Abstract
The ability of polar (1:1 water/methanol) and non-polar (dichloromethane) extracts of macroalgae from Arraial do Cabo, RJ, Brazil, to inhibit quorum sensing (QS) was investigated. Before extraction, half of the algae were treated with 30% ethanol to kill and remove surface-associated bacteria. Twenty of 22 polar extracts inhibited the QS of the acyl homoserine lactone (AHL) producer and reporter Chromobacterium violaceum CV017 with minimal inhibitory concentrations (MIC) ranging from 0.28 μg ml-1 (Ulvafasciata) to 189 μg ml-1 (Codium sp.). The MIC of non-polar extracts varied from 69 μg ml-1 (Sargassum furcatum) to 2730 μg ml-1 (Peyssonnelia capensis). Usually, extracts from algae with associated bacteria had a higher bioactivity than ones without them. Among 11 algal species tested, 50% of extracts with associated bacteria were toxic to C. violaceum CV026. None of the extracts contained AHLs, which was shown using reporters C. violaceum CV026 and Agrobacterium tumefaciens NTL4 (pZLR4). Polar (11%) and non-polar extracts (2%) inhibited QS-dependent attachment of Pseudomonas aeruginosa PA01 at tissue-level concentrations. Our data suggest that secondary metabolites from algae and their associated microbiota are an important source of QS inhibitors, which potentially can be used in future biotechnological applications.
Acknowledgments
The authors thank Dr. Maria Helena Neves Baeta (Marine Biotechnology Division/IEAPM) for help in analyses of epifluorescence microscopy. We are also grateful to Dr. William Romao from Chemistry Division of IEAPM for all assistance. This research was supported by the “Ciências sem Fronteiras” program of Conselho Nacional de Desenvolvimento Científico e Tecnológico-CNPq for collaborative research with SD. SD acknowledges HM Sultan Qaboos Research Trust Fund SR/AGR/FISH/10/01 and SQU internal grant IG/AGR/FISH/12/01. DB acknowledges CNPq-PDJ for their support of her postdoctoral grant.
References
Abarzua, S. and S. Jakubowski. 1995. Biotechnological investigation for the prevention of biofouling. I. Biological and biochemical principles for the prevention of biofouling. Mar. Ecol. Prog. Ser.123: 301–312.10.3354/meps123301Search in Google Scholar
Bhadury, P. and P.C. Wright. 2004. Exploitation of marine algae: biogenic compounds for potential antifouling applications. Planta219: 561–578.10.1007/s00425-004-1307-5Search in Google Scholar
Bigatti, G., M.A. Primosti, M. Clédon, A. Averjub, N. Theobald, W. Gerwinsk, W. Arntz, E. Moriconi and P.E. Penchaszadeh. 2009. Biomonitoring of TBT contamination and imposex incidence along 4700 km of Argentinean shoreline (SW Atlantic: from 38S to 54S). Mar. Pol. Bull.58: 695–701.10.1016/j.marpolbul.2009.01.001Search in Google Scholar
Borchardt, S.A., E.J. Allian, J.J. Michels, G.W. Stearns, R.F. Kelly and W.F. McCoy. 2001. Reaction of acylated homoserine lactone bacterial signaling molecules with oxidized halogen antimicrobials. Appl. Environ. Microbiol. 67: 3174–3179.10.1128/AEM.67.7.3174-3179.2001Search in Google Scholar
Bosgelmez-Tinaz, G., S. Ulusoy, A. Ugur and O. Ceylan. 2007. Inhibition of quorum sensing-regulated behaviors by Scorzonera sandrasica. Curr. Microbiol. 55: 114–118.10.1007/s00284-006-0624-2Search in Google Scholar
Burgess, J.G., E.M. Jordan, M. Bregu, A. Mearns-Spragg and K.G. Boyd. 1999. Microbial antagonism: a neglected avenue of natural products research. J. Biotechnol. 70: 27–32.10.1016/S0079-6352(99)80094-0Search in Google Scholar
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: 1119–1129.10.1094/MPMI.1998.11.11.1119Search in Google Scholar PubMed
Chambers, L.D., K.R. Stokes, F.C. Walsh and R.J.K. Wood. 2006. Modern approaches to marine antifouling coatings. Surf. Coat. Tech. 201: 3642–3652.10.1016/j.surfcoat.2006.08.129Search in Google Scholar
Chernin, L.S., M.K. Winson, J.M. Thompson, S. Haran, B.W. Bycroft and I. Chet. 1998. Chitinolytic activity in Chromobacterium violaceum: substrate analysis and regulation by quorum sensing. J. Bacteriol. 180: 4435–4441.10.1128/JB.180.17.4435-4441.1998Search in Google Scholar PubMed PubMed Central
Davies, D.G., M.R. Parsek, J.P. Pearson, B.H. Iglewski, J.W. Costerton and E.P. Greenberg. 1998. The involvement of cell-to-cell signals in the development of a bacterial biofilm. Science280: 295–298.10.1126/science.280.5361.295Search in Google Scholar PubMed
de Nys, R. and P.D. Steinberg. 2002. Linking marine biology and biotechnology. Curr. Opin. Biotechnol.13: 244–248.10.1016/S0958-1669(02)00311-7Search in Google Scholar
Dobretsov, S. and P.Y. Qian. 2002. Effect of bacteria associated with the green alga Ulva reticulata on marine micro- and macrofouling. Biofouling18: 217–228.10.1080/08927010290013026Search in Google Scholar
Dobretsov, S., H.U. Dahms and P.Y. Qian. 2006. Inhibition of biofouling by marine microorganisms and their metabolites. Biofouling22: 43–54.10.1080/08927010500504784Search in Google Scholar PubMed
Dobretsov, S., M. Teplitski and V.J. Paul. 2009. Mini-review: quorum sensing in the marine environment and its relationship to biofouling. Biofouling25: 413–427.10.1080/08927010902853516Search in Google Scholar PubMed
Dobretsov, S., M. Teplitski, A. Alagely, S.P. Gunasekera and V.J. Paul. 2010. Malyngolide from the cyanobacterium Lyngbya majuscula interferes with quorum sensing circuitrye. Environ. Microbiol. Rep.2: 739–744.10.1111/j.1758-2229.2010.00169.xSearch in Google Scholar PubMed
Dobretsov, S., M. Teplitski, M. Bayer, S. Gunasekera, P. Proksch and V. Paul. 2011. Inhibition of marine biofouling by bacterial quorum sensing inhibitors. Biofouling27: 893–905.10.1080/08927014.2011.609616Search in Google Scholar PubMed PubMed Central
Dobretsov, S., R.M. Abed and M. Teplitski. 2013. Mini-review: inhibition of biofouling by marine microorganisms. Biofouling29: 423–441.10.1080/08927014.2013.776042Search in Google Scholar PubMed
Givskov, M., R. de Nys, M. Manefield, L. Gram, R. Maximilien and L. Eberl. 1996. Eukaryotic interference with homoserine lactone-mediated prokaryotic signaling. J. Bacteriol. 178: 6618–6622.10.1128/jb.178.22.6618-6622.1996Search in Google Scholar PubMed PubMed Central
Goecke, F., A. Labes, J. Wiese and J.F. Imhoff. 2010. Chemical interactions between marine macroalgae and bacteria. Mar. Ecol. Prog. Ser. 409: 267–300.10.3354/meps08607Search in Google Scholar
Gollasch, S. 2002. The importance of ship hull fouling as a vector of species introductions into the North Sea. Biofouling18: 105–121.10.1080/08927010290011361Search in Google Scholar
Hellio, C., D.L. Broise, L. Dufossé, Y.L. Gal and N. Bourgougnon. 2001. Inhibition of marine bacteria by extracts of macroalgae: potential use for environmentally friendly antifouling paints. Mar. Environ. Res. 52: 231–247.10.1016/S0141-1136(01)00092-7Search in Google Scholar
Holm, E.R. 2012. Barnacles and biofouling. Integr. Comp. Biol.52: 348–355.10.1093/icb/ics042Search in Google Scholar PubMed
Jha, B., K. Kavita, J. Westphal, A. Hartmann and P. Schmitt-Kopplin. 2013. Quorum sensing inhibition by Asparagopsis taxiformis, a marine macro alga: separation of the compound that interrupts bacterial communication. Mar. Drugs11: 253–265.Search in Google Scholar
Joint, I., K. Tait and G. Wheeler. 2007. Cross-kingdom signalling: exploitation of bacterial quorum sensing molecules by the green seaweed Ulva. Philos. Trans. R. Soc. Lond. B. 362: 1223–1233.10.1098/rstb.2007.2047Search in Google Scholar PubMed PubMed Central
Kanagasabhapathy, M., G. Yamazaki, A. Ishida, H. Sasaki and S. Nagata. 2009. Presence of quorum-sensing inhibitor-like compounds from bacteria isolated from the brown alga Colpomenia sinuosa. Lett. Appl. Microbiol. 49: 573–579.10.1111/j.1472-765X.2009.02712.xSearch in Google Scholar PubMed
Kientz, B., M. Thabard, S. M. Cragg, J. Pope and C. Hellio. 2011. A new method for removing microflora from macroalgal surfaces: an important step for natural product discovery. Bot. Mar. 54: 2655–2661.10.1515/BOT.2011.053Search in Google Scholar
Kievit, T.R.D., R. Gillis, S. Marx, C. Brown and B.H. Iglewski. 2001. Quorum-sensing genes in Pseudomonas aeruginosa biofilms: their role and expression patterns. Appl. Environ. Microbiol.67: 1865–1873.10.1128/AEM.67.4.1865-1873.2001Search in Google Scholar PubMed PubMed Central
Kim, J.S., Y.H. Kim, Y.W. Seo and S. Park. 2007. Quorum sensing inhibitors from the red alga, Ahnfeltiopsis flabelliformis. Biotechnol. Bioprocess. Eng. 12: 308–311.Search in Google Scholar
Lejars, M., A. Margaillan and C. Bressy. 2012. Fouling release coatings: a nontoxic alternative to biocidal antifouling coatings. Chem. Rev. 112: 4347–4390.10.1021/cr200350vSearch in Google Scholar PubMed
Manefield, M., R. Nys, N. Kumar, R. Read, M. Givskov and P. Steinberg. 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. Microbiology145: 283–291.10.1099/13500872-145-2-283Search in Google Scholar PubMed
Manefield, M., T.B. Rasmussen, M. Henzter, J.B. Andersen, P. Steinberg, S. Kjelleberg and M. Givskov. 2002. Halogenated furanones inhibit quorum sensing through accelerated LuxR turnover. Microbiology148: 1119–1127.10.1099/00221287-148-4-1119Search in Google Scholar PubMed
Penesyan, A., Z. Marshall-Jones, C. Holmstrom, S. Kjelleberg and S. Egan. 2009. Antimicrobial activity observed among cultured epiphytic bacteria reflects their potential as source of new drugs. Microbiol. Ecol. 69: 113–124.10.1111/j.1574-6941.2009.00688.xSearch in Google Scholar PubMed
Qian, P.Y., Y. Xu and N. Fusetani. 2010. Natural products as antifouling compounds: recent progress and future perspectives. Biofouling26: 223–234.10.1080/08927010903470815Search in Google Scholar
Rittschof, D. 2001. Natural product antifoulants and coatings development. In: (J.B. McClintock and B.J. Baker, eds) Marine chemical ecology. CRC Press, Boca Raton, FL. pp. 543–566.Search in Google Scholar
Robson, N.D., A.R.J. Cox, S.J. McGowan, B.W. Bycroft and G.P. Salmond. 1997. Bacterial N-acylhomoserine lactone-dependent signaling and its potential bio-technological applications. Trends Biotechnol. 15: 458–46420.10.1016/S0167-7799(97)01102-5Search in Google Scholar
Salmond, G.P.C., B.W. Bycroft, G.S.A.B. Stewart and P. Williams. 1995. The bacterial ‘enigma’: cracking the code of cell-cell communication. Mol. Microbiol. 16: 615–624.10.1111/j.1365-2958.1995.tb02424.xSearch in Google Scholar
Scardino, A.J. and R. de Nys. 2011. Mini review: biomimetic models and bioinspired surfaces for fouling control. Biofouling27: 73–86.10.1080/08927014.2010.536837Search in Google Scholar
Schultz, M.P., J.A. Bendick, E.R. Holm and W.M. Hertel. 2011. Economic impact of biofouling on a naval surface ship. Biofouling27: 87–98.10.1080/08927014.2010.542809Search in Google Scholar
Skindersoe, M.E., P. Ettinger-Epstein, T.B. Rasmussen, T. Bjarnsholt, R. de Nys and M. Givskov. 2008. Quorum sensing antagonism from marine organisms. Mar. Biotechnol. 10: 56–63.10.1007/s10126-007-9036-ySearch in Google Scholar
Swift, S., J.A. Downie, N.A. Whitehead, A.M.L. Barnard, G.P.C. Salmond and P. Williams. 2001. Quorum sensing as a population-density-dependent determinant of bacterial physiology. Adv. Microb. Physiol. 45: 199–270.10.1016/S0065-2911(01)45005-3Search in Google Scholar
Tait, K., I. Joint, M. Daykin, D.L. Milton, P. Williams and M. Cámara. 2005. Disruption of quorum sensing in seawater abolishes attraction of zoospores of the green alga Ulva to bacterial biofilms. Environ. Microbiol. 7: 229–240.10.1111/j.1462-2920.2004.00706.xSearch in Google Scholar PubMed
Thabard, M., G.I. Daoud, B. Véron, R.L. Fletcher and C. Hellio. 2009. Screening of biological activities of extracts of Ralfsia verrucosa, Petalonia fasciaand Scytosiphon lomentaria (Phaeophyceae, Scytosiphonales) for potential antifouling application. Electronic J. Nat. Subs. 4:1–10.Search in Google Scholar
Waters, C.M. and B.L. Bassler. 2005. Quorum sensing: cell-to-cell communication in bacteria. Annu. Rev. Cell. Dev. Biol. 21: 319–346.10.1146/annurev.cellbio.21.012704.131001Search in Google Scholar PubMed
Xiong, Y. and Y. Liu. 2010. Biological control of microbial attachment: a promising alternative for mitigating membrane biofouling. Appl. Microbiol. Biotechnol. 86: 825–837.10.1007/s00253-010-2463-0Search in Google Scholar PubMed
Yan, L., K.G. Boyd and J.G. Burgess. 2009. Surface attachment induced production of antimicrobial compounds by marine epiphytic bacteria using modified roller bottle cultivation. Mar. Biotechnol. 4: 356–366.10.1007/s10126-002-0041-xSearch in Google Scholar PubMed
Yebra, D.M., S. Kiil and K. Dam-Johansen. 2004. Antifouling technology-past, present and future steps towards efficient and environmentally friendly antifouling coatings. Prog. Org. Coat.50: 75–104.Search in Google Scholar
©2014 by De Gruyter
