Bacterial dimethylsulfoniopropionate degradation genes in the oligotrophic North Pacific subtropical gyre

Applied and Environmental Microbiology

Volumn 78, Issue 8, 2012, Pages 2775-2782

  Varaljay, Vanessa A ^a   Gifford, Scott M ^a,c   Wilson, Samuel T ^b   Sharma, Shalabh ^a   Karl, David M ^b   Moran, Mary Ann ^a  

^a UNIVERSITY OF GEORGIA   (United States)

^b UNIVERSITY OF HAWAII   (United States)

^c USA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIOPLANKTONS; DATA SETS; DEEP CHLOROPHYLL MAXIMUMS; DEMETHYLATION; DIMETHYLSULFIDE; DIMETHYLSULFONIOPROPIONATE; ENVIRONMENTAL VARIABLES; GENE POOLS; GENES ENCODING; MARINE BACTERIUM; NORTH PACIFIC; ORGANIC SULFUR COMPOUNDS; PHOTOSYNTHETICALLY ACTIVE RADIATION; PRIMARY PRODUCTION; SUBTROPICAL GYRE;

CHLOROPHYLL; DEGRADATION; SULFUR COMPOUNDS; TUNGSTEN;

GENE EXPRESSION;

DEHYDRODOLICHYL DIPHOSPHATE SYNTHETASE; DIMETHYLPROPIOTHETIN; SEA WATER; SULFONIUM DERIVATIVE; TRANSFERASE;

ABUNDANCE; BACTERIOPLANKTON; BACTERIUM; BIODEGRADATION; DIMETHYLSULFIDE; GENE EXPRESSION; GYRE; MARINE ECOSYSTEM; METABOLISM; MICROBIAL COMMUNITY; OLIGOTROPHIC ENVIRONMENT; PHOTOSYNTHETICALLY ACTIVE RADIATION; SPECIES DIVERSITY; SULFUR COMPOUND;

ARTICLE; BACTERIAL GENE; BACTERIUM; BIOTRANSFORMATION; GENETIC VARIABILITY; GENETICS; METABOLISM; MICROBIOLOGY; PACIFIC OCEAN; TEMPERATURE;

ALKYL AND ARYL TRANSFERASES; BACTERIA; BIOTRANSFORMATION; GENES, BACTERIAL; GENETIC VARIATION; METABOLIC NETWORKS AND PATHWAYS; PACIFIC OCEAN; SEAWATER; SULFONIUM COMPOUNDS; TEMPERATURE;

PACIFIC OCEAN; PACIFIC OCEAN (NORTH);

BACILLARIOPHYTA; BACTERIA (MICROORGANISMS);

EID: 84859947413     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.07559-11     Document Type: Article

References (66)

1. Andersen RA, Bidigare RR, Keller MD, Latasa M. 1996. A comparison of HPLC pigment signatures and electron microscopic observations for oligotrophic waters of the North Atlantic and Pacific Oceans. Deep Sea Res. 43:517-537.
2. Andreae MO, Crutzen PJ. 1997. Atmospheric aerosols: biogeochemical sources and role in atmospheric chemistry. Science 276:1052-1058.
3. Bell TG, Poulton AJ, Malin G. 2010. Strong linkages between dimethylsulphoniopropionate (DMSP) and phytoplankton community physiology in a large subtropical and tropical Atlantic Ocean data set. Global Biogeochem. Cycles 24:1-12.
4. Biers EJ, Sun S, Howard EC. 2009. Prokaryotic genomes and diversity in surface ocean waters: interrogating the global ocean sampling metagenome. Appl. Environ. Microbiol. 75:2221-2229.
5. Bürgmann H, et al. 2007. Transcriptional response of Silicibacter pomeroyi DSS-3 to dimethylsulfoniopropionate (DMSP). Environ. Microbiol. 9:2742-2755.
6. Campbell L, Nolla HA, Vaulot D. 1994. The importance of Prochlorococcus to community structure in the central North Pacific Ocean. Limnol. Oceanogr. 39:954-961.
7. Campbell L, Vaulot D. 1993. Photosynthetic picoplankton community structure in the subtropical North Pacific Ocean near Hawaii (Station ALOHA). Deep Sea Res. 40:2043-2060.
8. Chandler DP, Wagnon CA, and Bolton H, Jr. 1998. Reverse transcriptase (RT) inhibition of PCR at low concentrations of template and its implications for quantitative RT-PCR. Appl. Environ. Microbiol. 64:669-677.
9. Curson ARJ, Rogers R, Todd JD, Brearley CA, Johnston AWB. 2008. Molecular genetic analysis of a dimethylsulfoniopropionate lyase that liberates the climate-changing gas dimethylsulfide in several marine α-proteobacteria and Rhodobacter sphaeroides. Environ. Microbiol. 10:757-767.
10. Curson ARJ, Sullivan MJ, Todd JD, Johnston AWB. 2011. DddY, a periplasmic dimethylsulfoniopropionate lyase found in taxonomically diverse species of Proteobacteria. ISME J. 5:1191-1200.
11. DeLong EF, et al. 2006. Community genomics among stratified microbial assemblages in the ocean's interior. Science 311:496-503.
12. Del Valle DA, Kiene RP, Karl DM. Effect of visible light on dimethylsulfoniopropionate assimilation and conversion to dimethylsulfide in the North Pacific Subtropical Gyre. Aquat. Microb. Ecol., in press.
13. Eiler A, Hayakawa DH, Church MJ, Karl DM, Rappé MS. 2009. Dynamics of the SAR11 bacterioplankton lineage in relation to environmental conditions in the oligotrophic North Pacific Subtropical Gyre. Environ. Microbiol. 11:2291-2300.
14. Frias-Lopez J, et al. 2008. Microbial community gene expression in ocean surface waters. P. Natl. Acad. Sci. U. S. A. 105:3805-3810.
15. Gifford SM, Sharma S, Rinta-Kanto JM, Moran MA. 2011. Quantitative analysis of a deeply sequenced marine microbial metatranscriptome. ISME J. 5:461-472.
16. Gonzalez JM, Kiene RP, Moran MA. 1999. Transformation of sulfur compounds by an abundant lineage of marine bacteria in the α-subclass of the class Proteobacteria. Appl. Environ. Microbiol. 65:3810-3819.
17. Holm-Hansen O, Sutcliffe WH, Jr, Sharp J. 1968. Measurement of deoxyribonucleic acid in the ocean and its ecological significance. Limnol. Oceanogr. 13:507-514.
18. Howard EC, et al. 2006. Bacterial taxa that limit sulfur flux from the ocean. Science 314:649-652.
19. Howard EC, Sun S, Biers EJ, Moran MA. 2008. Abundant and diverse bacteria involved inDMSPdegradation in marine surface waters. Environ. Microbiol. 10:2397-2410.
20. Howard EC, et al. 2011. Changes in dimethylsulfoniopropionate demethylase gene assemblages in response to an induced phytoplankton bloom. Appl. Environ. Microbiol. 77:524-531.
21. Johnston AWB, et al. 2008. Molecular diversity of bacterial production of the climate-changing gas, dimethyl sulphide, a molecule that impinges on local and global symbioses. J. Exp. Bot. 59:1059-1067.
22. Karl DM. 2007. Microbial oceanography: paradigms, processes and promises. Nat. Rev. Microbiol. 5:759-769.
23. Karl DM. 1999. A sea of change: biogeochemical variability in the North Pacific Subtropical Gyre. Ecosystems 2:181-214.
24. Karl DM, Bidigare RR, Letelier RM. 2002. Sustained and aperiodic variability in organic matter production and phototrophic microbial community structure in the North Pacific Subtropical Gyre, p 222-264. In Williams PJ, Thomas DN, Reynolds CS (ed), Phytoplankton productivity: carbon assimilation in marine and freshwater ecosystems. Blackwell Science Ltd., Ames, IA.
25. Karl DM, Lukas R. 1996. The Hawaii Ocean Time-series (HOT) program: background, rationale and field implementation. Deep Sea Res. 43:129-156.
26. Karl DM, Winn CD, Hebel DVW, Letelier R. 1990. Hawaii Ocean Time-series program. Field and laboratory protocols. School of Ocean and Earth Science and Technology, University of Hawaii, Honolulu, HI.
27. Kiene RP, Linn LJ. 2000. Distribution and turnover of dissolved DMSP and its relationship with bacterial production and dimethylsulfide in the Gulf of Mexico. Limnol. Oceanogr. 45:849-861.
28. Kiene RP, Linn LJ, Bruton JA. 2000. New and important roles for DMSP in marine microbial communities. J. Sea Res. 43:209-224.
29. Kiene RP, Linn LJ, Gonzalez J, Moran MA, Bruton JA. 1999. Dimethylsulfoniopropionate and methanethiol are important precursors of methionine and protein-sulfur in marine bacterioplankton. Appl. Environ. Microbiol. 65:4549-4558.
30. Ledyard KM, Dacey JWH. 1996. Microbial cycling of DMSP and DMS in coastal and oligotrophic seawater. Limnol. Oceanogr. 41:33-40.
31. Letelier R, et al. 1993. Temporal variability of phytoplankton community structure based on pigment analysis. Limnol. Oceanogr. 38:1420-1437.
32. Levine NM, et al. 2012. Environmental, biochemical, and genetic drivers of DMSP degradation and DMS production in the Sargasso Sea. Environ. Microbiol. doi:10.1111/j.1462-2920.2012.02700.x.
33. Lovelock JE, Maggs RJ, Rasmussen RA. 1972. Atmospheric dimethyl sulphide and the natural sulphur cycle. Nature 237:452-453.
34. Malmstrom RR, et al. 2010. Temporal dynamics of Prochlorococcus ecotypes in the Atlantic and Pacific oceans. ISME J. 4:1252-1264.
35. Malmstrom RR, Kiene RP, Cottrell MT, Kirchman DL. 2004. Contribution of SAR11 bacteria to dissolved dimethylsulfoniopropionate and amino acid uptake in the North Atlantic Ocean. Appl. Environ. Microbiol. 70:4129-4135.
36. Matrai P, Vernet M, Wassman P. 2007. Relating temporal and spatial patterns of DMSP in the Barents Sea to phytoplankton biomass and productivity. J. Marine Syst. 67:83-101.
37. Matsen EA, Kodner RB, Armbrust EV. 2010. pplacer: linear time maximum-likelihood and Bayesian phylogenetic placement of sequences onto a fixed reference tree. BMC Bioinformatics 11:538.
38. Monterey GI, Levitus S. 1997. Seasonal variability of mixed layer depth for the world ocean. NOAA NESDIS Atlas 14:5.
39. Oksanen J, et al. 2009. vegan: community ecology package. R package version 1.15-4. http://CRAN.R-project.org/package~vegan.
40. Pichereau V, Pocard J-A, Hamelin J, Blanco C, Bernard T. 1998. Differential effects of dimethylsulfoniopropionate, dimethylsulfonioacetate, and other S-methylated compounds on the growth of Sinorhizobium meliloti at low and high osmolarities. Appl. Environ. Microbiol. 64:1420-1429.
41. Poretsky RS, et al. 2009. Comparative day/night metatranscriptomic analysis of microbial communities in the North Pacific Subtropical Gyre. Environ. Microbiol. 11:1358-1375.
42. R Development Core Team. 2011. R: a language and environment for statistical computing. R foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org.
43. Reisch CR, Moran MA, Whitman WB. 2008. Dimethylsulfoniopropionatedependent demethylase (DmdA) from Pelagibacter ubique and Silicibacter pomeroyi. J. Bacteriol. 190:8018-8024.
44. Reisch CR, et al. 2011. Novel pathway for assimilation of dimethylsulphoniopropionate widespread in marine bacteria. Nature 473:208-211.
45. Rinta-Kanto JM, Sun S, Sharma S, Kiene RP, Moran MA. 2012. Bacterial community transcription patterns during a marine phytoplankton bloom. Environ. Microbiol. 14:228-239.
46. Rusch DB, et al. 2007. The Sorcerer II global ocean sampling expedition: Northwest Atlantic through Eastern Tropical Pacific. PLoS Biol. 5:e77.
47. Scharek R, Latasa M, Karl DM, Bidigare RR. 1999. Temporal variations in diatom abundance and downward vertical flux in the oligotrophic North Pacific Gyre. Deep Sea Res. 46:1051-1075.
48. Shi Y, Tyson GW, DeLong EF. 2009. Metatranscriptomics reveals unique microbial small RNAs in the ocean's water column. Nature 459:266-269.
49. Simo R. 2001. Production of atmospheric sulfur by oceanic plankton: biogeochemical, ecological and evolutionary links. Trends Ecol. Evol. 16: 287-294.
50. Slezak D, Kiene R, Toole D, Simó R, Kieber D. 2007. Effects of solar radiation on the fate of dissolved DMSP and conversion to DMS in seawater. Aquat. Sci. 69:377-393.
51. Stewart FJ, Ottesen EA, DeLong EF. 2010. Development and quantitative analyses of a universal rRNA-subtraction protocol for microbial metatranscriptomics. ISME J. 4:896-907.
52. Sunda W, Kieber DJ, Kiene RP, Huntsman S. 2002. An antioxidant function for DMSP and DMS in marine algae. Nature 418:317-320.
53. Suzuki MT, Taylor LT, DeLong EF. 2000. Quantitative analysis of smallsubunit rRNA genes in mixed microbial populations via 5=-nuclease assays. Appl. Environ. Microbiol. 66:4605-4614.
54. Todd JD, Curson AJ, Dupont CL, Nicholson P, Johnston AWB. 2009. The dddP gene, encoding a novel enzyme that converts dimethylsulfoniopropionate into dimethyl sulfide, is widespread in ocean metagenomes and marine bacteria and also occurs in some Ascomycete fungi. Environ. Microbiol. 11:1624-1625.
55. Todd JD, et al. 2011. DddQ, a novel, cupin-containing, dimethylsulfoniopropionate lyase in marine roseobacters and in uncultured marine bacteria. Environ. Microbiol. 13:427-438.
56. Todd JD, Kirkwood M, Newton-Payne S, Johnston AWB. 2012. DddW, a third DMSP lyase in a model Roseobacter marine bacterium, Ruegeria pomeroyi DSS-3. ISME J. 6:223-226.
57. Todd JD, et al. 2007. Structural and regulatory genes required to make the gas dimethyl sulfide in bacteria. Science 315:666-669.
58. Tripp HJ, et al. 2008. SAR11 marine bacteria require exogenous reduced sulphur for growth. Nature 452:741-744.
59. Turner SM, Malin G, Bågander LE, Leck C. 1990. Interlaboratory calibration and sample analysis of dimethyl sulphide in water. Mar. Chem. 29:47-62.
60. Vairavamurthy A, Andreae MO, Iverson RL. 1985. Biosynthesis of dimethylsulfide and dimethylpropiothetin by Hymenomonas carterae in relation to sulfur source and salinity variations. Limnol. Oceanogr. 30:59-70.
61. Vallina SM, Simo R. 2007. Strong relationship between DMS and the solar radiation dose over the global surface ocean. Science 315:506-508.
62. Varaljay VA, Howard EC, Sun S, Moran MA. 2010. Deep sequencing of a dimethylsulfoniopropionate-degrading gene (dmdA) by using PCR primer pairs designed on the basis of marine metagenomic data. Appl. Environ. Microbiol. 76:609-617.
63. Venter JC, et al. 2004. Environmental genome shotgun sequencing of the Sargasso Sea. Science 304:66-74.
64. Vila-Costa M, et al. 2010. Transcriptomic analysis of a marine bacterial community enriched with dimethylsulfoniopropionate. ISME J. 4:1410-1420.
65. Vila-Costa M, et al. 2006. Dimethylsulfoniopropionate uptake by marine phytoplankton. Science 314:652-654.
66. Winn CD, Karl DM. 1986. Diel nucleic acid synthesis and particulate DNA concentrations: conflicts with division rate estimates by DNA accumulation. Limnol. Oceanogr. 31:637-645.