Abstract
Any living or non-living surface immersed in seawaterrapidly acquires a bacterial biofilm. For living marineorganisms, biofilm formation can result in the death ofthe host, and thus there is strong evolutionary pressure formarine eukaryotes to evolve mechanisms which inhibit orcontrol the development of biofilms on their surfaces.Some marine eukaryotes are indeed successful incontrolling biofilms on their surfaces, and in manyinstances this control is achieved by the production ofinhibitory chemicals which act at or near the surface ofthe organism. In some cases these natural inhibitors aresimply toxic to bacteria. However, increasingly it appearsthat at least some of these compounds act by interferingspecifically with bacterial characteristics which effect theability of bacteria to colonize their hosts, such asattachment, surface spreading, or the production ofextracellular macromolecules. As an example, theAustralian seaweed Delisea pulchra appears tocontrol bacterial colonization by interfering with abacterial regulatory system (the acylated homoserinelactone system) that regulates several colonizationrelevant bacterial traits. Understanding how marineorganisms control specific bacterial colonization traitsshould provide us with insights into new technologies forthe control of biofilms on artificial surfaces.
Similar content being viewed by others
References
Alberte RS, Snyder S, Zahuranec BJ & Whetstone M (1992) Biofouling research needs for the United States Navy: Program history and goals. Biofouling 6: 91–95
Allen YC, De-Stasio BT & Ramcharan CW (1994) Individual and population level consequences of an algal epibiont on DaphniaLimnol. Oceanogr. 38 (3): 592–601
Atlas RM & Barta R (1993) Microbial ecology. Third edition. Benjamin/ Cummings Pub.
Angell P & Chamberlain AHL (1991) The role of extracellular products in copper colonization. Int. Biodeterior. 27: 135–143
Austin B & Austin DA (1993) Bacterial fish pathogens: disease in farmed and wild fish. Ellis Horwood, Ltd., Chichester, UK
Barthel D & Wolfrath B (1989) Tissue sloughing in the sponge Halichondria panicea: a fouling organism prevents being fouled. Oecologia 78: 357–360
Becker K & Wahl M (1991) Influence of substratum surface tension on biofouling of artificial substrata in Kiel Bay (Western Baltic): in situstudies. Biofouling 4: 275–291
Belas R, Simon M & Silverman M (1986) Regulation of lateral flagella gene transcription in Vibrio parahaemolyticus. J. Bacteriol. 167: 210–218
Branch GM & Griffiths CL (1988) The Benguela ecosystem. Part V. The coastal zone. Ocean. Mar. Biol. Annu. Review 26: 395–486
Characklis, WG & Marshall KC (1990) Biofilms. John Wiley & Sons Inc., New York.
Chatterjee A, Cui Y, Lui Y, Dumenyo CK & Chatterjee AK (1995) Inactivation of rsmA leads to overproduction of extracellular pectinases, cellulases, and proteases in Erwinia carotovorasubsp. carotovorain the absence of the starvation/cell density-sensing signal, N-(3-oxohexanoyl)-L-homoserine lactone. Appl. Environ. Microbiol. 61: 1959–67
Clare AS (1996) Marine natural product antifoulants: Status and potential. Biofouling 9: 211–229
Coll JC, Price IR, Konig GM & Bowden BF (1987) Algal overgrowth of alcyonacean soft corals. Mar. Biol. 96: 129–135
Correa JA & Sanchez PA (1996) Ecological aspects of algal infectious diseases. Hydrobiologia 326/327: 89–96
Costerton JW & Irvin RT (1981) The bacterial glycocalyx in nature and disease. Ann. Rev. Microbiol. 35: 299–324
Cowan MM & Fletcher M (1987) Rapid screening method for detection of bacterial mutants with altered adhesion abilities. J. Microbiol. Meth. 7: 241–249
Cundell AM, Sleeter TF & Mitchell R (1977) Microbial populations associated with the surface of the brown alga Ascophyllum nodosum. Microbial Ecology 4: 81–91
Dalton HM, Poulsen LK, Halasz P, Angles ML, Goodman AE & Marshall KC (1994) Substratum-induced morphological changes in a marine bacterium and their relevance to biofilm structure. J. Bact. 176: 6900–6906
D'Antonio C (1985) Epiphytes on the rocky intertidal red alga Rhodomela Larix(Turner) C. Agardh: Negative effects on the host and food for herbivores? J. Exp. Mar. Biol. Ecol. 86: 197–218
Davis AR, Targett NM, McConnell OJ & Young CM (1989) Epibiosis of marine algae and benthic invertebrates: natural products chemistry and other mechanisms inhibiting settlement and overgrowth. Bioorg. Mar. Chem. 3: 86–114
De Nys S, Steinberg PD, Rogers CN, Charlton TS & Duncan MW (1996) Quantitative variation of secondary metabolites in the sea hare Aplysia parvulaand its host plant, Delisea pulchra. Mar. Ecol. Prog. Ser. 130: 135–146
De Nys R, Wright AD, Konig GM & Stichter O (1993) New halogenated furanones from the marine alga Delisea pulchra(cf. fimbriata). Tetrahedron 49: 11213–11220
Dexter SC (1993) Role of microfouling organisms in marine corrosion. Biofouling 7: 97–127
Faulkner DJ (1996) Marine natural products. Natural Products Reports 13: 75–125
Filion-Myklebust C & Norton TA (1986) Epidermis shedding in the brown seaweed Ascophyllum nodosum(L.) Le Jolis, and its ecological significance. Mar. Biol. Lett. 2: 45–51
Fuqua CW, Winans CS & Greenberg PE (1994) Quorum sensing in bacteria: the LuxR-LuxI family of cell density-responsive transcriptional regulators. J. Bacteriol. 176: 269–275
Givskov M, De Nys R, Manefield M, Gram L, Maximilien R, Eberl L, Molin S, Steinberg PD & Kjelleberg S (1996) Eukaryotic interference with homoserine lactone mediated procaryotic signalling. J. Bacteriol. 178: 6618–6622
Gil-Turnes MS, Hay ME & Fenical W (1989) Symbiotic marine bacteria chemically defend crustacean embryos from a pathogenic fungus. Science 246: 116–118
Gram L, De Nys R, Givskov M, Steinberg PD & Kjelleberg S. Inhibition of homoserine lactone dependent exoprotease activity and protein expression by furanones from the red alga Delisea pulchra. FEMS Microbiol. Lett., submitted
Hay ME & Fenical W (1988) Marine plant herbivore interactions: the ecology of chemical defense. Ann. Rev. Ecol. Syst. 19: 111–145
Holmström C & Kjelleberg S (1994) The effect of external biological factors on settlement of marine invertebrate larvae and new antifouling technology. Biofouling 8: 147–160
Hornsey IS & Hilde D (1974) The production of antimicrobial compounds by British marine algae. I. Antibiotic producing algae. Br. Phycol. J. 9: 353–361
Hunter KA & Liss PS (1979) The surface charge of suspended particles in estuarine and coastal waters. Nature 282: 823–825
Jann K & Hoschützky H(1990) Nature and organization of adhesins. Curr. Topics Microbiol. Immunol. 151: 55–70
Jennings JG & Steinberg PD (1997) Phlorotanins vs. other factors affecting epiphyte abundance on the kelp Ecklonia radiata. Oecologia 109: 461–473
Johnson CR & Mann K (1986) The crustose coralline alga, PhymatolithonFoslie, inhibits the overgrowth of seaweeds without relying on herbivores. J. Exp. Mar. Biol. Ecol. 96: 127–146
Kell DB, Kaprelyants AS & Grafen A (1995) Pheromones, social behaviour and the functions of secondary metabolism in bacteria. Trends Ecol. Evol. 10: 126–129
Kjelleberg S, Steinberg PD, Givskov M, Gram L, Manefield M, De Nys R (1997) Do marine natural products interfere with prokaryotic AHL regulatory systems? Aq. Microb. Ecol., in press
Kirchman D, Graham S, Reisch D, Mitchell R(1982) Bacteria induce settlement and metamorphosis of Janua (Dexiospira) brasiliensisGrube (Polychaeta: Spirorbidae). J. Exp. Mar. Biol. Ecol. 56: 153–163
Kushmaro A, Rosenberg E, Fine M & Loya Y (1996) Bleaching of the coral Oculina patagonicaby VibrioAK-1. Mar. Ecol.-Prog. Ser. 147: 159–165
Leitz T & Wagner T (1993) The marine bacterium Altermonas epejianainduces metamorphosis of the hydroid Hydractinia echinata. Mar. Biol. 115: 173–178
Lethwaite JC, Molland AF & Thomas KW (1984) An investigation into the variation of ship skin frictional resistance with fouling. Trans. R. Inst. Naval Architects 127: 269–284
Lewandowski Z (1994) Dissolved oxygen gradients nearmicrobially colonized surfaces. In: Geesey G.G., Lewandoswski Z & Flemming H-C (Eds) Biofouling and Biocorrosion in Industrial Water Systems (pp 175–188). Lewis Publishers, Boca Raton, CA
Loosdrecht MCM van, Lyklema J, Norde W & Zehnder AJB (1989) Bacterial adhesion: A physicochemical approach. Microb. Ecol. 17: 1–15
Littler MM & Littler DS (1995) Impact of CLOD pathogen on Pacific coral reefs. Science 267: 1356–1360
Maier I & Muller DG(1986) Sexual pheromones in algae. Biol. Bull. 170: 145–175
Maki JS, Rittschof D, Costlow JD & Mitchell R (1988) Inhibition of attachment of larval barnacles, Balanus amphitrite, by bacterial films. Mar. Biol. 97: 199–206
Mann KH (1973) Seaweeds; their productivity and strategy for growth. Science 182: 975–981
Marshall KC & Goodman AE (1994) Effects of adhesion on microbial cell physiology. Colloids and Surfaces B: Biointerfaces 2: 1–7
Maximilien R (1995) Inhibition of bacteria by seaweed secondary metabolites. BSc Honours Thesis, UNSW, Sydney, Australia
McCaffrey EJ & Endean R (1985) Antimicrobial activity of tropical and subtropical sponges. Mar. Biol. 89: 1–8
McCarter LL, Showalter RE & Silverman MR (1992) Genetic analysis of surface sensing in Vibrio paramaemolyticus. Biofouling 5: 163–175
Neal AL & Yule AB (1994) The interaction between Elminius modestusDarwin cyprid and biofilms of Deleya marinaNCMB1877. J. Exp. Mar. Biol. Ecol. 176: 127–139
Neu TR & Marshall KC (1991) Microbial 'footprints'-a new approach to adhesive polymers. Biofouling 3: 101–112
Novak R (1984) A study in ultra-ecology: microorganisms on the seagrass Posidonia oceanica(L.) Delile. P.S.Z.N. Mar. Ecol. 5: 143–190
Pawlik JR (1992) Chemical ecology of the settlement of benthic marine invertebrates. Oceanogr. Mar. Biol. Ann. Rev. 30: 273–335
Quintero EJ & Weiner RM (1995) Evidence for the adhesive function of the exopolysaccharide of Hyphomonasstrain MHS-3 in its attachment to surfaces. Appl. Env. Microbiol. 61 (5): 1897–1903
Reichelt JL & Borowitzka MA (1984) Antimicrobial activity from marine algae: Results of a large scale screening programme. Hydrobiologia 116/117: 158–168
Rittschof D & Costlow JD (1989) Bryozoan and barnacle settlement in relation to initial surface wettability; a comparison of laboratory and field studies. In: Ros JD (Ed) Topics in Marine Biology (pp 411–416). Proc. 22nd European Mar. Biol. Symp. Instituto de Ciuencias del Mar, Barcelona, Spain
Ruby EG, McFall-Ngai MJ (1992) A squid that glows at night; development of an animal-bacterial mutualism. J. Bacteriol. 174: 4865–4870
Salmond GPC, Golby P, Jones S (1994) Global regulation of Erwinia carotovoravirulence factor production. In: Daniels MJ, Downie JA & Osburn AE (Eds) Advances in Molecular Genetics of Plant-Microbe Interactions (pp 13–20). Kluwer Academic, Boston
Sand-Jensen K (1977) Effects of epiphytes on eelgrass photosynthesis. Aquatic Botany 3: 55–63
Schmitt TM, Hay ME & Lindquist N (1995) Constraints on chemically mediated coevolution: multiple functions for seaweed secondary metabolites. Ecology 76: 107–123
Schneider RP (1996) Conditioning-film induced modification of sub-stratum physicochemistry-an analysis by contact angles. J. Colloid Interface Sci. 182: 204–213
Sieburth JM (1979) Sea microbes. Oxford University Press, New York
Slattery M, McClintock JB & Heine JN (1995) Chemical defenses in Antarctic soft corals evidence for antifouling compounds. J. Exp. Mar. Biol. Ecol. 190: 61–77
Steinberg PD, De Nys R & Kjelleberg S (1997) Chemical inhibition of epibiota by Australian seaweeds. Biofouling, in press
Swift S, Bainton NJ & Winston MK (1994) Gram-negatie bacterial communication by N-acyl homoserine lactones: a universal language? Trends Microbiol. 2: 193–198
Swift S, Throup JP, Williams P, Salmond GPC & Stewart GSAB (1996) Quorum sensing: a population-density component in the determination of bacterial phenotype. TIBS 21: 214–219
Ulitzur S. H-NS protein silences transcription of the luxsystem of Vibrio fischeriand other luminous bacteria cloned in Escherichia coli. Biolum. Chemilum., submitted
Unson MD, Holland ND & Faulkner DJ (1994) A brominated secondary metabolite synthesized by the cyanobacterial symbiont of a marine sponge and accumulation of the crystalline metabolite in the sponge. Marine Biol. 119: 1–11
Wahl M (1989) Marine epibiosis. I. Fouling and antifouling: some basic aspects. Mar. Ecol. Prog. Ser. 58: 175–189-(1995) Bacterial epibiosis on Bahamian and Pacific ascidians. J. Exp. Mar. Biol. Ecol. 191: 239-255-(1996) Living attached: aufwuchs, fouling, epibiosis. In: Nagabhushanam R & Thompson MF (Eds) Fouling Organisms of the Indian Ocean: Biology and Control Technology. Oxford & IBH Pub., New Delhi
Wahl M & Sonnichsen H (1992) Marine epibiosis. IV. The periwinkle Littorina littorealacks typical antifouling defences-why are some populations so little fouled? Mar. Ecol. Prog. Ser. 88: 225–235
Wahl M, Jensen PR, Fenical W (1994) Chemical control of bacterial epibiosis on ascidians. Mar. Ecol. Prog. Ser. 110: 45–57
Walker RP, Thompson JE & Faulkner DJ (1985) Exudation of biologically active metabolites in the sponge Aplysina fistularis, II. Chemical evidence. Marine Biol. 88: 27–32
Wrangstadh M, Conway PL & Kjelleberg S (1989) The role of an extracellular polysaccharide produced by the marine Pseudomonassp. S9 in cellular detachment during starvation. Can. J. Microbiol. 35: 309–312
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Steinberg, P.D., Schneider, R. & Kjelleberg, S. Chemical defenses of seaweeds against microbial colonization. Biodegradation 8, 211–220 (1997). https://doi.org/10.1023/A:1008236901790
Issue Date:
DOI: https://doi.org/10.1023/A:1008236901790