Inhibition of marine biofouling by bacterial quorum sensing inhibitors

Biofouling

Volumn 27, Issue 8, 2011, Pages 893-905

  Dobretsov, Sergey ^a   Teplitski, Max ^b   Bayer, Mirko ^c   Gunasekera, Sarath ^d   Proksch, Peter ^c   Paul, Valerie J ^d  

^a SULTAN QABOOS UNIVERSITY   (Oman)

^b UNIVERSITY OF FLORIDA   (United States)

^c Inst f Pharmazeutische Technologie   (Germany)

^d SMITHSONIAN MARINE STATION   (United States)

Author keywords

Antifouling; Biofilms; Inhibitors; Natural products; Quorum sensing

Indexed keywords

ALGA; ANTIFOULING; BACTERIUM; BIOFILM; BIOFOULING; BIOLUMINESCENCE; CYANOBACTERIUM; FUNGUS; INHIBITION; INHIBITOR; INVERTEBRATE; MARINE ENVIRONMENT; PLANT; TOXICITY;

ALGAE; BACILLARIOPHYTA; BACTERIA (MICROORGANISMS); CHROMOBACTERIUM VIOLACEUM; CYANOBACTERIA; ESCHERICHIA COLI; FUNGI; UROCHORDATA;

ANTINEOPLASTIC ANTIBIOTIC; AZEPINE DERIVATIVE; BIOLOGICAL PRODUCT; HYMENIALDISINE; KOJIC ACID; MICROCOLIN A; MICROCOLIN B; OLIGOPEPTIDE; PIGMENT; PYRONE DERIVATIVE; PYRROLE DERIVATIVE; PYRROLIDINE DERIVATIVE; TENUAZONIC ACID;

ANIMAL; ARTICLE; BIOFOULING; CHROMOBACTERIUM; DRUG EFFECT; METABOLISM; QUORUM SENSING;

ANIMALS; ANTIBIOTICS, ANTINEOPLASTIC; AZEPINES; BIOFOULING; BIOLOGICAL AGENTS; CHROMOBACTERIUM; OLIGOPEPTIDES; PIGMENTS, BIOLOGICAL; PYRONES; PYRROLES; PYRROLIDINES; QUORUM SENSING; TENUAZONIC ACID;

EID: 84855383767     PISSN: 08927014     EISSN: 10292454     Source Type: Journal    
DOI: 10.1080/08927014.2011.609616     Document Type: Article

References (72)

1. Alagely A, Rajamani S, Teplitski M. 2011. Luminescent reporters and their applications for the characterization of signals and signal-mimics that alter LasR-mediated quorum sensing. Methods Mol Biol 692:113-130.
2. Aly AH, Edrada-Ebel RA, Indriani ID, Wray V, Muller WEG, Totzke F, Zirrgiebel U, Schachtele C, Kubbutat MHG, Lin WH, et al. 2008. Cytotoxic metabolites from the fungal endophytic Alternaria sp. and their subsequent detection in its host plant Polygonum senegalense. J Nat Prod 71:972-980.
3. Antunes LC, Ferreira RB, Buckner MM, Finlay BB. 2010. Quorum sensing in bacterial virulence. Microbiology 156:2271-2282.
4. Bayer M. 2009. Naturstoffe aus chinesischen Mangrovenpflanzen - Untersuchung der insektiziden, tumorhemmenden und vor UV-Licht schutzenden Aktivitaten [PhD Dissertation] [Internet]. Dusseldorf University [cited 2011 Aug 4]. Available from: http://docserv.uni-duesseldorf.de/servlets/DerivateServlet/Derivate-11893/Dissertation%20M.Bayer%20PDFA.pdf.
5. Boyer M, Wisniewski-Dye F. 2009. Cell-cell signalling in bacteria: not simply a matter of quorum. FEMS Microbiol Ecol 70:1-19.
6. Burdock GA, Soni MG, Carabin IG. 2001. Evaluation of health aspects of kojic acid in food. Regul Toxicol Pharm 33:80-101.
7. Cabanes J, Chazarra S, Garcia-Carmona F. 1994. Kojic acid, a cosmetic skin whitening agent, is a slow-binding inhibitor of catecholase activity of tyrosinase. J Pharm Pharmacol 46:982-985.
8. Cardellina JH, Marner F-J, Moore RE. 1979. Malyngamide A, a novel chlorinated metabolite of the marine cyanophyte Lyngbya majuscula. J Am Chem Soc 101:240-242.
9. Cardellina JH, Dalietos D, Marner F-J, Mynderse JS, Moore RE. 1978. (-)-trans-7(S)-Methoxytetradec-4-enoic acid and related amides from the marine cyanophyte Lyngbya majuscula. Phytochemistry 17:2091-2095.
10. Casse F, Swain GW. 2006. The development of microfouling on four commercial antifouling coatings under static and dynamic immersion. Int Biodeterior Biodegr 57:179-185.
11. Chernin LS, Winson MK, Thompson JM, Haran S, Bycroft BW, Chet I, Williams P, Stewart GSAB. 1998. Chitinolytic activity in Chromobacterium violaceum: substrate analysis and regulation by quorum sensing. J Bacteriol 180:4435-4441.
12. Choudhary S, Schmidt-Dannert C. 2010. Applications of quorum sensing in biotechnology. Appl Microbiol Biotechnol 86:1267-1279.
13. Debbab A. 2007. Nouveaux composes naturels extraits des champignons endophytiques isoles de plantes medicinales marocaines caracterisation chimique et anticancereuse [PhD thesis] [Internet]. Universite Mohammed V [cited 2011 Aug 4]. Available from: http://toubkal.imist.ma/handle/123456789/1817.
14. Defoirdt T, Boon N, Bossier P, Verstraete W. 2004. Disruption of bacterial quorum sensing: an unexplored strategy to fight infections in aquaculture. Aquaculture 240:69-88.
15. Dickschat JS. 2010. Quorum sensing and bacterial biofilms. Nat Prod Rep 27:343-369.
16. Dobretsov S, Teplitski M, Paul V. 2009. Mini-review: quorum sensing in the marine environment and its relationship to biofouling. Biofouling 25:413-427
17. Dobretsov S, Dahms HU, Yili H, Wahl M, Qian PY. 2007. The effect of quorum-sensing blockers on the formation of marine microbial communities and larval attachment. FEMS Microbiol Ecol 60:177-188.
18. Dobretsov S, Teplitski M, Alagely A, Gunasekera SP, Paul VJ. 2010. Malyngolide from the cyanobacterium Lyngbya majuscula interferes with quorum sensing circuitry. Environ Microbiol Rep 2:739-744.
19. Duong NT. 2006. Isolation and structure elucidation of insecticidal secondary metabolites from Aglaia species collected in Vietnam [PhD dissertation] [Internet]. Dusseldorf University [cited 2011 Aug 4]. Available from: http://docserv.uni-duesseldorf.de/servlets/DerivateServlet/Derivate-3467.
20. Ebel R, Brenzinger M, Kunze A, Gross HJ, Proksch P. 1997. Wound activation of protoxins in the marine sponge Aplysina aerophoba. J Chem Ecol 23:1451-1462.
21. Eder C, Schupp P, Proksch P, Wray V, Steube K, Muller C, van Soest RWM. 1998. Bioactive pyridoacridine alkaloids from the Micronesian sponge Oceanapia sp. J Nat Prod 61:301-305.
22. Edrada RA. 1998. Isolation and structure elucidation of bioactive secondary metabolites from Philippine marine sponges and soft corals [PhD dissertation] [Internet]. Dusseldorf University. [cited 2011 Aug 4]. Available from: http://www.pharmazie.uni-duesseldorf.de/Institute/pharm_bio/arbeitskreise/diss.
23. Fay F, Linossier I, Carteau D, Dheilly A, Silkins A, Vallee-Rehel K. 2010. Booster biocides and microfouling. Biofouling 26:787-798.
24. Fendert T. 2000. Charakterisierung der enzymatischen Abwehrreaktion in Schwammen der Gattung Aplysina undIsolierung von Bromotyrosinalkaloiden aus Aplysina insularis [PhD dissertation] [Internet]. Wurzburg University [cited 2011 Aug 4]. Available from: http://www.opusbayern.de/uni-wuerzburg/volltexte/2002/116/.
25. Gawne B, Wang Y, Hoagland KD, Gretz MR. 1998. Role of bacteria and bacterial exopolymer in the attachment of Achnanthes longipes (Bacillariophyceae). Biofouling 13:137-156.
26. Goecke F, Labes A, Wiese J, Imhoff JF. 2010. Chemical interactions between marine macroalgae and bacteria. Mar Ecol Prog Ser 409:267-300.
27. Gunasekera SP, Ross C, Paul V, Mathew S, Luesch H. 2008. Dragonamides C and D, two linear lipopeptides from the marine cyanobacterium brown Lyngbya polychoroa. J Nat Prod. 71:887-890.
28. Handayani D. 1998. Isolierung und Strukturaufklarung biologisch aktiver Naturstoffe aus marinen Invertebraten Sudos-tasiens [PhD dissertation] [Internet]. Dusseldorf University. [cited 2011 Aug 4]. Available from: http://docserv.uniduesseldorf.de/servlets/DocumentServlet?id1/43153
29. Hassan A. 2007. Novel natural products from endophytic fungi of Egyptian medicinal plants: chemical and biological characterization [PhD dissertation] [Internet]. Dusseldorf University [cited 2011 Aug 4]. Available from: http://docserv.uni-duesseldorf.de/servlets/DerivateServlet/Derivate-5325/AmalHassan_2007.pdf.
30. Hertiani T. 2007. Isolation and structure elucidation of bioactive secondary metabolites from Indonesian marine sponges [PhD dissertation] [Internet]. Dusseldorf University [cited 2011 Aug 4]. Available from: http://docserv.uni-duesseldorf.de/servlets/DerivateServlet/Derivate-5651/Triana%20Hertiani-Dissertation.pdf.
31. Hertiani T, Edrada-Ebel RA, Ortlepp S, van Soest RWM, de Voogd NJ, Wray V, Hentschel U, Kozytska S, Muller WEG, Proksch P. 2010. From anti-fouling to biofilm inhibition: new cytotoxic secondary metabolites from two Indonesian Agelas sponges. Bioorganic Med Chem 18:1297-1311.
32. Hiort J, Maksimenka K, Reichert M, Lin WH, Wray V, Steube K, Schaumann K, Proksch P, Ebel R, Bringmann C. 2004. New natural products from the sponge- derived fungus Asperigillus niger. J Nat Prod 67:1532-1543.
33. Hmelo L, Van Mooy BAS. 2009. Kinetic constraints on acylated homoserine lactone-based quorum sensing in marine environments. Aquatic Microb Ecol 54:127-133.
34. Huber B, Eberl L, Feucht W, Polster J. 2003. Influence of polyphenols on bacterial biofilm formation and quorum- sensing. Z Naturforsch C 58:879-884.
35. Indriani ID. 2008. Biodiversity of marine-derived fungi and identification of their metabolites [PhD dissertation] [Internet]. Dusseldorf University [cited 2011 Aug 4]. Available from: http://docserv.uni-duesseldorf.de/servlets/DocumentServlet?id1/47333.
36. Irie Y, Parsek MR. 2008. Quorum sensing and microbial biofilms. Curr Top Microbiol Immunol 322:67-84.
37. Janssens JCA, Steenackers H, Robijns S, Gellens E, Levin J, Zhao H, Hermans K, De Coster D, Verhoeven TL, Marchal K, et al. 2008. Brominated furanones inhibit biofilm formation by Salmonella enterica serovar typhimurium. Appl Environ Microb 74:6639-6648.
38. Koehn FE, Longley RE, Reed JK. 1992. Microcolin A and B, new imminosuppressive peptides from the blue-green algae Lyngbya majuscula. J Nat Prod 55:613-619.
39. Kjelleberg S, Steinberg P, Givskov M, Gram L, Manefield M, De Nys R. 2001. Do marine natural products interfere with prokaryotic AHL regulatory systems? Aquat Microb Ecol 13:85-93.
40. Kjer J. 2010. New natural products from endophytic fungi from mangrove plants - structure elucidation and biological screening [PhD dissertation] [Internet]. Dusseldorf University [cited 2011 Aug 4]. Available from: http://docserv.uni-duesseldorf.de/servlets/DerivateServlet/Derivate-17938/Dissertation_JuliaKjer.pdf.
41. Kunze A. 1995. Chromene aus Asteraceen als chemischer Fraßschutz gegen herbivore Insekten [PhD dissertation] [Internet]. Dusseldorf University. [cited 2011 Aug 4]. Available from: http://www.pharmazie.uni-duesseldorf.de/Institute/pharm_bio/arbeitskreise/diss
42. Kwan JC, Teplitski M, Gunasekera SP, Paul VJ, Luesch H. 2010. Isolation and biological evaluation of 8-epimalyngamide C from the Floridian marine cyanobacterium Lyngbya majuscula. J Nat Prod 73:463-466.
43. Manefield M, de Nys R, Kumar N, Read R, Givskov M, Steinberg P, Kjelleberg S. 1999. Evidence that halogenated furanones from Delisea pulchra inhibit acylated homoserine lactone (AHL)-mediated gene expression by displacing the AHL signal from its receptor protein. Microbiology 145:283-291.
44. Marquez B, Verdier-Pinard P, Hamel E, Gerwick WH. 1998. Curacin D, an antimitotic agent from the marine cyanobac-terium Lyngbya majuscula. Phytochemistry 49:2387-2389.
45. Martinelli D, Grossmann G, Sequin U, Brandl H, Bachofen R. 2004. Effects of natural and chemically synthesized furanones on quorum sensing in Chromobacterium violaceum. BMC Microbiol 4:25.
46. Maximilien R, de Nys R, Holmstrm C, Gram L, Givskov M, Crass K, Kjelleberg S, Steinberg PD. 1998. Chemical mediation of bacterial surface colonisation by secondary metabolites from the red alga Delisea pulchra. Aquat Microb Ecol 15:233-246.
47. Molino PJ, Campbell E, Wetherbee R. 2009a. Development of the initial diatom microfouling layer on antifouling and fouling-release surfaces in temperate and tropical Australia. Biofouling 25:685-693.
48. Molino PJ, Childs S, Hubbard EMR, Carey JM, Burgman MA, Wetherbee R. 2009b. Development of the primary bacterial microfouling layer on antifouling and fouling release coatings in temperate and tropical environments in Eastern Australia. Biofouling 25:149-162.
49. Moustafa E. 2009. Insecticidal plant constituents - isolation, structure elucidation, and biological testing [PhD dissertation] [Internet]. Dusseldorf University [cited 2011 Aug 4]. Available from: http://docserv.uni-duesseldorf.de/servlets/DerivateServlet/Derivate-3467/1467.pdf.
50. Muh U, Schuster M, Heim R, Singh A, Olson ER, Greenberg EP. 2006. Novel Pseudomonas aeruginosa quorum-sensing inhibitors identified in an ultra-high- throughput screening. Antimicrob Agents Chemother 50:3674-3679.
51. Ni N, Li M, Wang J, Wang B. 2009. Inhibitors and antagonists of bacterial quorum sensing. Med Res Rev 29:65-124.
52. Ortlepp S, Sjogren M, Dahlstrom M, Weber H, Ebel R, Edrada R, Thoms C, Shupp P, Bohlin L, Proksch P. 2007. Antifouling activity of bromotyrosine-derived sponge metabolites and synthetic analogues. Mar Biotech 9:776-785.
53. Proksch P, Rodriguez E. 1982. High performance liquid chromatography of chromenes and benzofurans from the genus Encelia. J Chromatogr 240:543-546.
54. Putz A. 2009. Secondary metabolites from marine sponges, with focus on the chemical ecology and biochemical characterisation of the stress induced biotransformation of Aplysina alkaloids [PhD dissertation] [Internet]. Dusseldorf University [cited 2011 Aug 4]. Available from: http://docserv.uni-duesseldorf.de/servlets/DerivateServlet/Derivate-11835/Annika%20Putz.pdf.
55. Qian PY, Xu Y, Fusetani N. 2010. Natural products as antifouling compounds: recent progress and future perspectives. Biofouling 26:223-234.
56. Queiroz KCS, Medeiros VP, Queiroz LS, Abreu LRD, Rocha HAO, Ferreira CV, Juca MB, Aoyama H, Leite EL. 2008. Inhibition of reverse transcriptase activity of HIV by polysaccharides of brown algae. Biomed Pharmacother 62:303-307.
57. Rusman Y. 2006. Isolation of new secondary metabolites from sponge-associated and plant-derived endophytic fungi [PhD dissertation] [Internet]. Dusseldorf University. [cited 2011 Aug 4]. Available from: http://deposit.ddb.de/cgi-bin/dokserv?idn1/4983305986&dok_var1/4d1&dok_ext1/4pdf&filename1/4983305986.pdf
58. Schultz MP, Bendick JA, Holm ER, Hertel WM. 2010. Economic impact of biofouling on a naval surface ship. Biofouling 27:87-98.
59. Singh BN, Singh BR, Singh RL, Prakash D, Sarma BK, Singh HB. 2009a. Antioxidant and anti-quorum sensing activities of green pod of Acacia nilotica L. Food Chem Toxicol 47:778-786.
60. Singh BN, Singh BR, Singh RL, Prakash D, Dhakarey R, Upadhyay G, Singh HB. 2009b. Oxidative DNA damage protective activity, antioxidant and anti-quorum sensing potentials of Moringa oleifera. Food Chem Toxicol 47:1109-1116.
61. Skindersoe ME, Ettinger-Epstein P, Rasmussen TB, Bjarnsholt T, De Nys R, Givskov M. 2008a. Quorum sensing antagonism from marine organisms. Mar Biotech 10:56-63.
62. Skindersoe ME, Alhede M, Phipps R, Yang L, Jensen PO, Rasmussen TB, Bjarnsholt T, Tolker-Nielsen T, Hoiby N, Givskov M. 2008b. Effects of antibiotics on quorum sensing in Pseudomonas aeruginosa. Antimicrob Agents Chemother 52:3648-3663.
63. Soulere L, Sabbah M, Fontaine F, Queneau Y, Doutheau A. 2010. LuxR-dependent quorum sensing: computer aided discovery of new inhibitors structurally unrelated to Nacylhomoserine lactones. Bioorg Med Chem Lett 20:4355-4358.
64. Supriyono A, Schwarz B, Wray V, Witte L, Muller WEG, van Soest RWM, Sumaryono W, Proksch P. 1995. Bioactive alkaloids from the tropical marine sponge Axinella carteri. Z Naturforsch 50c:669-674.
65. Waters CM, Bassler BL. 2005. Quorum sensing: cell-to-cell communication in bacteria. Ann Rev Cell Devel Biol 21:319-346.
66. Weber N. 2007. Antioxidative Polyphenole chinesischer Leguminosen und weiterer chinesischer Gemuse [PhD dissertation] [Internet]. Dusseldorf University [cited 2011 Aug 4]. Available from: http://docserv.uni-duesseldorf.de/servlets/DerivateServlet/Derivate-5676/NadineWeber.pdf.
67. Wigglesworth-Cooksey B, Cooksey KE. 2005. Use of fluorophore-conjugated lectins to study cell-cell interactions in model marine biofilms. Appl Environ Microbiol 71:428-435.
68. Williams PG, Moore RE, Paul VJ. 2003. Isolation and structure determination of Lyngbyastatin 3, a Lyngbyastatin 1 homologue from the marine cyanobacterium Lyngbya majuscula. Determination of the configuration of the 4-amino-2,2-dimethyl-3-oxopentanoic acid unit in Majusculamide C, Dolastatin 12, Lyngbyastatin 1, and Lyngbyastatin 3 from cyanobacteria. J Nat Prod 66:1356-1363.
69. Winson MK, Swift S, Fish L, Throup JP, Jorgensen F, Chhabra SR, Bycroft BW, Williams P, Stewart GS. 1998. Construction and analysis of luxCDABE-based plasmid sensors for investigating N-acyl homoserine lactone- mediated quorum sensing. FEMS Microbiol Lett 163:185-192.
70. Xiong Y, Liu Y. 2010. Biological control of microbial attachment: a promising alternative for mitigating membrane biofouling. Appl Microbiol Biotechnol 86:825-837.
71. Yebra DM, Kiil S, Weinell CE, Dam-Johansen K. 2006. Effects of marine microbial biofilms on the biocide release rate from antifouling paints - a model-based analysis. Prog Org Coat 57:56-66.
72. Zar JH. 1996. Biostatistical analysis. Upper Saddle River (NJ): Prentice Hall International, Inc. 662 pp.