Diversity and distribution of microbial long-chain fatty acid biosynthetic genes in the marine environment

Environmental Microbiology

Volumn 13, Issue 3, 2011, Pages 684-695

  Shulse, Christine N ^a   Allen, Eric E ^a,b  

^a UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^b UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARACHIDONIC ACID; DOCOSAHEXAENOIC ACID; FATTY ACID SYNTHASE; ICOSAPENTAENOIC ACID; OMEGA 3 FATTY ACID; POLYKETIDE SYNTHASE; UNSATURATED FATTY ACID;

ARTICLE; BACTERIUM; BIOSYNTHESIS; CHEMISTRY; CLASSIFICATION; ENVIRONMENT; ENZYMOLOGY; GENETIC VARIABILITY; GENETICS; METAGENOME; PHYLOGENY;

ARACHIDONIC ACID; BACTERIA; DOCOSAHEXAENOIC ACIDS; EICOSAPENTAENOIC ACID; ENVIRONMENT; FATTY ACID SYNTHETASE COMPLEX; FATTY ACIDS, OMEGA-3; FATTY ACIDS, UNSATURATED; GENETIC VARIATION; METAGENOME; PHYLOGENY; POLYKETIDE SYNTHASES;

BACTERIA (MICROORGANISMS);

EID: 79952077821     PISSN: 14622912     EISSN: 14622920     Source Type: Journal    
DOI: 10.1111/j.1462-2920.2010.02373.x     Document Type: Article

References (66)

1. Abascal, F., Zardoya, R., and Posada, D. (2005) ProtTest: selection of best-fit models of protein evolution. Bioinformatics 21: 2104-2105.
2. Allen, E.E., and Bartlett, D.H. (2002) Structure and regulation of the omega-3 polyunsaturated fatty acid synthase genes from the deep-sea bacterium Photobacterium profundum strain SS9. Microbiology 148: 1903-1913.
3. Allen, E.E., Facciotti, D., and Bartlett, D.H. (1999) Monounsaturated but not polyunsaturated fatty acids are required for growth of the deep-sea bacterium Photobacterium profundum SS9 at high pressure and low temperature. Appl Environ Microbiol 65: 1710-1720.
4. Alonso, C., Warnecke, F., Amann, R., and Pernthaler, J. (2007) High local and global diversity of Flavobacteria in marine plankton. Environ Microbiol 9: 1253-1266.
5. Auman, A.J., Breezee, J.L., Gosink, J.J., Kampfer, P., and Staley, J.T. (2006) Psychromonas ingrahamii sp. nov., a novel gas vacuolate, psychrophilic bacterium isolated from Arctic polar sea ice. Int J Syst Evol Microbiol 56: 1001-1007.
6. Beatty, J.T., Overmann, J., Lince, M.T., Manske, A.K., Lang, A.S., Blankenship, R.E., etal. (2005) An obligately photosynthetic bacterial anaerobe from a deep-sea hydrothermal vent. Proc Natl Acad Sci USA 102: 9306-9310.
7. Bowman, J.P., McCammon, S.A., Nichols, D.S., Skerratt, J.H., Rea, S.M., Nichols, P.D., and McMeekin, T.A. (1997) Shewanella gelidimarina sp. nov. and Shewanella frigidimarina sp. nov., novel Antarctic species with the ability to produce eicosapentaenoic acid (20:5ω3) and grow anaerobically by dissimilatory Fe(III) reduction. Int J Syst Bacteriol 47: 1040-1047.
8. Bowman, J.P., McCammon, S.A., Lewis, T., Skerratt, J.H., Brown, J.L., Nichols, D.S., and McMeekin, T.A. (1998) Psychroflexus torquis gen. nov., sp. nov., a psychrophilic species from Antarctic sea ice, and reclassification of Flavobacterium gondwanense (Dobson etal. 1993) as Psychroflexus gondwanense gen. nov., comb. nov. Microbiology 144: 1601-1609.
9. Bowman, J.P., McCammon, S.A., Gibson, J.A.E., Robertson, L., and Nichols, P.D. (2003) Prokaryotic metabolic activity and community structure in Antarctic continental shelf sediments. Appl Environ Microbiol 69: 2448-2462.
10. Burja, A.M., Radianingtyas, H., Windust, A., and Barrow, C.J. (2006) Isolation and characterization of polyunsaturated fatty acid producing Thraustochytrium species: screening of strains and optimization of omega-3 production. Appl Microbiol Biotechnol 72: 1161-1169.
11. Campbell, E.L., Cohen, M.F., and Meeks, J.C. (1997) A polyketide-synthase-like gene is involved in the synthesis of heterocyst glycolipids in Nostoc punctiforme strain ATCC 29133. Arch Microbiol 167: 251-258.
12. Clamp, M., Cuff, J., Searle, S.M., and Barton, G.J. (2004) The Jalview Java alignment editor. Bioinformatics 20: 426-427.
13. Cottrell, M.T., and Kirchman, D.L. (2000) Community composition of marine bacterioplankton determined by 16S rRNA gene clone libraries and fluorescence in situ hybridization. Appl Environ Microbiol 66: 5116-5122.
14. Davies, C., Heath, R.J., White, S.W., and Rock, C.O. (2000) The 1.8 angstrom crystal structure and active-site architecture of beta-ketoacyl-acyl carrier protein synthase III (FabH) from Escherichia coli. Structure 8: 185-195.
15. DeLong, E.F. (1986) Adaptations of deep-sea bacteria to the abyssal environment. PhD Thesis. San Diego, CA, USA: University of Calfornia.
16. DeLong, E.E. (2005) Microbial community genomics in the ocean. Nat Rev Microbiol 3: 459-469.
17. Delong, E.F., and Yayanos, A.A. (1986) Biochemical function and ecological significance of novel bacterial lipids in deep-sea procaryotes. Appl Environ Microbiol 51: 730-737.
18. DeLong, E.F., Preston, C.M., Mincer, T., Rich, V., Hallam, S.J., Frigaard, N.U., etal. (2006) Community genomics among stratified microbial assemblages in the ocean's interior. Science 311: 496-503.
19. Drummond, A., and Strimmer, K. (2001) PAL: an object-oriented programming library for molecular evolution and phylogenetics. Bioinformatics 17: 662-663.
20. Edgar, R.C. (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32: 1792-1797.
21. Eloe, E.A., Shulse, C.N., Fadrosh, D.W., Williamson, S.J., Allen, E.E., and Bartlett, D.H. (2010) Compositional differences in particle-associated and free-living microbial assemblages from an extreme deep ocean environment. Environ Microbiol Rep (in press).
22. Freese, E., Koster, J., and Rullkotter, J. (2008) Origin and composition of organic matter in tidal flat sediments from the German Wadden Sea. Org Geochem 39: 820-829.
23. Freese, E., Rutters, H., Koster, J., Rullkotter, J., and Sass, H. (2009) Gammaproteobacteria as a possible source of eicosapentaenoic acid in anoxic intertidal sediments. Microb Ecol 57: 444-454.
24. Garren, M., Raymundo, L., Guest, J., Harvell, C.D., and Azam, F. (2009) Resilience of coral-associated bacterial communities exposed to fish farm effluent. PLoS ONE 4: e7319.
25. Ginolhac, A., Jarrin, C., Robe, P., Perriere, G., Vogel, T., Simonet, P., and Nalin, R. (2005) Type I polyketide synthases may have evolved through horizontal gene transfer. J Mol Evol 60: 716-725.
26. Guindon, S., and Gascuel, O. (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52: 696-704.
27. Ha, E.M., Oh, C.T., Ryu, J.H., Bae, Y.S., Kang, S.W., Jang, I.H., etal. (2005) An antioxidant system required for host protection against gut infection in Drosophila. Dev Cell 8: 125-132.
28. Huang, J.Z., Jiang, X.Z., Zhang, X.W., Chen, W.H., Tian, B.Y., Shu, Z.Y., and Hu, S.N. (2008) Expressed sequence tag analysis of marine fungus Schizochytrium producing docosahexaenoic acid. J Biotechnol 138: 9-16.
29. Huber, T., Faulkner, G., and Hugenholtz, P. (2004) Bellerophon: a program to detect chimeric sequences in multiple sequence alignments. Bioinformatics 20: 2317-2319.
30. Kato, C., and Nogi, Y. (2001) Correlation between phylogenetic structure and function: examples from deep-sea Shewanella. FEMS Microbiol Ecol 35: 223-230.
31. Kawasaki, K., Nogi, Y., Hishinuma, M., Nodasaka, Y., Matsuyama, H., and Yumoto, I. (2002) Psychromonas marina sp. nov., a novel halophilic, facultatively psychrophilic bacterium isolated from the coast of the Okhotsk Sea. Int J Syst Evol Microbiol 52: 1455-1459.
32. Leonardo, M.R., Moser, D.P., Barbieri, E., Brantner, C.A., MacGregor, B.J., Paster, B.J., etal. (1999) Shewanella pealeana sp. nov., a member of the microbial community associated with the accessory nidamental gland of the squid Loligo pealei. Int J Syst Bacteriol 49: 1341-1351.
33. Letunic, I., and Bork, P. (2007) Interactive Tree Of Life (iTOL): an online tool for phylogenetic tree display and annotation. Bioinformatics 23: 127-128.
34. Lippmeier, J.C., Crawford, K.S., Owen, C.B., Rivas, A.A., Metz, J.G., and Apt, K.E. (2009) Characterization of both polyunsaturated fatty acid biosynthetic pathways in Schizochytrium sp. Lipids 44: 621-630.
35. Lopez-Garcia, P., Rodriguez-Valera, F., Pedros-Alio, C., and Moreira, D. (2001) Unexpected diversity of small eukaryotes in deep-sea Antarctic plankton. Nature 409: 603-607.
36. Manganelli, M., Malfatti, F., Samo, T.J., Mitchell, B.G., Wang, H., and Azam, F. (2009) Major role of microbes in carbon fluxes during austral winter in the Southern Drake Passage. PLoS ONE 4: e6941.
37. Martin-Cuadrado, A.B., Lopez-Garcia, P., Alba, J.C., Moreira, D., Monticelli, L., Strittmatter, A., etal. (2007) Metagenomics of the deep Mediterranean, a warm bathypelagic habitat. PLoS ONE 2: e914.
38. Metz, J.G., Roessler, P., Facciotti, D., Levering, C., Dittrich, F., Lassner, M., etal. (2001) Production of polyunsaturated fatty acids by polyketide synthases in both prokaryotes and eukaryotes. Science 293: 290-293.
39. Miller, M.A., Holder, M.T., Vos, R., Midford, P.E., Liebowitz, T., Chan, L., etal. (2009) The CIPRES Portals. CIPRES [WWW document]. URL
40. Miyanaga, A., Funa, N., Awakawa, T., and Horinouchi, S. (2008) Direct transfer of starter substrates from type I fatty acid synthase to type III polyketide synthases in phenolic lipid synthesis. Proc Natl Acad Sci USA 105: 871-876.
41. Muller-Navarra, D. (1995) Evidence that a highly unsaturated fatty acid limits Dapnhia growth in nature. Arch Hydrobiol 132: 297-307.
42. Muller-Navarra, D.C., Brett, M.T., Liston, A.M., and Goldman, C.R. (2000) A highly unsaturated fatty acid predicts carbon transfer between primary producers and consumers. Nature 403: 74-77.
43. Murry, M.A., and Wolk, C.P. (1989) Evidence that the barrier to the penetration of oxygen into heterocysts depends upon two layers of the cell envelope. Arch Microbiol 151: 469-474.
44. Neuwirth, E. (2007) RColorBrewer: ColorBrewer palettes. R package version 1.0-2.
45. Nichols, D.S. (2003) Prokaryotes and the input of polyunsaturated fatty acids to the marine food web. FEMS Microbiol Lett 219: 1-7.
46. Nichols, D.S., and McMeekin, T.A. (2002) Biomarker techniques to screen for bacteria that produce polyunsaturated fatty acids. J Microbiol Methods 48: 161-170.
47. Nishida, T., Orikasa, Y., Ito, Y., Yu, R., Yamada, A., Watanabe, K., and Okuyama, H. (2006) Escherichia coli engineered to produce eicosapentaenoic acid becomes resistant against oxidative damages. FEBS Lett 580: 2731-2735.
48. Olsen, J.G., Kadziola, A., von Wettstein-Knowles, P., Siggaard-Andersen, M., and Larsen, S. (2001) Structures of beta-ketoacyl-acyl carrier protein synthase I complexed with fatty acids elucidate its catalytic machinery. Structure 9: 233-243.
49. R Development Core Team (2009) R: A Language and Environment for Statistical Computing. Vienna, Austria: R Foundation for Statistical Computing, ISBN 3-900051-07-0 [WWW document]. URL
50. Raghukumar, S., and Raghukumar, C. (1999) Thraustochytrid fungoid protists in faecal pellets of the tunicate Pegea confoederata, their tolerance to deep-sea conditions and implication in degradation processes. Mar Ecol Prog Ser 190: 133-140.
51. Reusch, R.N., and Sadoff, H.L. (1983) Novel lipid components of the Azotobacter vinelandii cyst membrane. Nature 302: 268-270.
52. Riley, M., Staley, J.T., Danchin, A., Wang, T.Z., Brettin, T.S., Hauser, L.J., etal. (2008) Genomics of an extreme psychrophile, Psychromonas ingrahamii. BMC Genomics 9: 210.
53. Rusch, D.B., Halpern, A.L., Sutton, G., Heidelberg, K.B., Williamson, S., Yooseph, S., etal. (2007) The Sorcerer II Global Ocean Sampling expedition: Northwest Atlantic through Eastern Tropical Pacific. PLoS Biol 5: 398-431.
54. Russell, N., and Nichols, D. (1999) Polyunsaturated fatty acids in marine bacteria - a dogma rewritten. Microbiology 145: 767-779.
55. Sato, S., Kurihara, T., Kawamoto, J., Hosokawa, M., Sato, S.B., and Esaki, N. (2008) Cold adaptation of eicosapentaenoic acid-less mutant of Shewanella livingstonensis Ac10 involving uptake and remodeling of synthetic phospholipids containing various polyunsaturated fatty acids. Extremophiles 12: 753-761.
56. Schloss, P.D., Westcott, S.L., Ryabin, T., Hall, J.R., Hartmann, M., Hollister, E.B., etal. (2009) Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 75: 7537-7541.
57. Schweizer, E., and Hofmann, J. (2004) Microbial type I fatty acid synthases (FAS): major players in a network of cellular FAS systems. Microbiol Mol Biol Rev 68: 501-517.
58. Stamatakis, A., Hoover, P., and Rougemont, J. (2008) A rapid bootstrap algorithm for the RAxML web servers. Syst Biol 57: 758-771.
59. Sugihara, S., Hori, R., Nakanowatari, H., Takada, Y., Yumoto, I., Morita, N., etal. (2010) Possible biosynthetic pathways for all cis-3, 6, 9, 12, 15, 19, 22, 25, 28-hentriacontanonaene in bacteria. Lipids 45: 167-177.
60. Sukovich, D.J., Seffernick, J.L., Richman, J.E., Hunt, K.A., Gralnick, J.A., and Wackett, L.P. (2010a) Structure, function, and insights into the biosynthesis of a head-to-head hydrocarbon in Shewanella oneidensis strain MR-1. Appl Environ Microbiol 76: 3842-3849.
61. Sukovich, D.J., Seffernick, J.L., Richman, J.E., Gralnick, J.A., and Wackett, L.P. (2010b) Widespread head-to-head hydrocarbon biosynthesis in bacteria and role of OleA. Appl Environ Microbiol 76: 3850-3862.
62. Tringe, S.G., von Mering, C., Kobayashi, A., Salamov, A.A., Chen, K., Chang, H.W., etal. (2005) Comparative metagenomics of microbial communities. Science 308: 554-557.
63. Venter, J.C., Remington, K., Heidelberg, J.F., Halpern, A.L., Rusch, D., Eisen, J.A., etal. (2004) Environmental genome shotgun sequencing of the Sargasso Sea. Science 304: 66-74.
64. Wang, F., Xiao, X., Ou, H.Y., Gai, Y.B., and Wang, F.P. (2009) Role and regulation of fatty acid biosynthesis in the response of Shewanella piezotolerans WP3 to different temperatures and pressures. J Bacteriol 191: 2574-2584.
65. Warnes, G.R. Includes R source code and/or documentation contributed by (in alphabetical order): Ben Bolker, Lodewijk Bonebakker, Robert Gentleman, Wolfgang Huber Andy Liaw, Thomas Lumley, Martin Maechler, Arni Magnusson, Steffen Moeller, Marc Schwartz and Bill Venables. (2009) gplots: Various R programming tools for plotting data. R package version 2.7.4 [WWW document]. URL
66. White, S.W., Zheng, J., Zhang, Y.M., and Rock, C.O. (2005) The structural biology of type II fatty acid biosynthesis. Annu Rev Biochem 74: 791-831.