Intercellular wiring enables electron transfer between methanotrophic archaea and bacteria

Nature

Volumn 526, Issue 7574, 2015, Pages 587-590

  Wegener, Gunter ^a,b   Krukenberg, Viola ^a   Riedel, Dietmar ^c   Tegetmeyer, Halina E ^d,e   Boetius, Antje ^a,b,d  

^a MAX PLANCK INSTITUTE FOR MARINE MICROBIOLOGY   (Germany)

^b UNIVERSITY OF BREMEN   (Germany)

^c MAX PLANCK INSTITUTE FOR BIOPHYSICAL CHEMISTRY   (Germany)

^d ALFRED WEGENER INSTITUTE FOR POLAR AND MARINE RESEARCH   (Germany)

^e BIELEFELD UNIVERSITY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

GENOMIC DNA; HYDROGEN; METHANE; TRANSCRIPTOME; CYTOCHROME; HEME; SULFATE;

ANOXIC CONDITIONS; CYTOCHROME; GENE EXPRESSION; GREENHOUSE GAS; HYDROGEN; MARINE SEDIMENT; METABOLISM; METHANE; METHANOTROPHY; OXIDATION; PROKARYOTE; SEAFLOOR; SULFATE; SULFATE-REDUCING BACTERIUM;

ANAEROBIC METABOLISM; ARCHAEAL GENOME; ARCHAEON; ARTICLE; BACTERIAL GENOME; BACTERIAL GROWTH; BACTERIUM CULTURE; BACTERIUM PILUS; CARBON FIXATION; CONTROLLED STUDY; ELECTRON TRANSPORT; ENERGY YIELD; ENRICHMENT CULTURE; ENZYME ACTIVE SITE; FLUORESCENCE IN SITU HYBRIDIZATION; GENE EXPRESSION; INTRACELLULAR SIGNALING; INTRACELLULAR TRANSPORT; METAGENOME; METHANOGENESIS; METHANOTROPHIC ARCHAEA; METHANOTROPHIC BACTERIUM; NONHUMAN; PRIORITY JOURNAL; STOICHIOMETRY; THERMOPHILIC ARCHAEON; THERMOPHILIC BACTERIUM; TRANSMISSION ELECTRON MICROSCOPY; ANAEROBIC GROWTH; BACTERIUM; FIMBRIA; HYDROTHERMAL VENT; METABOLISM; MICROBIOLOGY; MICROFLORA; MOLECULAR GENETICS; PHYSIOLOGY; SEA; SEDIMENT; SYMBIOSIS; TEMPERATURE;

BACTERIA (MICROORGANISMS); GEOBACTER;

ANAEROBIOSIS; ARCHAEA; BACTERIA; CYTOCHROMES; ELECTRON TRANSPORT; FIMBRIAE, BACTERIAL; GEOLOGIC SEDIMENTS; HEME; HYDROGEN; HYDROTHERMAL VENTS; METHANE; MICROBIOTA; MOLECULAR SEQUENCE DATA; OCEANS AND SEAS; SULFATES; SYMBIOSIS; TEMPERATURE;

EID: 84944755142     PISSN: 00280836     EISSN: 14764687     Source Type: Journal    
DOI: 10.1038/nature15733     Document Type: Article

References (55)

1. Reeburgh, W. S. Oceanic methane biogeochemistry. Chem. Rev. 107, 486-513 (2007).
2. Boetius, A.& Wenzhöfer, F. Seafloor oxygen consumption fuelled bymethane from cold seeps. Nat. Geosci. 6, 725-734 (2013).
3. Hinrichs, K.-U., Hayes, J. M., Sylva, S. P., Brewer, P. G. & DeLong, E. F. Methaneconsuming archaebacteria in marine sediments. Nature 398, 802-805 (1999).
4. Boetius, A. et al. A marine microbial consortium apparently mediating anaerobic oxidation of methane. Nature 407, 623-626 (2000).
5. Orphan, V. J. et al.Comparative analysis ofmethane-oxidizing archaea and sulfatereducing bacteria in anoxic marine sediments. Appl. Environ. Microbiol. 67, 1922-1934 (2001).
6. Holler, T. et al. Thermophilic anaerobic oxidation ofmethane by marine microbial consortia. ISME J. 5, 1946-1956 (2011).
7. Thauer, R. K. & Shima, S. Methane as fuel for anaerobic microorganisms. Ann. NY Acad. Sci. 1125, 158-170 (2008).
8. McGlynn, S. E., Chadwick, G. L., Kempes, C. P. & Orphan, V. J. Single cell activity reveals direct electron transfer in methanotrophic consortia. Nature http://dx.doi.org/10.1038/nature15512 (this issue).
9. Reguera, G. et al. Extracellular electron transfer via microbial nanowires. Nature 435, 1098-1101 (2005).
10. Summers, Z.M. et al. Direct exchange of electrons within aggregates of an evolved syntrophic coculture of anaerobic bacteria. Science 330, 1413-1415 (2010).
11. Knittel,K.A. Anaerobic oxidationofmethane: progresswithanunknown process. Annu. Rev. Microbiol. 63, 311-334 (2009).
12. Niemann, H. et al. Novel microbial communities of the Haakon Mosby mud volcano and their role as a methane sink. Nature 443, 854-858 (2006).
13. Schreiber, L., Holler, T., Knittel, K.,Meyerdierks, A. & Amann, R. Identification of the dominant sulfate-reducing bacterial partner of anaerobic methanotrophs of the ANME-2 clade. Environ. Microbiol. 12, 2327-2340 (2010).
14. Hoehler, T. M., Alperin, M. J., Albert, D. B. & Martens, C. S. Field and laboratory studies of methane oxidation in an anoxic marine sediment: evidence for a methanogen-sulfate reducer consortium. Glob. Biogeochem. Cycles 8, 451-463 (1994).
15. Krüger, M. et al. A conspicuous nickel protein in microbial mats that oxidize methane anaerobically. Nature 426, 878-881 (2003).
16. Hallam, S. J. et al. Reverse methanogenesis: testing the hypothesis with environmental genomics. Science 305, 1457-1462 (2004).
17. Meyerdierks, A. et al. Metagenome and mRNA expression analyses of anaerobic methanotrophic archaea of the ANME-1 group. Environ. Microbiol. 12, 422-439 (2010).
18. Kojima, H., Moll, J., Kahnt, J., Fukui, M. & Shima, S. A reversed genetic approach reveals the coenzyme specificity and other catalytic properties of three enzymes putatively involved in anaerobic oxidation of methane with sulfate. Environ. Microbiol. 16, 3431-3442 (2014).
19. Thauer, R. K.Anaerobic oxidationofmethanewith sulfate: onthe reversibility of the reactions that are catalyzed by enzymes also involved in methanogenesis from CO2. Curr. Opin. Microbiol. 14, 292-299 (2011).
20. Milucka, J., Widdel, F. & Shima, S. Immunological detection of enzymes for sulfate reduction in anaerobic methane-oxidizing consortia. Environ. Microbiol. 15, 1561-1571 (2013).
21. Milucka, J. et al. Zero-valent sulphur is a key intermediate in marine methane oxidation. Nature 491, 541-546 (2012).
22. Schink, B. Energetics of syntrophic cooperation in methanogenic degradation. Microbiol. Mol. Biol. Rev. 61, 262-280 (1997).
23. Stams, A. J. & Plugge, C. M. Electron transfer in syntrophic communities of anaerobic bacteria and archaea. Nature Rev. Microbiol. 7, 568-577 (2009).
24. Moran, J. J. et al. Methyl sulfides as intermediates in the anaerobic oxidation of methane. Environ. Microbiol. 10, 162-173 (2008).
25. Stokke, R., Roalkvam, I., Lanzen, A., Haflidason, H. & Steen, I. H. Integrated metagenomic andmetaproteomic analyses of an ANME-1-dominated community inmarine cold seep sediments. Environ. Microbiol. 14, 1333-1346 (2012).
26. Nagarajan, H. et al. Characterization and modelling of interspecies electron transfer mechanisms and microbial community dynamics of a syntrophic association. Nature Commun. 4, 2809 (2013).
27. Rotaru, A.-E. et al. A newmodel for electron flowduring anaerobic digestion: direct interspecies electron transfer toMethanosaeta for the reduction of carbon dioxide to methane. Energ. Environ. Sci. 7, 408-415 (2014).
28. Malvankar, N. S. et al. Structural basis for metallic-like conductivity in microbial nanowires. MBio 6, e00084-e00015 (2015).
29. Methé, B. A. et al. Genome of Geobacter sulfurreducens: metal reduction in subsurface environments. Science 302, 1967-1969 (2003).
30. Reitner, J. et al. Concretionarymethane-seep carbonates and associated microbial communities in Black Sea sediments. Palaeogeogr. Palaeoclimatol. Palaeoecol. 227, 18-30 (2005).
31. Widdel, F. & Bak, F. in The Prokaryotes Vol. 4 (eds Trüper, H. G., Balows, A., Dworkin, M., Harder, W. & Schleifer, K. H.) 3352-3378 (Springer, 1992).
32. Zhou, J.,Bruns,M.A.&Tiedje, J. M.DNArecovery fromsoils of diverse composition. Appl. Environ. Microbiol. 62, 316-322 (1996).
33. Muyzer, G., Teske, A., Wirsen, C. O. & Jannasch, H.W. Phylogenetic relationships of Thiomicrospira species and their identification in deep-sea hydrothermal vent Arch. Microbiol. 164, 165-172 (1995).
34. Massana, R., Murray, A., Preston, C. & DeLong, E. Vertical distribution and phylogenetic characterization of marine planktonic Archaea in the Santa Barbara Channel. Appl. Environ. Microbiol. 63, 50-56 (1997).
35. Teske, A. et al. Microbial diversity of hydrothermal sediments in the Guaymas Basin: evidence for anaerobic methanotrophic communities. Appl. Environ. Microbiol. 68, 1994-2007 (2002).
36. Ludwig, W. et al.ARB: a software environment for sequencedata.Nucleic Acids Res. 32, 1363-1371 (2004).
37. Pruesse, E. et al. SILVA: a comprehensive online resource for quality checked and aligned ribosomalRNAsequence data compatible withARB.Nucleic AcidsRes.35, 7188-7196 (2007).
38. Pernthaler, A., Pernthaler, J. & Amann, R. Fluorescence in situ hybridization and catalyzed reporter deposition for the identification of marine bacteria. Appl. Environ. Microbiol. 68, 3094-3101 (2002).
39. Steudel, R., Göbel, T. & Holdt, G. The molecular composition of hydrophilic sulfur sols prepared by decomposition of thiosulfate. Z. Naturforsch. B Chem. Sci. 43, 203-218 (1988).
40. Cord-Ruwisch, R. A quick method for the determination of dissolved and precipitated sulfides in cultures of sulfate-reducing bacteria. Microbiol. Meth. 4, 33-36 (1985).
41. Bankevich, A. et al. SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J. Comput. Biol. 19, 455-477 (2012).
42. Strous, M., Kraft, B., Bisdorf, R. & Tegetmeyer, H. E. The binning of metagenomic contigs for microbial physiology of mixed cultures. Front. Microbiol. 3, 410 (2012).
43. Seemann, T. Prokka: rapid prokaryotic genome annotation. Bioinformatics 30, 2068-2069 (2014).
44. Meyer, F. et al. GenDB-an open source genome annotation systemfor prokaryote genomes. Nucleic Acids Res. 31, 2187-2195 (2003).
45. Richter, M. et al. JCoast-a biologist-centric software tool for data mining and comparison of prokaryotic (meta) genomes. BMC Bioinformatics 9, 177 (2008).
46. Richter, M. & Rosselló-Móra, R. Shifting the genomic gold standard for the prokaryotic species definition. Proc. Natl Acad. Sci. USA 106, 19126-19131 (2009).
47. Eddy, S. HMMER User's Guide. Biological sequence analysis using profile hidden Markov models (Howard Hughes Medical Institute, 2003).
48. Finn, R. D., Miller, B. L., Clements, J. & Bateman, A. iPfam: a database of protein family and domain interactions found in the Protein Data Bank. Nucleic Acids Res. 42, D364-D373 (2014).
49. Haft, D. H., Selengut, J. D. & White, O. The TIGRFAMs database of protein families. Nucleic Acids Res. 31, 371-373 (2003).
50. Yu, N. Y. et al. PSORTb 3.0: improved protein subcellular localization prediction with refined localization subcategories and predictive capabilities for all prokaryotes. Bioinformatics 26, 1608-1615 (2010).
51. Li, B., Ruotti, V., Stewart, R. M., Thomson, J. A. & Dewey, C. N. RNA-Seq gene expression estimation with read mapping uncertainty. Bioinformatics 26, 493-500 (2010).
52. Fernandes, A. D. et al. Unifying the analysis of high-throughput sequencing datasets: characterizing RNA-seq, 16S rRNA gene sequencing and selective growth experiments by compositional data analysis. Microbiome 2, 1-13 (2014).
53. Liao, Y., Smyth, G. & Shi, W. featureCounts: an efficient general purpose program for assigning sequence reads to genomic features. Bioinformatics 30, 923-930 (2014).
54. Studer, D., Michel, M. & Mü ller, M. High pressure freezing comes of age. Scanning Microsc., Suppl. 3, 253-268 (1989).
55. Conrad, R. & Wetter, B. Influence of temperature on energetics of hydrogen metabolism in homoacetogenic, methanogenic, and other anaerobic bacteria. Arch. Microbiol. 155, 94-98 (1990).