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Substrate-specific clades of active marine methylotrophs associated with a phytoplankton bloom in a temperate coastal environment
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Neufeld, Josh D. , Boden, Rich, Moussard, Hélène, Schäfer, Hendrik and Murrell, J. C. (J. Colin). (2008) Substrate-specific clades of active marine methylotrophs associated with a phytoplankton bloom in a temperate coastal environment. Applied and Environmental Microbiology, Vol.74 (No.23). pp. 7321-7328. ISSN 0099-2240
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Official URL: http://dx.doi.org/10.1128/AEM.01266-08
Abstract
Marine microorganisms that consume one-carbon (C1) compounds are poorly described, despite their impact on global climate via an influence on aquatic and atmospheric chemistry. This study investigated marine bacterial communities involved in the metabolism of C1 compounds. These communities were of relevance to surface seawater and atmospheric chemistry in the context of a bloom that was dominated by phytoplankton known to produce dimethylsulfoniopropionate. In addition to using 16S rRNA gene fingerprinting and clone libraries to characterize samples taken from a bloom transect in July 2006, seawater samples from the phytoplankton bloom were incubated with 13C-labeled methanol, monomethylamine, dimethylamine, methyl bromide, and dimethyl sulfide to identify microbial populations involved in the turnover of C1 compounds, using DNA stable isotope probing. The [13C]DNA samples from a single time point were characterized and compared using denaturing gradient gel electrophoresis (DGGE), fingerprint cluster analysis, and 16S rRNA gene clone library analysis. Bacterial community DGGE fingerprints from 13C-labeled DNA were distinct from those obtained with the DNA of the nonlabeled community DNA and suggested some overlap in substrate utilization between active methylotroph populations growing on different C1 substrates. Active methylotrophs were affiliated with Methylophaga spp. and several clades of undescribed Gammaproteobacteria that utilized methanol, methylamines (both monomethylamine and dimethylamine), and dimethyl sulfide. rRNA gene sequences corresponding to populations assimilating 13C-labeled methyl bromide and other substrates were associated with members of the Alphaproteobacteria (e.g., the family Rhodobacteraceae), the Cytophaga-Flexibacter-Bacteroides group, and unknown taxa. This study expands the known diversity of marine methylotrophs in surface seawater and provides a comprehensive data set for focused cultivation and metagenomic analyses in the future.
| Item Type: | Journal Article |
|---|---|
| Subjects: | Q Science > QR Microbiology |
| Divisions: | Faculty of Science > Life Sciences (2010- ) > Warwick HRI (2004-2010) |
| Library of Congress Subject Headings (LCSH): | Methylotrophic microorganisms, Marine phytoplankton |
| Journal or Publication Title: | Applied and Environmental Microbiology |
| Publisher: | American Society for Microbiology |
| ISSN: | 0099-2240 |
| Date: | 10 October 2008 |
| Volume: | Vol.74 |
| Number: | No.23 |
| Page Range: | pp. 7321-7328 |
| Identification Number: | 10.1128/AEM.01266-08 |
| Status: | Peer Reviewed |
| Access rights to Published version: | Open Access |
| Funder: | Natural Environment Research Council (Great Britain) (NERC), Natural Sciences and Engineering Research Council of Canada (NSERC) |
| Grant number: | NE/C001 923/1 (NRC), NE/B501404/1 (NERC) |
| References: | 1. Abbattista Gentile, I., L. Ferraris, M. Sanguinetti, M. Tiprigan, and G. Fisichella. 1992. Methyl bromide in fresh waters: hydrolysis and volatilisation. Pesticide Science 34:297-301. 2. Anbar, A. D., Y. L. Yung, and F. R. Chavez. 1996. Methyl bromide: Ocean sources, ocean sinks, and climate sensitivity. Global Biogeochem. Cycles 10:175-190. 3. Ashelford, K. E., N. A. Chuzhanova, J. C. Fry, A. J. Jones, and A. J. Weightman. 2005. At least 1 in 20 16S rRNA sequence records currently held in public repositories is estimated to contain substantial anomalies. Appl. Environ. Microbiol. 71:7724-7736. 4. Bakera, J. M., C. E. Reeves, P. D. Nightingale, S. A. Penkett, S. W. Gibb, and A. D. Hatton. 1999. Biological production of methyl bromide in the coastal waters of the North Sea and open ocean of the northeast Atlantic. Mar. Chem. 64:267-285. 5. Beerli, R., and H.-J. Borschberg. 1991. Preparation of [13C2]-DMSO. J. Label. Comp. Radiopharm. 29:957-961. 6. Benson, D. A., I. Karsch-Mizrachi, D. J. Lipman, J. Ostell, B. A. Rapp, and D. L. Wheeler. 2000. Genbank. Nucleic Acids Res. 28:15-18. 7. Carpenter, L. J., A. C. Lewis, J. R. Hopkins, K. A. Read, I. D. Longley, and M. W. Gallagher. 2004. Uptake of methanol to the North Atlantic Ocean surface. Global Biogeochem. Cycles 18:GB4027. 8. de Zwart, J., P. Nelisse, and J. Kuenen. 1996. Isolation and characterization of Methylophaga sulfidovorans sp. nov.: an obligately methylotrophic, aerobic, dimethylsulfide oxidizing bacterium from a microbial mat. FEMS Microbiol. Ecol. 20:261-270. 9. Felsenstein, J. 1985. Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783-791. 10. Galbally, I. E., and W. Kirstine. 2002. The production of methanol by flowering plants and the global cycle of methanol. J. Atmos. Chem. 43:195-229. 11. Gibb, S., and A. Hatton. 2004. The occurrence and distribution of trimethylamine-N455 oxide in Antarctic coastal waters. Mar. Chem. 91:65-75. 12. Goodwin, K. D., R. K. Varner, P. M. Crill, and R. S. Oremland. 2001. Consumption of tropospheric levels of methyl bromide by C1 compound-utilizing bacteria and comparison to saturation kinetics. Appl. Environ. Microbiol. 67:5437-5443. 13. Heikes, B. G., W. Chang, M. E. Q. Pilson, E. Swift, H. B. Singh, A. Guenther, D. J. Jacob, B. D. Field, R. Fall, D. Riemer, and L. Brand. 2002. Atmospheric methanol budget and ocean implication. Global Biogeochem. Cycles 16:80-81. 14. Heyer, J., Y. Malashenko, U. Berger, and E. Budkova. 1984. Verbreitung methanotropher Bakterien. Z. Allg. Mikrobiol. 24:725–744. 15. Holmes, A. J., N. J. P. Owens, and J. C. Murrell. 1995. Detection of novel marine methanotrophs using phylogenetic and functional gene probes after methane enrichment. Microbiol. 141:1947-1955. 16. Holmes, A. J., N. J. P. Owens, and J. C. Murrell. 1996. Molecular analysis of enrichment cultures of marine methane oxidising bacteria. J. Exp. Mar. Biol. Ecol. 203:27-38. 17. Janvier, M., C. Frehel, F. Grimont, and F. Gasser. 1985. Methylophaga marina gen. nov., sp. nov. and Methylophaga thalassica sp. nov., marine methylotrophs. Int. J. Syst. Bacteriol. 35:131–139 18. Kalyuzhnaya, M. G., O. Nercessian, A. Lapidus, and L. Chistoserdova. 2005. Fishing for biodiversity: novel methanopterin-linked C1 transfer genes deduced from the Sargasso Sea metagenome. E 475 nviron. Microbiol. 7:1909-1916. 19. Kiene, R. P. 1990. Dimethyl sulfide production from dimethylsulfoniopropionate in coastal seawater samples and bacterial cultures. Appl. Environ. Microbiol. 56:3292-3297. 20. Kiene, R. P. 1992. Dynamics of dimethyl sulfide and dimethylsulfoniopropionate in oceanic water samples. Mar. Chem. 37:29-52. 21. Kiene, R. P. 1993. Microbial sources and sinks for methylated sulfur compounds in the marine environment, p. 15-33. In D. P. Kelley and J. C. Murrell (ed.), Microbial Growth on C1 Compounds. Intercept Ltd., London. 22. Kim, S. K., F. Rassoulzadegan, B. Krajka, B. C. Nguyen, N. Mihalopoulos, and P. Buat-Menard. 1990. Production of dimethylsulfonium propionate (DMSP) and dimethylsulfide (DMS) by a microbial food web. Limnol. Oceanog. 35:1810-1821. 23. Kimura, T., I. Sugahara, and K. Hayashi. 1990. Use of short-chain amines and amino acids as sole sources of nitrogen in a marine methylotrophic bacterium, Methylophaga sp. AA-30. Agric. Biol. Chem. 54:1873-1874. 24. Kwint, R. L. J., and K. J. M. Kramer. 1995. Dimethylsulphide production by plankton communities. Mar. Ecol. Prog. Ser. 121:227-237. 25. Lane, D. J. 1991. 16S/23S rRNA sequencing., p. 115-175. In E. Stackebrandt and M. Goodfellow (ed.), Nucleic acid techniques in bacterial systematics. John Wiley & Sons, Inc., Chichester, UK. 26. Levasseur, M., S. Michaud, J. Egge, G. Cantin, J. C. Nejstgaard, R. Sanders, E. Fernandez, P. T. Solberg, B. Heimdal, and M. Gosselin. 1996. Production of DMSP 23 and DMS during a mesocosm study of an Emiliania huxleyi bloom: influence of bacteria and Calanus finmarchicus grazing. Mar. Biol. 126:609-618. 27. Lidstrom, M. E. 1988. Isolation and characterization of marine methanotrophs. Antonie van Leeuwenhoek 54:189-199. 28. Liss, P., G. Malin, and S. Turner. 1992. Production of DMS by marine phytoplankton, p. 1-14. In G. Restelli and G. Angeletti (ed.), Dimethylsulphide: oceans, atmosphere and climate. Kluwer Academic Publishing, Dordrecht. 29. Ludwig, W., O. Strunk, R. Westram, L. Richter, H. Meier, Yadhukumar, A. Buchner, T. Lai, S. Steppi, G. Jobb, W. Forster, I. Brettske, S. Gerber, A. W. Ginhart, O. Gross, S. Grumann, S. Hermann, R. Jost, A. Konig, T. Liss, R. Lussmann, M. May, B. Nonhoff, B. Reichel, R. Strehlow, A. Stamatakis, N. Stuckmann, A. Vilbig, M. Lenke, T. Ludwig, A. Bode, and K.-H. Schleifer. 2004. ARB: a software environment for sequence data. Nucl. Acids Res. 32:1363-1371. 30. McDonald, I. R., K. L. Warner, C. McAnulla, C. A. Woodall, R. S. Oremland, and J. C. Murrell. 2002. A review of bacterial methyl halide degradation: biochemistry, genetics and molecular ecology. Environmental Microbiology 4:193-203. 31. Muyzer, G., E. C. de Waal, and A. G. Uitterlinden. 1993. Profiling of complex microbial populations by denaturing gradient gel electrophoresis analysis of polymerase chain reaction-amplified genes coding for 16S rRNA. Appl. Environ. Microbiol. 59:695- 700. 32. Naqvi, S. W. A., H. W. Bange, S. W. Gibb, C. Goyet, A. D. Hatton, and R. C. Upstill- Goddard. 2005. Biogeochemical ocean-atmosphere transfers in the Arabian Sea. Prog. Oceanogr. 65:116. 33. Neufeld, J. D., Y. Chen, M. G. Dumont, and J. C. Murrell. 2008. Marine methylotrophs revealed by stable-isotope probing, multiple displacement amplification and metagenomics. Environ. Microbiol. 10:1526-1535. 34. Neufeld, J. D., M. G. Dumont, J. Vohra, and J. C. Murrell. 2007. Methodological considerations for the use of stable isotope probing in microbial ecology. Microb. Ecol. 53:435-442. 35. Neufeld, J. D., H. Schäfer, M. J. Cox, R. Boden, I. R. McDonald, and J. C. Murrell. 2007. Stable-isotope probing implicates Methylophaga spp. and novel Gammaproteobacteria in marine methanol and methylamine metabolism. ISME J. 1:480- 491. 36. Neufeld, J. D., J. Vohra, M. G. Dumont, T. Lueders, M. Manefield, M. W. Friedrich, and J. C. Murrell. 2007. DNA stable-isotope probing. Nat. Protocols 2:860-866. 37. Neufeld, J. D., Z. Yu, W. Lam, and W. W. Mohn. 2004. Serial analysis of ribosomal sequence tags (SARST): a high-throughput method for profiling complex microbial communities. Environ. Microbiol. 6:131-144. 38. Oremland, R. S. 1979. Methanogenic activity in plankton samples and fish intestines: a mechanism for in situ methanogenesis in oceanic subsurface waters. Limnol. Oceanogr. 24:1136-1141. 39. Radajewski, S., P. Ineson, N. R. Parekh, and J. C. Murrell. 2000. Stable-isotope probing as a tool in microbial ecology. Nature 403:646-649. 40. Rusch, D. B., A. L. Halpern, G. Sutton, K. B. Heidelberg, S. Williamson, S. Yooseph, D. Wu, J. A. Eisen, J. M. Hoffman, K. Remington, K. Beeson, B. Tran, H. Smith, H. Baden-Tillson, C. Stewart, J. Thorpe, J. Freeman, C. Andrews-Pfannkoch, J. E. Venter, K. Li, S. Kravitz, J. F. Heidelberg, T. Utterback, Y.-H. Rogers, L. I. Falcón, V. Souza, G. Bonilla-Rosso, L. E. Eguiarte, D. M. Karl, S. Sathyendranath, T. Platt, E. Bermingham, V. Gallardo, G. Tamayo-Castillo, M. R. Ferrari, R. L. Strausberg, K. Nealson, R. Friedman, M. Frazier, and J. C. Venter. 545 2007. The Sorcerer II global ocean sampling expedition: Northwest Atlantic through Eastern Tropical Pacific. PLoS Biol. 5:e77. 41. Sæmundsdóttir, S., and P. A. Matrai. 1998. Biological production of methyl bromide by cultures of marine phytoplankton. Limnol. Oceanogr. 43:81-87. 42. Schaefer, J. K., K. D. Goodwin, I. R. McDonald, J. C. Murrell, and R. S. Oremland. 2002. Leisingera methylohalidivorans gen. nov., sp. nov., a marine methylotroph that grows on methyl bromide. Int. J. Syst. Evol. Microbiol. 52:851-859. 43. Schäfer, H. 2007. Isolation of Methylophaga spp. from marine dimethylsulfidedegrading enrichment cultures and identification of polypeptides induced during growth on dimethylsulfide. Appl. Environ. Microbiol. 73:2580-2591. 44. Schäfer, H., I. R. McDonald, P. D. Nightingale, and J. C. Murrell. 2005. Evidence for the presence of a CmuA methyltransferase pathway in novel marine methyl halideoxidizing bacteria. Environ. Microbiol. 7:839-852. 45. Schäfer, H., L. Miller, R. Oremland, and J. C. Murrell. 2007. Bacterial cycling of methyl halides, p. 307-346. In A. I. Laskin, S. Sariaslani, and G. Gadd (ed.), Adv. Appl. Microbiol., vol. 61. 46. Sieburth, J. N., P. W. Johnson, M. A. Eberhardt, M. E. Sieracki, M. Lidstrom, and D. Laux. 1987. The first methane-oxidizing bacterium from the upper mixing layer of the deep ocean: Methylomonas pelagica sp. nov. Curr. Microbiol. 14:285-293. 47. Singh, H. B., A. Tabazadeh, M. J. Evans, B 565 . D. Field, D. J. Jacob, G. Sachse, J. H. Crawford, R. Shetter, and W. H. Brune. 2003. Oxygenated volatile organic chemicals in the oceans: inferences and implications based on atmospheric observations and air-sea exchange models. Geophys. Res. Lett. 30:1862. 48. Tamura, K., J. Dudley, M. Nei, and S. Kumar. 2007. MEGA4: Molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol. Biol. Evol. 24:1596. 49. Tamura, K., M. Nei, and S. Kumar. 2004. Prospects for inferring very large phylogenies by using the neighbor-joining method. Proc. Natl. Acad. Sci. U. S. A. 101:11030-11035. 50. Venter, J. C., K. Remington, J. F. Heidelberg, A. L. Halpern, D. Rusch, J. A. Eisen, D. Wu, I. Paulsen, K. E. Nelson, W. Nelson, D. E. Fouts, S. Levy, A. H. Knap, M. W. Lomas, K. Nealson, O. White, J. Peterson, J. Hoffman, R. Parsons, H. Baden- Tillson, C. Pfannkoch, Y.-H. Rogers, and H. O. Smith. 2004. Environmental genome shotgun sequencing of the Sargasso Sea. Science 304:66-74. 51. Vila-Costa, M., D. A. del Valle, J. M. Gonzalez, D. Slezak, R. P. Kiene, O. Sanchez, and R. Simo. 2006. Phylogenetic identification and metabolism of marine dimethylsulfide-consuming bacteria. Environ. Microbiol. 8:2189-2200. 52. Wang, Q., G. M. Garrity, J. M. Tiedje, and J. R. Cole. 2007. Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl. Environ. Microbiol. 73:5261-5267. 53. Williams, J., R. Holzinger, V. Gros, X. Xu, E. Atlas, and D. W. R. Wallace. 2004. Measurements of organic species in air and seawater from the tropical Atlantic. Geophys. Res. Lett. 31:L23S06. |
| URI: | http://wrap.warwick.ac.uk/id/eprint/359 |
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