Production of antibacterial compounds and biofilm formation by Roseobacter species are influenced by culture conditions

Applied and Environmental Microbiology

Volumn 73, Issue 2, 2007, Pages 442-450

  Bruhn, Jesper Bartholin ^a   Gram, Lone ^a   Belas, Robert ^b  

^a TECHNICAL UNIVERSITY OF DENMARK   (Denmark)

^b UNIVERSITY OF MARYLAND BIOTECHNOLOGY INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALGAE; BACTERIA; BIOFILMS; CELL CULTURE; GROWTH KINETICS; STRAIN;

ANTIBACTERIAL COMPOUNDS; MARINE ALGAE; ROSEOBACTER CLADE; ROSETTE FORMATION;

BIODIVERSITY;

BACTERIAL PROTEIN; POLYPEPTIDE ANTIBIOTIC AGENT;

ALGA; ANTIMICROBIAL ACTIVITY; BIOFILM; DINOFLAGELLATE; GROWTH RATE; MICROBIAL COMMUNITY; PHENOLOGY;

ARTICLE; BACTERIAL COLONIZATION; BACTERIAL FLORA; BACTERIAL GROWTH; BACTERIAL STRAIN; BACTERIUM CULTURE; BIOFILM; CLADISTICS; DINOFLAGELLATE; LIQUID CULTURE; MARINE BACTERIUM; NONHUMAN; PFIESTERIA; PHENOTYPE; ROSEOBACTER; ROSETTE FORMATION; SUPERNATANT;

ANIMALS; ANTI-BACTERIAL AGENTS; BACTERIAL ADHESION; BIOFILMS; CULTURE MEDIA; GENE EXPRESSION REGULATION, BACTERIAL; MICROBIAL SENSITIVITY TESTS; PFIESTERIA PISCICIDA; PIGMENTS, BIOLOGICAL; ROSEOBACTER; SIGNAL TRANSDUCTION; VIBRIO;

ALGAE; BACTERIA (MICROORGANISMS); DINOPHYCEAE; PFIESTERIA PISCICIDA; PHAEOBACTER; ROSEOBACTER; SILICIBACTER;

EID: 33846430909     PISSN: 00992240     EISSN: None     Source Type: Journal    
DOI: 10.1128/AEM.02238-06     Document Type: Article

References (48)

1. Alavi, M., T. Miller, K. Erlandson, R. Schneider, and R. Belas. 2001. Bacterial community associated with Pfiesteria-like dinoflagellate cultures. Environ. Microbiol. 3:380-396.
2. Amaro, A. M., M. S. Fuentes, S. R. Ogalde, J. A. Venegas, and B. A. Suarez-Isla. 2005. Identification and characterization of potentially algallytic marine bacteria strongly associated with the toxic dinoflagellate Alexandrium catenella. J. Eucaryot. Microbiol. 52:191-200.
3. Bainton, N. J., P. Steadm, S. R. Chhabra, B. W. Bycroft, G. P. C. Salmond, G. S. A. B. Stewart, and P. Williams. 1992. N-(3-Oxohexanoyl)-L- homoserine lactone regulates carbapenem antibiotic production in Erwinia carotovora. Biochem. J. 288:997-1004.
4. Ben-Haim, Y., M. Zicherman-Keren, and E. Rosenberg. 2003. Temperature-regulated bleaching and lysis of the coral Pocillopora damicornis by the novel pathogen Vibrio coralliilyticus. Appl. Environ. Microbiol. 69:4236-4242.
5. Bourne, D. G., and C. B. Munn. 2005. Diversity of bacteria associated with the coral Pocillopora damicornis from the Great Barrier Reef. Environ. Microbiol. 7:1162-1174.
6. Brinkhoff, T., G. Bach, T. Heidorn, L. F. Liang, A. Schlingloff, and M. Simon. 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.
7. Bruhn, J. B., J. A. J. Haagensen, D. Bagge-Ravn, and L. Gram. 2006. Culture conditions of Roseobacter strain 27-4 affect its attachment and biofilm formation as quantified by real-time PCR. Appl. Environ. Microbiol. 72:3011-3015.
8. Bruhn, J. B., K. F. Nielsen, M. Hjelm, M. Hansen, J. Bresciani, S. Schulz, and L. Gram. 2005. Ecology, inhibitory activity, and morphogenesis of a marine antagonistic bacterium belonging to the Roseobacter clade. Appl. Environ. Microbiol. 71:7263-7270.
9. Buchan, A., J. M. Gonzalez, and M. A. Moran. 2005. Overview of the marine Roseobacter lineage. Appl. Environ. Microbiol. 71:5665-5677.
10. Cha, C., P. Gao, Y. C. Chen, P. D. Shaw, and S. K. Farrand. 1998. Production of acyl-homoserine lactone quorum-sensing signals by gram-negative plant-associated bacteria. Mol. Plant-Microbe Interact. 11:1119-1129.
11. Dang, H. Y., and C. R. Lovell. 2000. Bacterial primary colonization and early succession on surfaces in marine waters as determined by amplified rRNA gene restriction analysis and sequence analysis of 16S rRNA genes. Appl. Environ. Microbiol. 66:467-475.
12. Gallacher, S., and E. A. Smith. 1999. Bacteria and paralytic shellfish toxins. Protist 150:245-255.
13. Giovannoni, S. J., and U. Stingl. 2005. Molecular diversity and ecology of microbial plankton. Nature 437:343-348.
14. Gonzalez, J. M., J. S. Covert, W. B. Whitman, J. R. Henriksen, F. Mayer, B. Scharf, R. Schmitt, A. Buchan, J. A. Fuhrman, R. P. Kiene, and M. A. Moran. 2003. Silicibacter pomeroyi sp. nov. and Roseovarius nubinhibens sp. nov., dimethylsulfoniopropionate-demethylating bacteria from marine environments. Int. J. Syst. Bacteriol. 53:1261-1269.
15. Gonzalez, J. M., R. Simo, R. Massana, J. S. Covert, E. O. Casamayor, C. Pedros-Alio, and M. A. Moran. 2000. Bacterial community structure associated with a dimethylsulfoniopropionate-producing North Atlantic algal bloom. Appl. Environ. Microbiol. 66:4237-4246.
16. Gram, L., H. P. Grossart, A. Schlingloff, and T. Kiorboe. 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.
17. Grossart, H. P., T. Kiorboe, K. Tang, and H. Ploug. 2003. Bacterial colonization of particles: growth and interactions. Appl. Environ. Microbiol. 69: 3500-3509.
18. Grossart, H. P., F. Levold, M. Allgaier, M. Simon, and T. Brinkhoff. 2005. Marine diatom species harbour distinct bacterial communities. Environ. Microbiol. 7:860-873.
19. Harder, T., S. C. K. Lau, S. Dobretsov, T. K. Fang, and P. Y. Qian. 2003. A distinctive epibiotic bacterial community on the soft coral Dendronephthya sp. and antibacterial activity of coral tissue extracts suggest a chemical mechanism against bacterial epibiosis. FEMS Microb. Ecol. 43:337-347.
20. Hjelm, M., Ø. Bergh, A. Riaza, J. Nielsen, J. Melchiorsen, S. Jensen, H. Duncan, P. Ahrens, H. Birkbech, and L. Gram. 2004. Selection and identification of autochthonous potential probiotic bacteria from turbot larvae (Scophthalmus maximus) rearing units. Syst. Appi. Microbiol. 27:360-371.
21. Jastl, S., M. E. Sieracki, N. J. Poulton, M. W. Giewat, and J. N. Rooney-Varga. 2005. Phylogenetic diversity and specificity of bacteria closely associated with Alexandrium spp. and other phytoplankton. Appl. Environ. Microbiol. 71:3483-3494.
22. Kiorboe, T. 2000. Colonization of marine snow aggregates by invertebrate Zooplankton: abundance, scaling, and possible role. Limnol. Oceanogr. 45: 479-484.
23. Lafay, B., R. Ruimy, C. R. Detraubenberg, V. Breittmayer, M. J. Gauthier, and R. Christen. 1995. Roseobacter algicola sp. nov., a new marine bacterium isolated from the phycosphere of the toxin-producing dinoflagellate Prorocentrum lima. Int. J. Syst. Bacteriol. 45:290-296.
24. Long, R. A., and F. Azam. 2001. Antagonistic interactions among marine pelagic bacteria. Appl. Environ. Microbiol. 67:4975-4983.
25. Long, R. A., D. C. Rowley, E. Zamora, J. Y. Liu, D. H. Bartlett, and F. Azam. 2005. Antagonistic interactions among marine bacteria impede the proliferation of Vibrio cholerae. Appl. Environ. Microbiol. 71:8531-8536.
26. Martens, T., T. Heidorn, R. Pukall, M. Simon, B. J. Tindall, and T. Brinkhoff. 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. 1999 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.
27. Miller, T. R., and R. Belas. 2004. Dimethylsulfoniopropionate metabolism by Pfiesteria-associated Roseobacter spp. Appl. Environ. Microbiol. 70:3383-3391.
28. Miller, T. R., K. Hnilicka, A. Dziedzic, P. Desplats, and R. Belas. 2004. Chemotaxis of Silicibacter sp. strain TM1040 toward dinoflagellate products. Appl. Environ. Microbiol. 70:4692-4701.
29. Moran, M. A., J. M. Gonzalez, and R. P. Kiene. 2003. Linking a bacterial taxon to sulfur cycling in the sea: studies of the marine Roseobacter group. Geomicrobiol. J. 20:375-388.
30. Morris, R. M., M. S. Rappe, S. A. Connon, K. L. Vergin, W. A. Siebold, C. A. Carlson, and S. J. Giovannoni. 2002. SAR11 clade dominates ocean surface bacterioplankton communities. Nature 420:806-810.
31. Nicolas, J. L., S. Corre, and J. C. Cochard. 2004. Bacterial population association with phytoplankton cultured in a bivalve hatchery. Microb. Ecol. 48:400-413.
32. Ploug, H., and H. P. Grossart. 2000. Bacterial growth and grazing on diatom aggregates: respiratory carbon turnover as a function of aggregate size and sinking velocity. Limnol. Oceanogr. 45:1467-1475.
33. Rao, D., J. S. Webb, and S. Kjelleberg. 2005. Competitive interactions in mixed-species biofilms containing the marine bacterium Pseudoalteromonas tunicata. Appl. Environ. Microbiol. 71:1729-1736.
34. Rao, D., J. S. Webb, and S. Kjelleberg. 2006. Microbial colonization and competition on the marine alga Ulva australis. Appl. Environ. Microbiol. 72:5547-5555.
35. Ravn, L., A. B. Christensen, S. Molin, M. Givskov, and L. Gram. 2001. Methods for detecting acylated homoserine lactones produced by gram-negative bacteria and their application in studies of AHL-production kinetics. J. Microbiol. Methods 44:239-251.
36. Rosenberg, E., and L. Falkovitz. 2004. The Vibrio shiloi/Oculina patagonica model system of coral bleaching. Annu. Rev. Microbiol. 58:143-159.
37. Ruger, H. J., and M. G. Hofle. 1992. Marine star-shaped-aggregate- forming bacteria: Agrobacterium atlanticum sp. nov.; Agrobacterium meteori sp. nov.; Agrobacterium ferrugineum sp. nov., nom. rev.; Agrobacterium gelatinovorum sp. nov., nom. rev.; and Agrobacterium stellulatum sp. nov., nom. rev. Int. J. Syst. Bacteriol. 42:133-143.
38. Ruiz-Ponte, C., V. Cilia, C. Lambert, and J. L. Nicolas. 1998. Roseobacter gallaeciensis sp. nov., a new marine bacterium isolated from rearings and collectors of the scallop Pecten maximus. Int. J. Syst. Bacteriol. 48:537-542.
39. Schweitzer, B., I. Huber, R. Amann, W. Ludwig, and M. Simon. 2001. α- and β-Proteobacteria control the consumption and release of amino acids on lake snow aggregates. Appl. Environ. Microbiol. 67:632-645.
40. Selje, N., M. Simon, and T. Brinkhoff. 2004. A newly discovered Roseobacter cluster in temperate and polar oceans. Nature 427:445-448.
41. 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.
42. Throup, J. P., M. Camara, G. S. Briggs, M. K. Winson, S. R. Chhabra, B. W. Bycroft, P. Williams, and G. S. A. B. Stewart. 1995. Characterization of the Yenl/Yenr locus from Yersinia enterocolitica mediating the synthesis of 2 N-acylhomoserine lactone signal molecules. Mol. Microbiol. 17:345-356.
43. Uchino, Y., A. Hirata, A. Yokota, and J. Sugiyama. 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 gelatinovara comb, nov., Ruegeria algicola comb, nov., and Ahrensia kieliense gen. nov., sp. nov., nom. rev. J. Gen. Appl. Microbiol. 44:201-210.
44. Wagner-Döbler, I., and H. Biebl. 2006. Environmental biology of the marine Roseobacter lineage. Annu. Rev. Microbiol. 60:255-280.
45. Wagner-Döbler, I., V. Thiel, L. Eberl, M. Allgaier, A. Bodor, S. Meyer, S. Ebner, A. Hennig, R. Pukall, and S. Schulz. 2005. Discovery of complex mixtures of novel long-chain quorum sensing signals in free-living and host-associated marine alphaproteobacteria. Chembiochem 6:2195-2206.
46. Whitehead, N. A., A. M. L. Barnard, H. Slater, N. J. L. Simpson, and G. P. C. Salmond. 2001. Quorum-sensing in gram-negative bacteria. FEMS Microbiol. Rev. 25:365-404.
47. Wichels, A., C. Hummert, M. Elbrachter, B. Luckas, C. Schutt, and G. Gerdts. 2004. Bacterial diversity in toxic Alexandrium tamarense blooms off the Orkney Isles and the Firth of Forth. Helgol. Mar. Res. 58:93-103.
48. Wood, D. W., and L. S. Pierson III. 1996. The phzI gene of Pseudomonas aureofaciens 30-84 is responsible for the production of a diffusible signal required for phenazine antibiotic production. Gene 168:49-53.