Information de reference pour ce titreAccession Number: | 00006056-201510220-00047.
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Author: | McGlynn, Shawn E. 1; Chadwick, Grayson L. 1; Kempes, Christopher P. 2,3,4; Orphan, Victoria J. 1
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Institution: | (1)Division of Geological and Planetary Sciences, California Institute of Technology, Pasadena, California 91125, USA (2)Exobiology Branch, National Aeronautics and Space Administration Ames Research Center, Moffett Field, California 94035, USA (3)Control and Dynamical Systems, California Institute of Technology, Pasadena, California 91125, USA (4)SETI Institute, Mountain View, California 94034, USA
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Title: | Single cell activity reveals direct electron transfer in methanotrophic consortia.[Article]
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Source: | Nature. 526(7574):531-535, October 22, 2015.
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Abstract: | : Multicellular assemblages of microorganisms are ubiquitous in nature, and the proximity afforded by aggregation is thought to permit intercellular metabolic coupling that can accommodate otherwise unfavourable reactions. Consortia of methane-oxidizing archaea and sulphate-reducing bacteria are a well-known environmental example of microbial co-aggregation; however, the coupling mechanisms between these paired organisms is not well understood, despite the attention given them because of the global significance of anaerobic methane oxidation. Here we examined the influence of interspecies spatial positioning as it relates to biosynthetic activity within structurally diverse uncultured methane-oxidizing consortia by measuring stable isotope incorporation for individual archaeal and bacterial cells to constrain their potential metabolic interactions. In contrast to conventional models of syntrophy based on the passage of molecular intermediates, cellular activities were found to be independent of both species intermixing and distance between syntrophic partners within consortia. A generalized model of electric conductivity between co-associated archaea and bacteria best fit the empirical data. Combined with the detection of large multi-haem cytochromes in the genomes of methanotrophic archaea and the demonstration of redox-dependent staining of the matrix between cells in consortia, these results provide evidence for syntrophic coupling through direct electron transfer.
(C) 2015 Nature Publishing Group
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References: | 1. Tolker-Nielsen, T. & Molin, S. Spatial organization of microbial biofilm communities. Microb. Ecol. 40, 75-84 (2000)
2. Rickard, A. H., Gilbert, P., High, N. J., Kolenbrander, P. E. & Handley, P. S. Bacterial coaggregation: an integral process in the development of multi-species biofilms. Trends Microbiol. 11, 94-100 (2003)
3. Battin, T. J. et al. Microbial landscapes: new paths to biofilm research. Nature Rev. Microbiol. 5, 76-81 (2007)
4. Kim, H. J., Boedicker, J. Q., Choi, J. W. & Ismagilov, R. F. Defined spatial structure stabilizes a synthetic multispecies bacterial community. Proc. Natl Acad. Sci. USA 105, 18188-18193 (2008)
5. Wintermute, E. H. & Silver, P. A. Dynamics in the mixed microbial concourse. Genes Dev. 24, 2603-2614 (2010)
6. Wessel, A. K., Hmelo, L., Parsek, M. R. & Whiteley, M. Going local: technologies for exploring bacterial microenvironments. Nature Rev. Microbiol. 11, 337-348 (2013)
7. Momeni, B., Brileya, K. A., Fields, M. W. & Shou, W. Strong inter-population cooperation leads to partner intermixing in microbial communities. eLife 2, e00230 (2013)
8. Kempes, C. P., Okegbe, C., Mears-Clarke, Z., Follows, M. J. & Dietrich, L. E. P. Morphological optimization for access to dual oxidants in biofilms. Proc. Natl Acad. Sci. USA 111, 208-213 (2014)
9. Nielsen, A. T., Tolker-Nielsen, T., Barken, K. B. & Molin, S. Role of commensal relationships on the spatial structure of a surface-attached microbial consortium. Environ. Microbiol. 2, 59-68 (2000)
10. Boetius, A. et al. A marine microbial consortium apparently mediating anaerobic oxidation of methane. Nature 407, 623-626 (2000)
11. Orphan, V. J., House, C. H., Hinrichs, K. U., McKeegan, K. D. & DeLong, E. F. Methane-consuming archaea revealed by directly coupled isotopic and phylogenetic analysis. Science 293, 484-487 (2001)
12. Orcutt, B. & Meile, C. Constraints on mechanisms and rates of anaerobic oxidation of methane by microbial consortia: process-based modeling of ANME-2 archaea and sulfate reducing bacteria interactions. Biogeosciences 5, 1587-1599 (2008)
13. Alperin, M. J. & Hoehler, T. M. Anaerobic methane oxidation by archaea/sulfate-reducing bacteria aggregates: 1. thermodynamic and physical constraints. Am. J. Sci. 309, 869-957 (2009)
14. Orphan, V. J., House, C. H., Hinrichs, K.-U., McKeegan, K. D. & DeLong, E. F. Multiple archaeal groups mediate methane oxidation in anoxic cold seep sediments. Proc. Natl Acad. Sci. USA 99, 7663-7668 (2002)
15. Knittel, K., Losekann, T., Boetius, A., Kort, R. & Amann, R. Diversity and distribution of methanotrophic archaea at cold seeps. Appl. Environ. Microbiol. 71, 467-479 (2005)
16. Orphan, V. J., Turk, K. A., Green, A. M. & House, C. H. Patterns of 15N assimilation and growth of methanotrophic ANME-2 archaea and sulfate-reducing bacteria within structured syntrophic consortia revealed by FISH-SIMS. Environ. Microbiol. 11, 1777-1791 (2009)
17. Nauhaus, K., Boetius, A., Kruger, M. & Widdel, F. In vitro demonstration of anaerobic oxidation of methane coupled to sulphate reduction in sediment from a marine gas hydrate area. Environ. Microbiol. 4, 296-305 (2002)
18. Thauer, R. K. Anaerobic oxidation of methane with sulfate: on the reversibility of the reactions that are catalyzed by enzymes also involved in methanogenesis from CO2. Curr. Opin. Microbiol. 14, 292-299 (2011)
19. Moran, J. J. et al. Methyl sulfides as intermediates in the anaerobic oxidation of methane. Environ. Microbiol. 10, 162-173 (2008)
20. Milucka, J. et al. Zero-valent sulphur is a key intermediate in marine methane oxidation. Nature 491, 541-546 (2012)
21. Dolfing, J. The energetic consequences of hydrogen gradients in methanogenic ecosystems. FEMS Microbiol. Ecol. 101, 183-187 (1992)
22. Schink, P. B. & Stams, A. J. M. in The Prokaryotes (eds Rosenberg, E., DeLong, E. F., Lory, S., Stackebrandt, E. & Thompson, F.) 471-493 (Springer, 2013)
23. 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)
24. Kruger, M., Wolters, H., Gehre, M., Joye, S. B. & Richnow, H.-H. Tracing the slow growth of anaerobic methane-oxidizing communities by (15)N-labelling techniques. FEMS Microbiol. Ecol. 63, 401-411 (2008)
25. 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)
26. Lovley, D. R. Electromicrobiology. Annu. Rev. Microbiol. 66, 391-409 (2012)
27. Michelusi, N., Pirbadian, S., El-Naggar, M. Y. & Mitra, U. A stochastic model for electron transfer in bacterial cables. IEEE J. Sel. Areas Comm. 32, 2402-2416 (2014)
28. Meysman, F. J. R., Risgaard-Petersen, N., Malkin, S. Y. & Nielsen, L. P. The geochemical fingerprint of microbial long-distance electron transport in the seafloor. Geochim. Cosmochim. Acta 152, 122-142 (2015)
29. Meyerdierks, A. et al. Metagenome and mRNA expression analyses of anaerobic methanotrophic archaea of the ANME-1 group. Environ. Microbiol. 12, 422-439 (2010)
30. Wang, F.-P. et al. Methanotrophic archaea possessing diverging methane-oxidizing and electron-transporting pathways. ISME J. 8, 1069-1078 (2014)
31. Haroon, M. F. et al. Anaerobic oxidation of methane coupled to nitrate reduction in a novel archaeal lineage. Nature 500, 567-570 (2013)
32. Strycharz-Glaven, S. M., Snider, R. M., Guiseppi-Elie, A. & Tender, L. M. On the electrical conductivity of microbial nanowires and biofilms. Energy Environ. Sci. 4, 4366-4379 (2011)
33. Richardson, D. J. et al. The 'porin-cytochrome' model for microbe-to-mineral electron transfer. Mol. Microbiol. 85, 201-212 (2012)
34. Okamoto, A., Hashimoto, K. & Nakamura, R. Long-range electron conduction of Shewanella biofilms mediated by outer membrane C-type cytochromes. Bioelectrochemistry 85, 61-65 (2012)
35. Graham, R. C. & Karnovsky, M. J. The early stages of absorption of injected horseradish peroxidase in the proximal tubules of mouse kidney: ultrastructural cytochemistry by a new technique. J. Histochem. Cytochem. 14, 291-302 (1966)
36. Litwin, J. A. Transition metal-catalysed oxidation of 3,3'-diaminobenzidine [DAB] in a model system. Acta Histochem. 71, 111-117 (1982)
37. Welte, C. & Deppenmeier, U. Bioenergetics and anaerobic respiratory chains of aceticlastic methanogens. Biochim. Biophys. Acta 1837, 1130-1147 (2014)
38. Summers, Z. M. et al. Direct exchange of electrons within aggregates of an evolved syntrophic coculture of anaerobic bacteria. Science 330, 1413-1415 (2010)
39. Rotaru, A.-E. et al. Direct interspecies electron transfer between Geobacter metallireducens and Methanosarcina barkeri. Appl. Environ. Microbiol. 80, 4599-4605 (2014)
40. Beal, E. J., House, C. H. & Orphan, V. J. Manganese- and iron-dependent marine methane oxidation. Science 325, 184-187 (2009)
41. Kletzin, A. et al. Cytochromes c in Archaea: distribution, maturation, cell architecture and the special case of Ignicoccus hospitalis. Front. Microbiol. 6, 439 (2015)
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Language: | English.
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Document Type: | ARTICLE.
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Journal Subset: | Life & Biomedical Sciences. Science.
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ISSN: | 0028-0836
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NLM Journal Code: | 0410462, nsc
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DOI Number: | https://dx.doi.org/10.1038/natur...- ouverture dans une nouvelle fenêtre
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