorek A, Mohammadi SS, Francoijs K-J, Stunnenberg HG et al. (2011). Auto-trophic methanotrophy in Verrucomicrobia: Methylacidiphilum fumariolicum SolV uses the Calvin-Benson-Bassham cycle for carbon dioxide fixation. J Bacteriol 193: 4438-4446.
44. Kleiveland CR, Hult LTO, Kuczkowska K, Jacobsen M, Lea T, Pope PB. (2012). Draft genome sequence of the methane-oxidizing bacterium Methylococcus capsula-tus (Texas). J Bacteriol 194: 6626-6626.
45. Kolb S, Knief C, Stubner S, Conrad R. (2003). Quantitative detection of methanotrophs in soil by novel pmoA-targeted real-time PCR assays. Appl Environ Microbiol 69: 2423-2429.
46. Kuramae EE, Yergeau E, Wong LC, Pijl AS, van Veen JA, Kowalchuk GA. (2012). Soil characteristics more strongly influence soil bacterial communities than land-use type. FEMS Microbiol Ecol 79: 12-24.
47. Lennon JT, Jones SE. (2011). Microbial seed banks: the ecological and evolutionary implications of dormancy. Nat Rev Microbiol 9: 119-130.
48. Levine UY, Teal TK, Robertson GP, Schmidt TM. (2011). Agriculture's impact on microbial diversity and associated fluxes of carbon dioxide and methane. ISME J 5: 1683-1691.
49. Loreau M. (2010). Linking biodiversity and ecosystems: towards a unifying ecological theory. Philos Trans R Soc Lond B Biol Sci 365: 49-60.
50. Lüke C, Frenzel P. (2011). Potential of pmoA amplicon pyrosequencing for methanotroph diversity studies. Appl Environ Microbiol 77: 6305-6309.
51. McDonald IR, Bodrossy L, Chen Y, Murrell JC. (2008). Molecular ecology techniques for the study of aerobic methanotrophs. Appl Environ Microbiol 74: 1305-1315.
52. Mohanty SR, Bodelier PLE, Floris V, Conrad R. (2006). Differential effects of nitrogenous fertilizers on methane-consuming microbes in rice field and forest soils. Appl Environ Microbiol 72: 1346-1354.
53. Monard C, Vandenkoornhuyse P, Le Bot B, Binet F. (2011). Relationship between bacterial diversity and function under biotic control: the soil pesticide degraders as a case study. ISME J 5: 1048-1056.
54. Mora C, Tittensor DP, Adl S, Simpson AGB, Worm B. (2011). How many species are there on earth and in the ocean? PLoS Biol 9: e1001127.
55. 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.
56. Neufeld JD, Wagner M, Murrell JC. (2007). Who eats what, where and when? Isotope-labelling experiments are coming of age. ISME J 1: 103-110.
57. Op den Camp HJM, Islam T, Stott MB, Harhangi HR, Hynes A, Schouten S et al. (2009). Environmental, genomic and taxonomic perspectives on methano-trophic Verrucomicrobia. Environ Microbiol Rep 1: 293-306.
58. Pan Y, Bodrossy L, Frenzel P, Hestnes A, Krause SBM, Lüke C et al. (2010). Impacts of inter-and intralabora-tory variations on the reproducibility of microbial community analyses. Appl Environ Microbiol 76: 7451-7458.
59. Paszczynski AJ, Paidisetti R, Johnson AK, Crawford RL, Colwell FS, Green T et al. (2011). Proteomic and targeted qPCR analyses of subsurface microbial communities for presence of methane monooxygenase. Biodegradation 22: 1045-1059.
60. Perkins DN, Pappin DJC, Creasy DM, Cottrell JS. (1999). Probability-based protein identification by searching sequence databases using mass spectrometry data. Electrophoresis 20: 3551-3567.
61. Pester M, Bittner N, Deevong P, Wagner M, Loy A. (2010). A 'rare biosphere' microorganism contributes to sulfate reduction in a peatland. ISME J 4: 1591-1602.
62. Peter H, Beier S, Bertilsson S, Lindstrom ES, Langenheder S, Tranvik LJ. (2011). Function-specific response to depletion of microbial diversity. ISME J 5: 351-361.
63. Pol A, Heijmans K, Harhangi HR, Tedesco D, Jetten MSM, den Camp H. (2007). Methanotrophy below pH1 by a new Verrucomicrobia species. Nature 450: 874-878.
64. Seifert J, Taubert M, Jehmlich N, Schmidt F, Volker U, Vogt C et al. (2012). Protein-based stable isotope probing (protein-SIP) in functional metaproteomics. Mass Spectrom Rev 31: 683-697.
65. Semrau JD, DiSpirito AA, Yoon S. (2010). Methanotrophs and copper. Fems Microbiol Rev 34: 496-531.
66. Semrau JD, DiSpirito AA, Vuilleumier S. (2011). Facultative methanotrophy: false leads, true results, and suggestions for future research. FEMS Microbiol Lett 323: 1-12.
67. Sharp CE, Stott MB, Dunfield PF. (2012). Detection of autotrophic verrucomicrobial methanotrophs in a geothermal environment using stable isotope probing. Front Microbiol 3: 303-303.
68. Spahni R, Wania R, Neef L, van Weele M, Pison I, Bousquet P et al. (2011). Constraining global methane emissions and uptake by ecosystems. Biogeosciences 8: 1643-1665.
69. Steenbergh AK, Meima MM, Kamst M, Bodelier PLE. (2010). Biphasic kinetics of a methanotrophic community is a combination of growth and increased activity per cell. FEMS Microbiol Ecol 71: 12-22.
70. Stein LY, Yoon S, Semrau JD, DiSpirito AA, Crombie A, Murrell JC et al. (2010). Genome sequence of the obligate methanotroph Methylosinus trichosporium strain OB3b. J Bacteriol 192: 6497-6498.
71. Stein LY, Bringel F, DiSpirito AA, Han S, Jetten MSM, Kalyuzhnaya MG et al. (2011). Genome sequence of the methanotrophic Alphaproteobacterium Methylocystis sp strain Rockwell (ATCC 49242). J Bacteriol 193: 2668-2669.
72. Stein LY, Roy R, Dunfield PF. (2012). Aerobic Methano-trophy and Nitrification: Processes and Connections. eLS. John Wilet & Sons Ltd.: Chichester.
73. Taubert M, Jehmlich N, Vogt C, Richnow HH, Schmidt F, von Bergen M et al. (2011). Time resolved protein-based stable isotope probing (protein-SIP) analysis allows quantification of induced proteins in substrate shift experiments. Proteomics 11: 2265-2274.
74. 4-oxidizing bacteria. Geochim Cosmochim Acta 70: 1739-1752.
75. Wang J, Krause S, Muyzer G, Meima-Franke M, Laanbroek HJ, Bodelier PLE. (2012). Spatial patterns of iron-and methane-oxidizing bacterial communities in an irregularly flooded, riparian wetland. Front Microbiol 3: 64-64.
76. Ward N, Larsen O, Sakwa J, Bruseth L, Khouri H, Durkin AS et al. (2004). Genomic insights into methanotro-phy: the complete genome sequence of Methylococcus capsulatus (Bath). PLoS Biol 2: 1616-1628.
77. Wessen E, Hallin S, Philippot L. (2010). Differential responses of bacterial and archaeal groups at high taxonomical ranks to soil management. Soil Biol Biochem 42: 1759-1765.
78. Whitman WB, Coleman DC, Wiebe WJ. (1998). Prokar-yotes: the unseen majority. Proc Natl Acad Sci USA 95: 6578-6583.
79. Wohl DL, Arora S, Gladstone JR. (2004). Functional redundancy supports biodiversity and ecosystem function in a closed and constant environment. Ecology 85: 1534-1540.
80. 13C-labeling study. Front Microbiol 4: 70.