Expression of sulfatases in Rhodopirellula baltica and the diversity of sulfatases in the genus Rhodopirellula

Marine Genomics

Volumn 9, Issue , 2013, Pages 51-61

  Wegner, Carl Eric ^a,b,e   Richter Heitmann, Tim ^a,c,f   Klindworth, Anna ^a,d   Klockow, Christine ^a,d   Richter, Michael ^a   Achstetter, Tilman ^c   Glöckner, Frank Oliver ^a,d   Harder, Jens ^a  

^a MAX PLANCK INSTITUTE FOR MARINE MICROBIOLOGY   (Germany)

^b UNIVERSITY OF OLDENBURG   (Germany)

^c HOCHSCHULE BREMEN   (Germany)

^d JACOBS UNIVERSITY BREMEN   (Germany)

^e MAX PLANCK INSTITUTE FOR TERRESTRIAL MICROBIOLOGY   (Germany)

^f UNIVERSITY OF BREMEN   (Germany)

Author keywords

Marine planctomycetes; Phylogenomics; Sulfatases; Transcriptomics

Indexed keywords

BACTERIAL PROTEIN; BACTERIAL RNA; MESSENGER RNA; SULFATASE;

ANIMAL; ARTICLE; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PHYLOGENY; PHYSIOLOGY; PLANCTOMYCETALES;

ANIMALS; BACTERIAL PROTEINS; GENE EXPRESSION REGULATION, BACTERIAL; GENE EXPRESSION REGULATION, ENZYMOLOGIC; PHYLOGENY; PLANCTOMYCETALES; RNA, BACTERIAL; RNA, MESSENGER; SULFATASES;

PLANCTOMYCETES; RHODOPIRELLULA; RHODOPIRELLULA BALTICA;

EID: 84876458487     PISSN: 18747787     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.margen.2012.12.001     Document Type: Article

References (50)

1. Altschul S., Gish W., Miller W., Myers E., Lipman D. Basic local alignment search tool. J. Mol. Biol. 1990, 215:403-410.
2. Battke F., Symons S., Nieselt K. Mayday - integrative analytics for expression data. BMC Bioinforma. 2010, 11:121.
3. Bendtsen J.D., Nielsen H., von Heijne G., Brunak S. Improved prediction of signal peptides: SignalP 3.0. J. Mol. Biol. 2004, 340:783-795.
4. Bengtsson M.M., Sjotun K., Ovreas L. Seasonal dynamics of bacterial biofilms on the kelp Laminaria hyperborea. Aquat. Microb. Ecol. 2010, 60:71-83.
5. Benjdia A., Deho G., Rabot S., Berteau O. First evidences for a third sulfatase maturation system in prokaryotes from E. coli aslB and ydeM deletion mutants. FEBS Lett. 2007, 581:1009-1014.
6. Berteau O., Guillot A., Benjdia A., Rabot S. A new type of bacterial sulfatase reveals a novel maturation pathway in prokaryotes. J. Biol. Chem. 2006, 281:22464-22470.
7. Bilan M.I., Grachev A.A., Shashko A.S., Nifantiev N.E., Usov A.I. Structure of a fucoidan from the brown seaweed Fucus serratus. Carbohydr. Res. 2006, 341:238-245.
8. Carlson B.L., Ballister E.R., Skordalakes E., King D.S., Breidenbach M.A., Gilmore S.A., Berger J.M., Bertozzi C.R. Function and structure of a prokaryotic formylglycine-generating enzyme. J. Biol. Chem. 2008, 283:20117-20125.
9. Chen F., Mackey A.J., Stoeckert C.J., Roos D.S. OrthoMCL-DB: querying a comprehensive multi-species collection of ortholog groups. Nucleic Acids Res. 2006, 34:D363-D368.
10. Crooks G.E., Hon G., Chandonia J.M., Brenner S.E. WebLogo: a sequence logo generator. Genome Res. 2004, 14:1188-1190.
11. Deutscher J., Francke C., Postma P.W. How phosphotransferase system-related protein phosphorylation regulates carbohydrate metabolism in bacteria. Microbiol. Mol. Biol. Rev. 2006, 70:939-1031.
12. Dierks T., Lecca M.R., Schlotterhose P., Schmidt B., von Figura K. Sequence determinants directing conversion of cysteine to formylglycine in eukaryotic sulfatases. EMBO J. 1999, 18:2084-2091.
13. Finn R.D., Mistry J., Tate J., Coqqill P., Heger A., Pollington J.E., Gavin O.L., Gunasekaran P., Ceric G., Forslund K., Holm L., Sonnhammer E.L., Eddy S.R., Bateman A. The Pfam protein families database. Nucleic Acids Res. 2010, 38:D211-D222.
14. Frank C.S., Langhammer P., Harder J. Ammonia and attachment of Rhodopirellula baltica. Arch. Microbiol. 2011, 193:365-372.
15. Gade D., Gobom J., Rabus R. Proteomic analysis of carbohydrate catabolism and regulation in the marine bacterium Rhodopirellula baltica. Proteomics 2005, 5:3672-3683.
16. Ghosh D. Human sulfatases: a structural perspective to catalysis. Cell. Mol. Life Sci. 2007, 64:2013-2022.
17. Glöckner F.O., Kube M., Bauer M., Teeling H., Lombardot T., Ludwig W., Gade D., Beck A., Borzym K., Heitmann K., Rabus R., Schlesner H., Amann R., Reinhardt R. Complete genome sequence of the marine planctomycete Pirellula sp. strain 1. Proc. Natl. Acad. Sci. U.S.A. 2003, 100:8298-8303.
18. Hagelueken G., Adams T.M., Wiehlmann L., Widow U., Kolmar H., Tuemmler B., Heinz D.W., Schubert W.-D. The crystal structure of SdsA1, an alkylsulfatase from Pseudomonas aeruginosa, defines a third class of sulfatases. Proc. Natl. Acad. Sci. U.S.A. 2006, 103:10824.
19. Han M.V., Zmasek C.M. phyloXML: XML for evolutionary biology and comparative genomics. BMC Bioinforma. 2009, 10:356.
20. Hanson S.R., Best M.D., Wong C.H. Sulfatases: structure, mechanism, biological activity, inhibition, and synthetic utility. Angew. Chem. Int. Edit. 2004, 43:5736-5763.
21. T. Proteomics 2008, 8:1608-1623.
22. Jogler C., Glöckner F.O., Kolter R. Characterization of Planctomyces limnophilus and development of genetic tools for its manipulation establish it as a model species for the phylum Planctomycetes. Appl. Environ. Microbiol. 2011, 77:5826-5829.
23. Katoh K., Misawa K., Kuma K., Miyata T. MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucl. Acids Res. 2002, 30:3059-3066.
24. Krogh A., Larsson B., von Heijne G., Sonhammer E.L. Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. J. Mol. Biol. 2001, 305:567-580.
25. Lage M.L., Bondoso J. Planctomycetes diversity associated with macroalgae. FEMS Microbiol. Ecol. 2011, 78:366-375.
26. Lahaye M., Robic A. Structure and functional properties of ulvan, a polysaccharide from green seaweeds. Biomacromolecules 2007, 8:1765-1774.
27. Li B., Lu F., Wei X., Zhao R. Fucoidan: structure and bioactivity. Molecules 2008, 13:1671-1695.
28. Liesack W., Koenig H., Schlesner H., Hirsch P. Chemical composition of the peptidoglycan-free cell envelopes of budding bacteria of the Pirella/Planctomyces group. Arch. Microbiol. 1986, 145:361-366.
29. Michel G., Nyval-Collen P., Barbeyron T., Czjzek M., Helbert W. Bioconversion of red seaweed galactans: a focus on bacterial agarases and carrageenases. Appl. Microbiol. Biotechnol. 2006, 71:23-33.
30. Miller M.A., Pfeiffer W., Schwartz T. Creating the CIPRES Science Gateway for inference of large phylogenetic trees. Proceedings of the Gateway Computing Environments Workshop (GCE), 14 Nov. 2010, New Orleans, LA 2010, 1-8.
31. Müller I., Kahnert A., Pape T., Sheldrick G.M., Meyer-Klaucke W., Dierks T., Kertesz M., Uson I. Crystal structure of the alkylsulfatase AtsK: insights into the catalytic mechanism of the Fe(II) alpha-ketoglutarate-dependent dioxygenase superfamily. Biochemistry 2004, 43:3075-3088.
32. Poli A., Anzelmo G., Nicolaus B. Bacterial exopolysaccharides from extreme habitats: production, characterization and biological activities. Mar. Drugs 2010, 8:1779-1802.
33. Punta M., Coggill P.C., Eberhardt R.Y., Mistry J., Tate J., Boursnell C., Pang N., Forslund K., Ceric G., Clements J., Heger A., Holm L., Sonnhammer E.L.L., Eddy S.R., Bateman A., Finn R.D. The Pfam protein families database. Nucleic Acids Res. 2012, 40:D290-D301.
34. Richter M., Rosselló-Móra R. Shifting the genomic gold standard for the prokaryotic species definition. Proc. Natl. Acad. Sci. U.S.A. 2009, 106:19126-19131.
35. Sardiello M., Annunziata I., Roma G., Ballabio A. Sulfatases and sulfatase modifying factors: an exclusive and promiscuous relationship. Hum. Mol. Genet. 2005, 14:3203-3217.
36. Schlesner H. The development of media suitable for the microorganisms morphologically resembling Planctomycetes spp., Pirellula spp. and other Planctomycetales from various aquatic habitats using dilute media. Syst. Appl. Microbiol. 1994, 17:135-145.
37. Schlesner H., Rensmann C., Tindall B.J., Gade D., Rabus R., Pfeiffer S., Hirsch P. Taxonomic heterogeneity within the Planctomycetales as derived by DNA-DNA hybridization, description of Rhodopirellula baltica gen. nov., sp. nov., transfer of Pirellula marina to the genus Blastopirellula gen. nov. as Blastopirellula marina comb. nov. and emended description of the genus Pirellula. Int. J. Syst. Evol. Microbiol. 2004, 54:1567-1580.
38. Siebold C., Flukiger K., Beutler R., Erni B. Carbohydrate transporters of the bacterial phosphoenolpyruvate: sugar phosphotransferase system (PTS). FEBS Lett. 2001, 504:104-111.
39. Stamatakis A. RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 2006, 22:2688-2690.
40. The UniProt Consortium Reorganizing the protein space at the Universal Protein Resource (UniProt). Nucleic Acids Res. 2012, 40:D71-D75.
41. Thrash J.C., Cho J.C., Vergin K.L., Morris R.M., Giovannoni S.J. Genome sequence of Lentisphaera araneosa HTCC2155T, the type species of the order Lentisphaerales in the phylum Lentisphaerae. J. Bacteriol. 2010, 192:2938-2939.
42. Usov A.I., Bilan M.I. Fucoidans - sulfated polysaccharides of brown algae. Russ. Chem. Rev. 2009, 78:785-799.
43. Waterhouse A.M., Procter J.B., Martin D.M.A., Clamp M., Barton G.J. Jalview Version 2-a multiple sequence alignment editor and analysis workbench. Bioinformatics 2009, 25:1189.
44. T to changing environmental conditions. BMC Genomics 2009, 10:410.
45. T by transcriptome studies. Microb. Biotechnol. 2010, 3:583-594.
46. Winkelmann N., Harder J. An improved isolation method for attached-living Planctomycetes of the genus Rhodopirellula. J. Microbiol. Meth. 2009, 77:276-284.
47. Winkelmann N., Jaekel U., Meyer C., Serrano W., Rosselló-Móra R.R., Harder J. Determination of the diversity of Rhodopirellula isolates from European seas by multilocus sequence analysis. Appl. Environ. Microbiol. 2010, 76:776-785.
48. Wöbken D., Teeling H., Wecker P., Dumitriu A., Kostadinov I., DeLong E.F., Amann R., Glöckner F.O. From the Namibian and Oregon coast upwelling systems and their cross-comparison with planctomycete genomes. ISME J. 2007, 1:419-435.
49. Zierer M.S., Mourao P.A.S. A wide diversity of sulfated polysaccharides are synthesized by different species of marine sponges. Carbohydr. Res. 2000, 328:209-216.
50. Ziervogel K., Arnosti C. Polysaccharide hydrolysis in aggregates and free enzyme activity in aggregate-free seawater from the north-eastern Gulf of Mexico. Environ. Microbiol. 2008, 10:289-299.