Distribution and activity of the anaerobic methanotrophic community in a nitrogen-fertilized Italian paddy soil

FEMS Microbiology Ecology

Volumn 92, Issue 12, 2016, Pages

  Vaksmaa, A ^a   Luke C ^a   van Alen, T ^a   Vale G ^b   Lupotto, E ^b   Jetten, M S M ^a   Ettwig, K F ^a  

^a RADBOUD UNIVERSITY NIJMEGEN   (Netherlands)

^b CRA RIS Rice Research Unit   (Italy)

Author keywords

16S rRNA gene; Amplicon sequencing; Anaerobic oxidation of methane; Methanoperedens nitroreducens; AAA; Microbial community; Paddy fields; Rice rhizosphere

Indexed keywords

ANOXIC CONDITIONS; FERTILIZER APPLICATION; GENE EXPRESSION; GENETIC ANALYSIS; METHANE; METHANOGENIC BACTERIUM; METHANOTROPHY; MICROBIAL COMMUNITY; NITROGEN; OXIDATION; PADDY FIELD; PHYLOGENETICS; RHIZOSPHERE; RICE;

ITALY;

ARCHAEA; BACTERIA (MICROORGANISMS);

EID: 84995784291     PISSN: 01686496     EISSN: 15746941     Source Type: Journal    
DOI: 10.1093/femsec-fiw181     Document Type: Article

References (70)

1. Ahn JH, JeongWS, Choi MY et al. Phylogenetic diversity of dominant bacterial and archaeal communities in plant-microbial fuel cells using rice plants. J Microbiol Biotechnol 2014;24: 1707-18.
2. Ahn JH, Song J, Kim BY et al. Characterization of the bacterial and archaeal communities in rice field soils subjected to longterm fertilization practices. J Microbiol 2012;50:754-65.
3. Arshad A, Speth DR, de Graaf RM et al. A metagenomics-based metabolic model of nitrate-dependent anaerobic oxidation of methane by methanoperedens-like archaea. Front Microbiol 2015;6:1423.
4. Aslam Z, Yasir M, Yoon HS et al. Diversity of the bacterial community in the rice rhizosphere managed under conventional and no-tillage practices. J Microbiol 2013;51:747-56.
5. Bodelier PLE. Interactions between nitrogenous fertilizers and methane cycling in wetland and upland soils. Curr Opin Env Sust 2011;3:379-88.
6. Boetius A, Wenzhofer F. Seafloor oxygen consumption fuelled by methane from cold seeps. Nat Geosci 2013;6:725-34.
7. Borrel G, Jézéquel D, Biderre-Petit C et al. Production and consumption of methane in freshwater lake ecosystems. Res Microbiol 2011;162:832-47.
8. Camacho C, Coulouris G, Avagyan V et al. BLAST+: architecture and applications. BMC Bioinformatics 2009;10:421.
9. Conrad R. Microbial ecology of methanogens and methanotrophs. Adv Agron 2007;96:1-63.
10. Conrad R. The global methane cycle: recent advances in understanding the microbial processes involved. Environ Microbiol Rep 2009;1:285-92.
11. Conrad R, Klose M. Dynamics of the methanogenic archaeal community in anoxic rice soil upon addition of straw. Eur J Soil Sci 2006;57:476-84.
12. Conrad R, Klose M, Noll M et al. Soil type links microbial colonization of rice roots to methane emission. Global Change Biol 2008;14:657-69.
13. Daebeler A, Gansen M, Frenzel P. Methyl fluoride affects methanogenesis rather than community composition of methanogenic archaea in a rice field soil. PLoS One 2013;8: e53656.
14. Deutzmann JS, Schink B. Anaerobic oxidation of methane in sediments of an oligotrophic freshwater lake (Lake Constance). Appl Environ Microbiol 2011;77:4429-36.
15. Deutzmann JS, Stief P, Brandes J et al. Anaerobic methane oxidation coupled to denitrification is the dominant methane sink in a deep lake. Proc Natl Acad Sci U S A 2014;111: 18273-8.
16. Edwards J, Johnson C, Santos-Medellin C et al. Structure, variation, and assembly of the root-associated microbiomes of rice. Proc Natl Acad Sci U S A 2015;112:E911-20.
17. Erkel C, Kube M, Reinhardt R et al. Genome of rice cluster I archaea-the key methane producers in the rice rhizosphere. Science 2006;313:370-2.
18. Ettwig KF, Butler MK, Le Paslier D et al. Nitrite-driven anaerobic methane oxidation by oxygenic bacteria. Nature 2010;464:543-8.
19. Ettwig KF, Shima S, van de Pas-Schoonen KT et al. Denitrifying bacteria anaerobically oxidize methane in the absence of archaea. Environ Microbiol 2008;10:3164-73.
20. Ettwig KF, van Alen T, van de Pas-Schoonen KT et al. Enrichment andmolecular detection of denitrifying methanotrophic bacteria of the NC10 phylum. Appl Environ Microbiol 2009;75: 3656-62.
21. Gilbert BFP. Methanotrophic bacteria in the rhizosphere of rice microcosms and their effect on porewater methane concentration and methane emission. Biol Fertil Soils 1995; 20:93-100.
22. Girguis PR, Orphan VJ, Hallam SJ et al. Growth and Methane Oxidation Rates of Anaerobic Methanotrophic Archaea in a Continuous-Flow Bioreactor. Appl Environ Microbiol 2003;69:5472-82.
23. Haroon MF, Hu S, Shi Y et al. Anaerobic oxidation of methane coupled to nitrate reduction in a novel archaeal lineage. Nature 2013;500:567-70.
24. Herlemann DPR, Labrenz M, Juürgens K et al. Transitions in bacterial communities along the 2000km salinity gradient of the Baltic Sea. ISME J 2011;5:1571-9.
25. Hinrichs KU, Boetius A. The anaerobic oxidation of methane: new insights in microbial ecology and biogeochemistry. In: Wefer G, Billett D, Hebbeln D et al. (eds). Ocean Margin Systems. Heidelberg: Springer, 2002, 457-77.
26. Ho A, Luke C, Cao Z et al. Ageing well: methane oxidation and methane oxidizing bacteria along a chronosequence of 2000 years. Environ Microbiol Rep 2011;3:738-43.
27. Hu BL, Shen LD, Lian X et al. Evidence for nitrite-dependent anaerobic methane oxidation as a previously overlooked microbial methane sink in wetlands. Proc Natl Acad Sci U S A 2014;111:4495-500.
28. Hu S, Zeng RJ, Burow LC et al. Enrichment of denitrifying anaerobic methane oxidizing microorganisms. Environ Microbiol Rep 2009;1:377-84.
29. Hu S, Zeng RJ, Haroon MF et al. A laboratory investigation of interactions between denitrifying anaerobic methane oxidation (DAMO) and anammox processes in anoxic environments. Sci Rep 2015;5:8706.
30. Hug LA, Thomas BC, Sharon I et al. Critical biogeochemical functions in the subsurface are associated with bacteria from new phyla and little studied lineages. Environ Microbiol 2016;18:159-73.
31. Ionescu D, Siebert C, Polerecky L et al. Microbial and Chemical Characterization of Underwater Fresh Water Springs in the Dead Sea. PloS One 2012;7:e38319.
32. Klindworth A, Pruesse E, Schweer T et al. Evaluation of general 16S ribosomal RNA gene PCR primers for classical and nextgeneration sequencing-based diversity studies. Nucleic Acids Res 2013;41:e1.
33. Knittel K, Boetius A. Anaerobic oxidation of methane: progress with an unknown process. Annu Rev Microbiol 2009;63: 311-34.
34. Krause S, Luke C, Frenzel P. Succession of methanotrophs in oxygen-methane counter-gradients of flooded rice paddies. ISME J 2010;4:1603-7.
35. Kruüger M, Frenzel P, Conrad R. Microbial processes influencing methane emission from rice fields. Global Change Biol 2001;7:49-63.
36. Kuzyakov Y, Blagodatskaya E. Microbial hotspots and hot moments in soil: Concept & review. Soil Biol Biochem 2015;83: 184-99.
37. Lee HJ, Jeong SE, Kim PJ et al. High resolution depth distribution of bacteria, archaea, methanotrophs, and methanogens in the bulk and rhizosphere soils of a flooded rice paddy. Front Microbiol 2015;6:639.
38. Lee HJ, Kim SY, Kim PJ et al. Methane emission and dynamics of methanotrophic and methanogenic communities in a flooded rice field ecosystem. FEMS Microbiol Ecol 2014;88: 195-212.
39. Li W, Godzik A. Cd-hit: a fast program for clustering and comparing large sets of protein or nucleotide sequences. Bioinformatics 2006;22:1658-9.
40. Lloyd KG, Lapham L, Teske A. An anaerobic methane-oxidizing community of ANME-1b archaea in hypersaline Gulf of Mexico sediments. Appl Environ Microbiol 2006;72:7218-30.
41. Lueders T, Chin KJ, Conrad R et al. Molecular analyses of methylcoenzyme M reductase alpha-subunit (mcrA) genes in rice field soil and enrichment cultures reveal the methanogenic phenotype of a novel archaeal lineage. Environ Microbiol 2001;3:194-204.
42. Luüke C, Frenzel P. Potential of pmoA amplicon pyrosequencing for methanotroph diversity studies. Appl EnvironMicrobiol 2011;77:6305-9.
43. Luesken F, van Alen T, van der Biezen E et al. Diversity and enrichment of nitrite-dependent anaerobic methane oxidizing bacteria fromwastewater sludge. Appl Microbiol Biotechnol 2011;92:845-54.
44. Mills HJ, Hodges C, Wilson K et al. Microbial diversity in sediments associated with surface-breaching gas hydrate mounds in the Gulf of Mexico. FEMS Microbiol Ecol 2003;46: 39-52.
45. Mills HJ, Martinez RJ, Story S et al. Characterization of microbial community structure in Gulf of Mexico gas hydrates: comparative analysis of DNA-and RNA-derived clone libraries. Appl Environ Microbiol 2005;71:3235-47.
46. Milucka J, Widdel F, Shima S. Immunological detection of enzymes for sulfate reduction in anaerobic methane-oxidizing consortia. Environ Microbiol 2012;15:1561-71.
47. Muyzer G, de Waal EC, Uitterlinden AG. Profiling of complex microbial populations by denaturing gradient gel electrophoresis analysis of polymerase chain reaction-amplified genes coding for 16S rRNA. Appl Environ Microbiol 1993; 59:695-700.
48. Myhre G, Shindell D, Bréon FM et al. Anthropogenic and natural radiative forcing. In: Stocker TF, Qin D, Plattner G-K et al. (eds). Climate Change 2013: The Physical Science Basis. Contribution of Working Group I to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge and New York: Cambridge University Press, 2013, 659-740.
49. Nauhaus K, Boetius A, Kruüger M et al. In vitro demonstration of anaerobic oxidation of methane coupled to sulphate reduction in sediment from a marine gas hydrate area. Environ Microbiol 2002;4:296-305.
50. Ondov BD, Bergman NH, Phillippy AM. Interactive metagenomic visualization in a Web browser. BMC Bioinformatics 2011;12:385.
51. Op den Camp HJM, Islam T, Stott MB et al. Environmental, genomic and taxonomic perspectives on methanotrophic Verrucomicrobia. Environ Microbiol Rep 2009;1:293-306.
52. Pruesse E, Peplies J, Glockner FO. SINA: accurate highthroughput multiple sequence alignment of ribosomal RNA genes. Bioinformatics 2012;28:1823-9.
53. Quast C, Pruesse E, Yilmaz P et al. The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res 2013;41:D590-6.
54. Raghoebarsing AA, Pol A, van de Pas-Schoonen KT et al. A microbial consortium couples anaerobic methane oxidation to denitrification. Nature 2006;440:918-21.
55. Reeburgh WS. Methane consumption in Cariaco Trench waters and sediments. Earth Planet Sci Lett 1976;28:337-44.
56. Scheller S, Yu H, Chadwick GL et al. Artificial electron acceptors decouple archaeal methane oxidation from sulfate reduction. Science 2016;351:703-7.
57. Schubert CJ, Vazquez F, Lösekann-Behrens T et al. Evidence for anaerobic oxidation of methane in sediments of a freshwater system (Lago di Cadagno). FEMS Microbiol Ecol 2011;76: 26-38.
58. Semrau JD, DiSpirito AA, Yoon S. Methanotrophs and copper. FEMS Microbiol Rev 2010;34:496-531.
59. Sharp CE, Smirnova AV, Graham JM et al. Distribution and diversity of Verrucomicrobia methanotrophs in geothermal and acidic environments. Environ Microbiol 2014;16: 1867-78.
60. Sharp CE, Stott MB, Dunfield PF. Detection of autotrophic verrucomicrobial methanotrophs in a geothermal environment using stable isotope probing. Front Microbiol 2012;3:303.
61. Söhngen NL. Uüber Bakterien, welche Methan als Kohlenstoffnahrung und Energiequelle gebrauchen. Zentrabl Bakteriol Parasitenk Infektionskr 1906;15:513-7.
62. Strous M, Jetten MSM. Anaerobic oxidation of methane and ammonium. Annu Rev Microbiol 2004;58:99-117.
63. Takai K, Horikoshi K. Rapid detection and quantification of members of the archaeal community by quantitative PCR using fluorogenic probes. Appl Environ Microbiol 2000;66: 5066-72.
64. Trotsenko YA, Murrell JC. Metabolic aspects of aerobic obligate methanotrophy. Adv Appl Microbiol 2008;63:183-229.
65. van Teeseling MCF, Pol A, Harhangi HR et al. Expanding the verrucomicrobial methanotrophic world: description of three novel species of Methylacidimicrobium gen. nov. Appl Environ Microbiol 2014;80:6782-91.
66. Wang Y, Zhu G, Harhangi HR et al. Co-occurrence and distribution of nitrite-dependent anaerobic ammonium and methane-oxidizing bacteria in a paddy soil. FEMS Microbiol Lett 2012;336:79-88.
67. Watanabe T, KimuraM, Asakawa S. Distinct members of a stable methanogenic archaeal community transcribe mcrA genes under flooded and drained conditions in Japanese paddy field soil. Soil Biol Biochem 2009;41:276-85.
68. Winkler MK, Ettwig KF, Vannecke TP et al. Modelling simultaneous anaerobic methane and ammonium removal in a granular sludge reactor. Water Res 2015;73:323-31.
69. Xu Y, Ma K, Huang S et al. Diel cycle of methanogen mcrA transcripts in rice rhizosphere. Environ Microbiol Rep 2012;4: 655-63.
70. Zhu B, van Dijk G, Fritz C et al. Anaerobic oxidization of methane in aminerotrophic peatland: enrichment of nitritedependent methane-oxidizing bacteria. Appl Environ Microbiol 2012;78:8657-65.