Diversity of DMSP transport in marine bacteria, revealed by genetic analyses

Biogeochemistry

Volumn 110, Issue 1-3, 2012, Pages 121-130

  Sun, Lei ^a,b   Curson, Andrew R J ^a   Todd, Jonathan D ^a   Johnston, Andrew W B ^a  

^a UNIVERSITY OF EAST ANGLIA   (United Kingdom)

^b UNIVERSITY OF KENT   (United Kingdom)

Author keywords

ABC transporter; BCCT transporter; ddd Genes; DMSP; Halomonas; Marinomonas; Roseovarius; Sulfitobacter

Indexed keywords

AMINO ACID; CATABOLISM; COLIFORM BACTERIUM; ENZYME ACTIVITY; GENE EXPRESSION; GENETIC ANALYSIS; MARINE ENVIRONMENT; MUTATION; OSMOSIS; PHENOTYPE; SPECIES DIVERSITY; SULFIDE;

ALPHAPROTEOBACTERIA; BACTERIA (MICROORGANISMS); BURKHOLDERIA AMBIFARIA; BURKHOLDERIA AMBIFARIA AMMD; ESCHERICHIA COLI; HALOMONAS; MARINOMONAS; ROSEOVARIUS; ROSEOVARIUS NUBINHIBENS ISM; SULFITOBACTER; SULFITOBACTER SP. EE-36;

EID: 84867143781     PISSN: 01682563     EISSN: 1573515X     Source Type: Journal    
DOI: 10.1007/s10533-011-9666-z     Document Type: Article

References (42)

1. Allaway D, Schofield NA, Leonard ME, Gilardoni L, Finan TM et al (2001) Use of differential fluorescence induction and optical trapping to isolate environmentally induced genes. Env Microbiol 3: 397-406.
2. Bürgmann H, Howard EC, Ye W, Sun F, Sun S, Napierala S, Moran MA (2007) Transcriptional response of Silicibacter pomeroyi DSS-3 to dimethylsulfoniopropionate (DMSP). Env Microbiol 9: 2742-2755.
3. Casadaban MJ (1976) Transposition and fusion of the lac genes to selected promoters in Escherichia coli using bacteriophage lambda and mu. J Mol Biol 104: 541-555.
4. Cosquer A, Pichereau V, Pocard JA, Minet J, Cormier M, Bernard T (1999) Nanomolar levels of dimethylsulfoniopropionate, dimethylsulfonioacetate, and glycine betaine are sufficient to confer osmoprotection to Escherichia coli. Appl Env Microbiol 65: 3304-3311.
5. 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 alpha-proteobacteria and Rhodobacter sphaeroides. Env Microbiol 10: 757-767.
6. Curson ARJ, Fowler EK, Dickens S, Johnston AWB, Todd JD (2011a) Multiple DMSP lyases in the γ-proteobacterium Oceanimonas doudoroffii. Biogeochemistry. doi: 10. 1007/s10533-011-9663-2.
7. Curson ARJ, Sullivan MJ, Todd JD, Johnston AWB (2011b) DddY, a periplasmic dimethylsulfoniopropionate lyase found in taxonomically diverse species of proteobacteria. ISME J 5: 191-200.
8. de Souza MP, Yoch DC (1995) Comparative physiology of dimethyl sulfide production by dimethylsulfoniopropionate lyase in Pseudomonas doudoroffii and Alcaligenes sp. strain M3A. Appl Env Microbiol 61: 3986-3991.
9. Dickson DMJ, Hirst GO (1987) Osmotic adjustment in marine eukaryotic algae - the role of inorganic ions, quaternary ammonium, tertiary sulphonium and carbohydrate solutes. I. Diatoms and a Rhodophyte. New Phytol 106: 545-655.
10. Eitinger T, Rodionov DA, Grote M, Schneider E (2011) Canonical and ECF-type ATP-binding cassette importers in prokaryotes: diversity in modular organization and cellular functions. FEMS Microbiol Rev 35: 3-67.
11. Figurski DH, Helinski DR (1979) Replication of an origin-containing derivative of plasmid RK2 dependant on a plasmid function provided in trans. Proc Natl Acad Sci USA 76: 1648-1652.
12. González JM, Whitman WB, Hodson RE, Moran MA (1996) Identifying numerically abundant culturable bacteria from complex communities: an example from a lignin enrichment culture. Appl Env Microbiol 62: 4433-4440.
13. González 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 Env Microbiol 65: 3810-3819.
14. Gowrishankar J (1989) Nucleotide sequence of the osmoregulatory proU operon of Escherichia coli. J Bacteriol 171: 1923-1931.
15. Haardt M, Kempf B, Faatz E, Bremer E (1995) The osmoprotectant proline betaine is a major substrate for the binding-protein-dependent transport system ProU of Escherichia coli K-12. Mol Gen Genet 246: 783-786.
16. Hanson AD, Rathinasabapathi B, Rivoal J, Burnet M, Dillon MO, Gage DA (1994) Osmoprotective compounds in the Plumbaginaceae: a natural experiment in metabolic engineering of stress tolerance. Proc Natl Acad Sci USA 91: 306-310.
17. Howard EC, Henriksen JR, Buchan A, Reisch CR, Bürgmann H et al (2006) Bacterial taxa that limit sulfur flux from the ocean. Science 314: 649-652.
18. Igarashi K, Kashiwagi K (2010) Characteristics of cellular polyamine transport in prokaryotes and eukaryotes. Plant Physiol Biochem 48: 506-512.
19. Johnston AWB, Todd JD, Sun L, Nikolaidou-Katsaridou MN, Curson ARJ, Rogers R (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.
20. Karsten U, Kirst GO, Wiencke C (1992) Dimethylsulphoniopropionate (DMSP) accumulation in green macroalgae from polar to temperate regions: interactive effects of light versus salinity and light versus temperature. Polar Biol 12: 603-607.
21. Keen NT, Tamaki S, Kobayashi D, Trollinger D (1988) Improved broad-host-range plasmids for DNA cloning in gram-negative bacteria. Gene 70: 191-197.
22. Kempf B, Gade J, Bremer E (1997) Lipoprotein from the osmoregulated ABC transport system OpuA of Bacillus subtilis: purification of the glycine betaine binding protein and characterization of a functional lipidless mutant. J Bacteriol 179: 6213-6220.
23. Kiene RP, Williams LPH, Walker JE (1998) Seawater microorganisms have a high affinity glycine betaine uptake system which also recognises dimethylsulfoniopropionate. Aqu Microb Ecol 15: 39-51.
24. Kirkwood M, Todd JD, Rypien KL, Johnston AWB (2010) The opportunistic coral pathogen Aspergillus sydowii contains dddP and makes dimethyl sulfide from dimethylsulfoniopropionate. ISME J 4: 147-150.
25. 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 Env Microbiol 70: 4129-4135.
26. Messing J, Crea R, Seeburg PH (1983) A system for shotgun cloning DNA sequencing. Nucleic Acid Res 9: 309-314.
27. Moran MA, Buchan A, González JM, Heidelberg JF, Whitman WB, Kiene RP et al (2004) Genome sequence of Silicibacter pomeroyi reveals adaptations to the marine environment. Nature 432: 910-913.
28. Newton RJ, Griffin LE, Bowles KM, Meile C, Gifford S, Givens CE et al (2010) Genome characteristics of a generalist marine bacterial lineage. ISME J 4: 784-798.
29. Otte ML, Wilson G, Morris JT, Moran BM (2004) Dimethylsulphoniopropionate (DMSP) and related compounds in higher plants. J Exp Bot 55: 1919-1925.
30. Peter H, Burkovski A, Krämer R (1996) Isolation, characterization, and expression of the Corynebacterium glutamicum betP gene, encoding the transport system for the compatible solute glycine betaine. J Bacteriol 178: 5229-5234.
31. Schmidt S, Pflüger K, Kögl S, Spanheimer R, Müller V (2007) The salt-induced ABC transporter Ota of the methanogenic archaeon Methanosarcina mazei Gö1 is a glycine betaine transporter. FEMS Microbiol Lett 277: 44-49.
32. Todd JD, Rogers R, Li YG, Wexler M, Bond PL et al (2007) Structural and regulatory genes required to make the gas dimethyl sulfide in bacteria. Science 315: 666-669.
33. Todd JD, Curson ARJ, 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. Env Microbiol 11: 1376-1385.
34. Todd JD, Curson ARJ, Nikolaidou-Katsaraidou N, Brearley CA, Watmough NJ, Chan Y, Page PC, Sun L, Johnston AWB (2010) Molecular dissection of bacterial acrylate catabolism-unexpected links with dimethylsulfoniopropionate catabolism and dimethyl sulfide production. Env Microbiol 12: 327-343.
35. Todd JD, Curson ARJ, Kirkwood M, Sullivan MJ, Green RT, Johnston AWB (2011a) DddQ, a novel, cupin-containing, dimethylsulfoniopropionate lyase in marine roseobacters and in uncultured marine bacteria. Env Microbiol 13: 427-438.
36. Todd JD, Kirkwood M, Newton-Payne S, Johnston AWB (2011b) DddW, a third DMSP lyase in a model Roseobacter marine bacterium, Ruegeria pomeroyi DSS-3. ISME J. doi: 10. 1038/ismej. 2011. 79.
37. Trinick MJ (1973) Symbiosis between Rhizobium and the non-legume, Trema aspera. Nature 244: 459-460.
38. Tripp HJ, Kitner JB, Schwalbach MS, Dacey JWH, Wilhelm LJ, Stephen J, Giovannoni SJ (2008) SAR11 marine bacteria require exogenous reduced sulphur for growth. Nature 452: 741-744.
39. Vila-Costa M, Simó R, Harada H, Gasol JM, Slezak D, Kiene RP (2006) Dimethylsulfoniopropionate uptake by marine phytoplankton. Science 314: 652-654.
40. Wexler M, Yeoman KH, Stevens JB, de Luca NG, Sawers G, Johnston AWB (2001) The Rhizobium leguminosarum tonB gene is required for the uptake of siderophore and haem as sources of iron. Mol Microbiol 41: 801-816.
41. Yoch DC (2002) Dimethylsulfoniopropionate: its sources, role in the marine food web, and biological degradation to dimethylsulfide. Appl Env Microbiol 68: 5804-5815.
42. Ziegler C, Bremer E, Krämer R (2010) The BCCT family of carriers: from physiology to crystal structure. Mol Microbiol 78: 13-34.