Skip to main content

Advertisement

SpringerLink
Log in

Diversity, ecology, and genomics of the Roseobacter clade: a short overview

  • Mini Review
  • Published:
Archives of Microbiology Aims and scope Submit manuscript

Abstract

Due to worldwide distribution, high abundance and availability of physiologically diverse isolates the Roseobacter clade is one of the most intensively studied groups of marine bacteria. Organisms of this clade have been detected in a large variety of habitats, from coastal regions to deep-sea sediments and from polar ice to tropical latitudes, and constitute up to 25% of the total bacterial community. Use of a multitude of organic compounds, sulfur oxidation, aerobic anoxygenic photosynthesis, oxidation of carbon monoxide, DMSP demethylation, and production of secondary metabolites are some of the important traits found in this clade. Physiological characteristics and the different isolation sources indicate that organisms of the Roseobacter clade occupy various ecological niches. Since the first description of Roseobacter spp. in 1991, 38 affiliated and validated genera have been described. More than half of these descriptions have been published within the last 3 years. Genome sequencing of currently 40 different strains demonstrates enormous interest in the genetic and metabolic diversity of these bacteria. Plasmids with an enormous size range are also widespread in the Roseobacter clade indicating an adaptive genomic structure. Comparisons with other highly relevant groups, like the SAR11 clade, have shown drastic differences in genome organization.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1

Similar content being viewed by others

References

  • Allgaier M, Uphoff H, Felske A, Wagner-Döbler I (2003) Aerobic anoxygenic photosynthesis in Roseobacter clade bacteria from diverse marine habitats. Appl Environ Microbiol 69:5051–5059

    Article  PubMed  CAS  Google Scholar 

  • Arahal DR, Macian MC, Garay E, Pujalte MJ (2005) Thalassobius mediterraneus gen. nov., sp nov., and reclassification of Ruegeria gelatinovorans as Thalassobius gelatinovorus comb. nov. Int J Syst Evol Microbiol 55:2371–2376

    Article  PubMed  CAS  Google Scholar 

  • Beja O, Suzuki MT, Heidelberg JF, Nelson WC, Preston CM, Hamada T, Eisen JA, Fraser CM, DeLong EF (2002) Unsuspected diversity among marine aerobic anoxygenic phototrophs. Nature 415:630–633

    Article  PubMed  CAS  Google Scholar 

  • Biebl H, Allgaier M, Tindall BJ, Koblizek M, Lunsdorf H, Pukall R, Wagner-Döbler I (2005) Dinoroseobacter shibae gen. nov., sp nov., a new aerobic phototrophic bacterium isolated from dinoflagellates. Int J Syst Evol Microbiol 55:1089–1096

    Article  PubMed  CAS  Google Scholar 

  • Brinkhoff T, Bach G, Heidorn T, Liang LF, Schlingloff A, Simon M (2004) Antibiotic production by a Roseobacter clade-affiliated species from the German Wadden Sea and its antagonistic effects on indigenous isolates. Appl Environ Microbiol 70:2560–2565

    Article  PubMed  CAS  Google Scholar 

  • Brinkmeyer R, Knittel K, Jürgens J, Weyland H, Amann R, Helmke E (2003) Diversity and structure of bacterial communities in Arctic versus Antarctic Pack Ice. Appl Environ Microbiol 69:6610–6619

    Article  PubMed  CAS  Google Scholar 

  • Bruhn JB, Nielsen KF, Hjelm M, Hansen M, Bresciani J, Schulz S, Gram L (2005) Ecology, inhibitory activity, and morphogenesis of a marine antagonistic bacterium belonging to the Roseobacter clade. Appl Environ Microbiol 71:7263–7270

    Article  PubMed  CAS  Google Scholar 

  • Bruhn JB, Gram L, Belas R (2007) Production of antibacterial compounds and biofilm formation by Roseobacter species are influenced by culture conditions. Appl Environ Microbiol 73:442–450

    Article  PubMed  CAS  Google Scholar 

  • Buchan A, Gonzalez JM, Moran MA (2005) Overview of the marine Roseobacter lineage. Appl Environ Microbiol 71:5665–5677

    Article  PubMed  CAS  Google Scholar 

  • Chen F, Wang K, Stewart J, Belas R (2006) Induction of multiple prophages from a marine bacterium: a genomic approach. Appl Environ Microbiol 72:4995–5001

    Article  PubMed  CAS  Google Scholar 

  • Choi DH, Cho JC, Lanoil BD, Giovannoni SJ, Cho BC (2007) Maribius salinus gen. nov., sp. nov., isolated from a solar saltern and Maribius pelagius sp. nov., cultured from the Sargasso Sea, belonging to the Roseobacter clade. Int J Syst Evol Microbiol 57:270–275

    Article  PubMed  CAS  Google Scholar 

  • Denner EBM, Kolari M, Hoornstra D, Tsitko I, Kämpfer P, Busse HJ, Salkinoja-Salonen M (2006) Rubellimicrobium thermophilum gen. nov., sp nov., a red-pigmented, moderately thermophilic bacterium isolated from coloured slime deposits in paper machines. Int J Syst Evol Microbiol 56:1355–1362

    Article  PubMed  CAS  Google Scholar 

  • Giovannoni SJ, Tripp HJ, Givan S, Podar M, Vergin KL, Baptista D, Bibbs L, Eads J, Richardson TH, Noordewier M, Rappe MS, Short JM, Carrington JC, Mathur EJ (2005) Genome streamlining in a cosmopolitan oceanic bacterium. Science 309:1242–1245

    Article  PubMed  CAS  Google Scholar 

  • Gosink JJ, Herwig RP, Staley JT (1997) Octadecabacter arcticus gen nov, sp nov, and O. antarcticus, sp nov, nonpigmented, psychrophilic gas vacuolate bacteria from polar sea ice and water. Syst Appl Microbiol 20:356–365

    Google Scholar 

  • Gram L, Grossart HP, Schlingloff A, Kiorboe T (2002) Possible quorum sensing in marine snow bacteria: production of acylated homoserine lactones by Roseobacter strains isolated from marine snow. Appl Environ Microbiol 68:4111–4116

    Article  PubMed  CAS  Google Scholar 

  • Hansel CM, Francis CA (2006) Coupled photochemical and enzymatic Mn(II) oxidation pathways of a planktonic Roseobacter-like bacterium. Appl Environ Microbiol 72:3543–3549

    Article  PubMed  CAS  Google Scholar 

  • Kolber ZS, Plumley FG, Lang AS, Beatty JT, Blankenship RE, VanDover CL, Vetriani C, Koblizek M, Rathgeber C, Falkowski PG (2001) Contribution of aerobic photoheterotrophic bacteria to the carbon cycle in the ocean. Science 292:2492–2495

    Article  PubMed  CAS  Google Scholar 

  • Labrenz M, Collins MD, Lawson PA, Tindall BJ, Braker G, Hirsch P (1998) Antarctobacter heliothermus gen. nov., sp. nov., a budding bacterium from hypersaline and heliothermal Ekho Lake. Int J Syst Evol Microbiol 48:1363–1372

    CAS  Google Scholar 

  • Labrenz M, Lawson PA, Tindall BJ, Collins MD, Hirsch P (2005) Roseisalinus antarcticus gen. nov., sp. nov., a novel aerobic bacteriochlorophyll a-producing a-proteobacterium isolated from hypersaline Ekho Lake, Antarctica. Int J Syst Evol Microbiol 55:41–47

    Article  PubMed  CAS  Google Scholar 

  • Ludwig W, Strunk O, Westram R, Richter L, Meier H, Yadhukumar, Buchner A, Lai T, Steppi S, Jobb G, Forster W, Brettske I, Gerber S, Ginhart AW, Gross O, Grumann S, Hermann S, Jost R, Konig A, Liss T, Lussmann R, May M, Nonhoff B, Reichel B, Strehlow R, Stamatakis A, Stuckmann N, Vilbig A, Lenke M, Ludwig T, Bode A, Schleifer KH (2004) ARB: a software environment for sequence data. Nucleic Acids Res 32:1363–1371

    Article  PubMed  CAS  Google Scholar 

  • Malmstrom RR, Straza TRA, Cottrell MT, Kirchman DL (2007) Diversity, abundance, and biomass production of bacterial groups in the western Arctic Ocean. Aquat Microb Ecol 47:45–55

    Article  CAS  Google Scholar 

  • Martens T, Heidorn T, Pukall R, Simon M, Tindall BJ, Brinkhoff T (2006) Reclassification of Roseobacter gallaeciensis Ruiz-Ponte et al. 1998 as Phaeobacter gallaeciensis gen. nov., comb. nov., description of Phaeobacter inhibens sp. nov., reclassification of Ruegeria algicola (Lafay et al. 1995) Uchino et al. 1998 as Marinovum algicola gen. nov., comb. nov., and emended descriptions of the genera Roseobacter, Ruegeria, and Leisingera. Int J Syst Evol Microbiol 56:1293–1304

    Article  PubMed  CAS  Google Scholar 

  • Martens T, Gram L, Grossart H-P, Kessler D, Müller R, Simon M, Wenzel SC, Brinkhoff T (2007) Bacteria of the Roseobacter clade show potential for secondary metabolite production. Microb Ecol 54:31–42

    Article  PubMed  CAS  Google Scholar 

  • Martinez-Checa F, Quesada E, Martinez-Canovas MJ, Llamas I, Bejar V (2005) Palleronia marisminoris gen. nov., sp. nov., a moderately halophilic, exopolysaccharideproducing bacterium belonging to the ‘Alphaproteobacteria’, isolated from a saline soil. Int J Syst Evol Microbiol 55:2525–2530

    Article  PubMed  CAS  Google Scholar 

  • Moran MA, Buchan A, Gonzalez JM, Heidelberg JF, Whitman WB, Kiene RP, Henriksen JR, King GM, Belas R, Fuqua C, Brinkac L, Lewis M, Johri S, Weaver B, Pai G, Eisen JA, Rahe E, Sheldon WM, Ye WY, Miller TR, Carlton J, Rasko DA, Paulsen IT, Ren QH, Daugherty SC, Deboy RT, Dodson RJ, Durkin AS, Madupu R, Nelson WC, Sullivan SA, Rosovitz MJ, Haft DH, Selengut J, Ward N (2004) Genome sequence of Silicibacter pomeroyi reveals adaptations to the marine environment. Nature 432:910–913

    Article  PubMed  CAS  Google Scholar 

  • Moran MA, Belas R, Schell MA, González JM, Sun F, Sun S, Binder BJ, Edmonds J, Ye W, Orcutt B, Howard EC, Meile C, Palefsky W, Goesmann A, Ren Q, Paulsen I, Ulrich LE, Thompson LS, Saunders E, Buchan A (2007) Ecological genomics of marine Roseobacters. Appl Environ Microbiol 73:4559–69

    Article  PubMed  CAS  Google Scholar 

  • Muramatsu Y, Uchino Y, Kasai H, Suzuki K, Nakagawa Y (2007) Ruegeria mobilis sp. nov., a member of the Alphaproteobacteria isolated in Japan and Palau. Int J Syst Evol Microbiol 57:1304–1309

    Article  PubMed  CAS  Google Scholar 

  • Petursdottir SK, Kristjansson JK (1997) Silicibacter lacuscaerulensis gen. nov., sp. nov., a mesophilic moderately halophilic bacterium characteristic of the Blue Lagoon geothermal lake in Iceland. Extremophiles 1:94–99

    Article  PubMed  CAS  Google Scholar 

  • Pommier T, Pinhassi J, Hagström A (2005) Biogeographic analysis of ribosomal RNA clusters from marine bacterioplankton. Aquat Microbial Ecol 41:79–89

    Article  Google Scholar 

  • Pradella S, Allgaier M, Hoch C, Pauker O, Stackebrandt E, Wagner-Döbler I (2004) Genome organization and localization of the pufLM genes of the photosynthesis reaction center in phylogenetically diverse marine Alphaproteobacteria. Appl Environ Microbiol 70:3360–3369

    Article  PubMed  CAS  Google Scholar 

  • Pujalte MJ, Macian MC, Arahal DR, Ludwig W, Schleifer KH, Garay E (2005) Nereida ignava gen. nov., sp nov., a novel aerobic marine alpha-proteobacterium that is closely related to uncultured Prionitis (alga) gall symbionts. Int J Syst Evol Microbiol 55:631–636

    Article  PubMed  CAS  Google Scholar 

  • Rao D, Webb JS, Kjelleberg S (2005) Competitive interactions in mixed-species biofilms containing the marine bacterium Pseudoalteromonas tunicata. Appl Environ Microbiol 71:1729–1736

    Article  PubMed  CAS  Google Scholar 

  • Ruiz-Ponte C, Cilia V, Lambert C, Nicolas JL (1998) Roseobacter gallaeciensis sp. nov., a new marine bacterium isolated from rearings and collectors of the scallop Pecten maximus. Int J Syst Evol Microbiol 48:537–542

    Article  CAS  Google Scholar 

  • Rusch DB, Halpern AL, Sutton G, Heidelberg KB, Williamson S, Yooseph S, Wu D, Eisen JA, Hoffman JM, Remington K, Beeson K, Tran B, Smith H, Baden-Tillson H, Stewart C, Thorpe J, Freeman J, Andrews-Pfannkoch C, Venter JE, Li K, Kravitz S, Heidelberg JF, Utterback T, Rogers YH, Falcon LI, Souza V, Bonilla-Rosso G, Eguiarte LE, Karl DM, Sathyendranath S, Platt T, Bermingham E, Gallardo V, Tamayo-Castillo G, Ferrari MR, Strausberg RL, Nealson K, Friedman R, Frazier M, Venter JC (2007) The Sorcerer II global ocean sampling expedition: Northwest Atlantic through Eastern Tropical Pacific. PLoS Biol 5:e77

    Article  PubMed  CAS  Google Scholar 

  • Schaefer JK, Goodwin KD, McDonald IR, Murrell JC, Oremland RS (2002) Leisingera methylohalidivorans gen. nov., sp. nov., a marine methylotroph that grows on methyl bromide. Int J Syst Evol Microbiol 52:851–859

    Article  PubMed  CAS  Google Scholar 

  • Schwalbach MS, Fuhrman JA (2005) Wide-ranging abundances of aerobic anoxygenic phototrophic bacteria in the world ocean revealed by epifluorescence microscopy and quantitative PCR. Limnol Oceanogr 50:620–628

    Article  CAS  Google Scholar 

  • Sekiguchi H, Koshikawa H, Hiroki M, Murakami S, Xu K, Watanabe M, Nakahara T, Zhu M, Uchiyama H (2002) Bacterial distribution and phylogenetic diversity in the Changjiang estuary before the construction of the Three Gorges Dam. Microb Ecol 43:82–91

    Article  PubMed  CAS  Google Scholar 

  • Selje N, Simon M, Brinkhoff T (2004) A newly discovered Roseobacter cluster in temperate and polar oceans. Nature 427:445–448

    Article  PubMed  CAS  Google Scholar 

  • Shiba T (1991) Roseobacter litoralis gen-nov, sp-nov, and Roseobacter denitrificans sp-nov, aerobic pink-pigmented bacteria which contain bacteriochlorophyll-a. Syst Appl Microbiol 14: 140–145

    Google Scholar 

  • Shiba T, Simidu U, Taga N (1979) Another aerobic bacterium which contains bacteriochlorophyll a. Bull Jpn Soc Sci Fish 45:801

    Google Scholar 

  • Sorokin DY (1995) Sulfitobacter pontiacus gen-nov, sp-nov—a new heterotrophic bacterium from the Black Sea, specialized on sulfite oxidation. Microbiology 64:295–305

    Google Scholar 

  • Staley JT, Gosink JJ (1999) Poles apart: biodiversity and biogeography of sea ice bacteria. Ann Rev Microbiol 53:198–215

    Article  Google Scholar 

  • Swingley WD, Sadekar S, Mastrian SD, Matthies HJ, Hao J, Ramos H, Acharya CR, Conrad AL, Taylor HL, Dejesa LC, Shah MK, O’Huallachain ME, Lince MT, Blankenship RE, Beatty JT, Touchman JW (2007) The complete genome sequence of Roseobacter denitrificans reveals a mixotrophic rather than photosynthetic metabolism. J Bacteriol 189:683–690

    Article  PubMed  CAS  Google Scholar 

  • Uchino Y, Hirata A, Yokota A, Sugiyama J (1998) Reclassification of marine Agrobacterium species: proposals of Stappia stellulata gen. nov., comb. nov., Stappia aggregata sp. nov., nom. rev., Ruegeria atlantica gen. nov., comb. nov., Ruegeria gelatinovora comb. nov., Ruegeria algicola comb. nov., and Ahrensia kieliense gen. nov., sp. nov., nom. rev. J Gen Appl Microbiol 44:201–210

    Article  PubMed  CAS  Google Scholar 

  • Urbance JW, Bratina BJ, Stoddard SF, Schmidt TM (2001) Taxonomic characterization of Ketogulonigenium vulgare gen. nov., sp. nov. and Ketogulonigenium robustum sp. nov., which oxidize l-sorbose to 2-keto-l-gulonic acid. Int J Syst Evol Microbiol 51:1059–1070

    PubMed  CAS  Google Scholar 

  • Wagner-Döbler I, Biebl H (2006) Environmental biology of the marine Roseobacter lineage. Annu Rev Microbiol 60:255–280

    Article  PubMed  CAS  Google Scholar 

  • Wagner-Döbler I, Rheims H, Felske A, El-Ghezal A, Flade-Schorder D, Laatsch H, Lang S, Pukall R, Tindall BJ (2004) Oceanibulbus indolifex gen. nov., sp nov., a North Sea alphaproteobacterium that produces bioactive metabolites. Int J Syst Evol Microbiol 54:1177–1184

    Article  PubMed  CAS  Google Scholar 

  • Yi H, Lim YW, Chun J (2007) Taxonomic evaluation of the genera Ruegeria and Silicibacter: a proposal to transfer the genus Silicibacter Petursdottir and Kristjansson 1999 to the genus Ruegeria Uchino et al. 1999. Int J Syst Evol Microbiol 57:815–819

    Article  PubMed  CAS  Google Scholar 

  • Ying JY, Wang BJ, Dai X, Yang SS, Liu SJ, Liu ZP (2007) Wenxinia marina gen. nov., sp. nov., a novel member of the Roseobacter clade isolated from oilfield sediments of the South China Sea. Int J Syst Evol Microbiol 57:1711–1716

    Article  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Institute for Chemistry and Biology of the Marine Environment (ICBM), University of Oldenburg, P.O. Box 2503, 26111, Oldenburg, Germany

    Thorsten Brinkhoff, Helge-Ansgar Giebel & Meinhard Simon

Authors
  1. Thorsten Brinkhoff
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Helge-Ansgar Giebel
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Meinhard Simon
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Thorsten Brinkhoff.

Additional information

Communicated by Erko Stackebrandt.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Brinkhoff, T., Giebel, HA. & Simon, M. Diversity, ecology, and genomics of the Roseobacter clade: a short overview. Arch Microbiol 189, 531–539 (2008). https://doi.org/10.1007/s00203-008-0353-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00203-008-0353-y

Keywords

Search

Navigation