Mini-review: Inhibition of biofouling by marine microorganisms

Figures & data

Table 1. Antimicrobial activity of marine heterotrophic bacteria.

Bacteria	Effective against	Source (host)	Location	Inhibitive compound	Reference
92 Isolates	Environmental and pathogenic bacteria	Nine species of red algae	India, Indian Ocean	NI	Kanagasabhapathy and Nagata (2008)
210 Isolates belonging to α-, β-, γ-proteobacteria, Firmicutes, Actinobacteria and Bacteriodetes	Pathogens	Laminaria saccharina	Germany, North Sea	NI	Wiese et al. (2009)
325 Isolates most belonged to α- and γ-proteobacteria	Pathogens	Algae Ulva australis and Delisea pulchra	Australia, Pacific Ocean	NI	Penesyan et al. (2009)
Pseudovibrio sp. D323	Environmental bacteria	D. pulchra	Australia, Pacific Ocean	Tropodithietic acid	Penesyan et al. (2011)
10 Bacterial isolates	Environmental bacteria	Ulva lactuca	Fiji, South Pacific Ocean	NI	Kumar et al. (2011)
Shewanella irciniae, Roseivirga spongocola, Gillisia myxillae, Fabibacter halotolarans, Microbulbifer mediterranus, Stenothermonacter spongiae, Winogradskyella poriferorum	Environmental bacteria	Lissodendoryx isodictyalis	Caribbean, Atlantic Ocean	NI	Dash et al. (2009)
75 Isolates	Environmental bacteria	Sponges Anoxycalyx joubini and Lissodendoryx nobilis	Antarctica	NI	Mangano et al. (2009)
52 Isolates	Pathogens	Haliclona simulans	Ireland, North Sea	NI	Kennedy et al. (2009)
Bacillus licheniformis	Pathogens	Halichondria sp.	India, Indian Ocean	Indole, 3-phenylpropionic acid, 4,4′-oxybis[3-phenylpropionic acid]	Devi et al. (2010)
105 Isolates	Environmental and pathogenic bacteria	14 Invertebrates: sea urchins, brittle stars, tunicates, oysters, seaweed	Australia, Pacific Ocean	NI	Wilson et al. (2011)
Pseudoalteromonas haloplanktis	Environmental and pathogenic bacteria	Scallop hatchery	Chili, Pacific Ocean	Isovaleric acid (3-methylbutanoic acid) and 2-methylbutyric acid (2-methylbutanoic acid)	Hayashiga-Soiza et al. (2008)
14 Roseobacter bacteria	Environmental bacteria	Pfiesteria piscicida and seawater	Denmark, North Sea	NI	Bruhn et al. (2007)
90 Actinomyces spp.	Pathogens	11 Sponge species	Egypt, Red Sea	NI	Abdelmohsen et al. (2010)
20 Isolates	Pathogens	9 Sponge species	Brazil, Atlantic Ocean	NI	Santos et al. (2010)
2562 Isolates	Pathogens	10 Sponge species	Germany, North Sea	NI	Muscholl-Silberhorn et al. (2008)
36 Bacteria	Pathogens	Antipathes dichotoma	China, South China Sea	NI	Zhang et al. (2012a)
340 Isolates	Pathogens	14 Bryozoan species	Baltic, Mediterranean Seas	NI	Heindl et al. (2010)
28 Isolates	Pathogens	Balanus amphitrite	India, Indian Ocean	NI	Jebasingh and Murugan (2011)
78 Isolates	Pathogens	9 Species of corals	Israel, Red Sea	Evidence of cell bound proteinaceous compounds	Shnit-Orland and Kushmaro (2009)
1138 Bacteria	Pathogens	5 Species of corals	Taiwan, South China Sea	NI	Chen et al. (2012)
519 Bacteria	Pathogens	Seawater and surface of organisms	Global waters	Tropodithietic acid	Gram et al. (2010)
101 Strains of Pseudoalteromonas	Pathogens	Seawater and surface of organisms	Global waters	NI	Vynne et al. (2011)
110 Bacteria	Environmental bacteria	Seawater	Denmark, North Sea	NI	Bernbom et al. (2011)
Shewanella oneidensis SCH0402	Environmental bacteria	Seawater	Korea, South Sea	Cis-9-oleic acid	Bhattarai et al. (2007)
Pseudoalteromonas sp. 3J6	Environmental bacteria and pathogens	Seawater	France, Morbihan Gulf	NI	Dheilly et al. (2010)
Bacillus mojavensis, B. firmus	Environmental bacteria	Turtle grass and limestone	Mexico, Atlantic Ocean	Surfacin A, mycosubtilin, bacillomycin D	Ortega-Morales et al. (2008)
Pseudomonas rhizosphaerae	Environmental bacteria	Deep sea sediments	Pacific Ocean	Cyclo(Tyr-Pro), cyclo(Tyr-Ile), cyclo(Phe-Pro), cyclo(Val-Pro)3-phenyl-2-propenoic acid, uracil acid	Qi, Xu, Gao et al. (2009)
Note: NI = compound has not been identified.

Table 2. Antimicrobial compounds from cyanobacteria.

Species of cyanobacteria	Effective against	Source (host)	Location	Inhibitive compound	Reference
Family Oscillatoriaceae
Lyngbya majuscula	Mycobacterium tuberculosis	Seawater	Guam, Pacific Ocean	Depsipepetides (ie pitipeptolides A–F)	Montaser et al. (2011)
L. majuscula	Escherichia coli, Bacillus subtilis, B. cereus, Staphylococcus epidermis	Culture collection	India	Methanol extract	Kaushik et al. (2009)
Family Nostocaceae
Anabaena constricta	B. cereus, Arthrospira laxissima, Nostoc carneum, Chroococcus minutus, and Synechosystis aquatilis	Seawater	Kuwait, Persian Gulf	6-Bromo-3hydroxy-methyl-indole-2-one	Volk et al. (2009)
Nodularia harveyana and Nostoc insulare	E. coli, P. aeruginosa, S. aureus and B. subtilis, Arthrospira laxissima	Seawater	Germany, Baltic Sea	Norharmane (9H-pyrido(3,4-b)indole) and 4,4’-dihydroxybiphenyl	Volk and Furkert (2006)
Family Chroococcaceae
Synechocystis spp., Synechococcus spp.	Gram-positive bacteria	Rocky shores	Portugal, Atlantic Ocean	Dichloromethane extracts	Martins et al. (2008)

Table 3. Antifouling activity of marine fungi.

Fungal strain	Effective against	Source (host)	Location (country)	Inhibitive compound	Reference
Eurotiales Hypocreales Pleosporales Botryosphaeriales	Pathogenic microbes	Antipathes dichotoma	China	NI	Zhang et al. (2012a)
18 Fungal isolates	Pathogenic microbes	Echinogorgia rebekka	China	NI	Wang et al. (2011)
121 Isolates belonging to 20 genera	Environmental and pathogenic bacteria	6 Gorgonian corals	China	NI	Zhang et al. (2012b)
Aspergillus sp.	Environmental bacterial strains	Xestospongia testudinaria	China	Aspergiterpenoid A, (-)-sydonol, (-)-sydonic acid, and (-)-5-(hydroxymethyl)-2-(2′,6′,6′-trimethyltetrahydro-2H-pyran-2-yl)phenol	Li et al. (2012)
Cladosporium sp. F14	Environmental bacteria and Bugula neritina	Seawater	China	3-phenyl-2propenoic acid, cyclo(Phe-Pro), cyclo(Val-Pro), bis(2-ethylhexyl)phthalate	Xiong et al. (2009); Qi, Xu, Xiong et al. (2009)
Ampelomyces sp.	Environmental bacteria, Balanus amphitrite and Hydroides elegans	Seawater	China	3-chloro-2,5-dihydroxybenzyl alcohol	Kwong et al. (2006)
Cochliobolus lunatus	The B. amphitrite	Dichotella gemmmacea	China	14 New resorcylic acid lactones	Shao, Wang (2011)
Aspergillus sp.	B. amphitrite	D. gemmmacea	China	Aspergilones A	Shao, Wu (2011)
Penicillium sp. OUCMDZ-776	Bugula neritina	Hypersaline sediments	China	Penispirolloid A	He et al. (2012)
Note: Fungal strains are classified by their activity against bacteria and invertebrate larvae. NI = compound has not been identified.

Table 4. Inhibition of the settlement of algal spores and diatoms by marine heterotrophic bacteria.

Bacteria	Effective against	Source (host)	Location	Inhibitive compound	References	Comments
10 Bacterial isolates	Cylindrotheca fusiformis	Ulva lactuca	South Pacific Ocean, Fiji	NI	Kumar et al. (2011)	Species specific anti-diatom and anti-bacterial activity
Alteromonas sp.	Eight benthic diatoms and spores of Ulva sp.	Water column	South Pacific, Chile	Theromostable hydrophilic peptide	Silva-Aciares et al. (2008)
Leucothrix mucor	Navicula annexa and spores of Ulva pertusa	Seawater	South Sea, Korea	17-(1,2-Dihydroxyl-5-methyl-hexane)-2,3-dihydroxyl-cholest-4-en-6-one [compound and 13-acetate-17-(1,5-dimethylhexane)-cholest-7-en-3,5,6,15-tetraol	Cho (2012)
Shewanella oneidensis SCH0402	Spores of Ulva pertusa; barnacles; mussels	Seawater	Yellow Sea, Korea	2-Hydroxymyristic acid and cis-9-oleic acid	Bhattarai et al. (2007)	Field experiments showed good AF effect after 1.5 years
22 Bacterial isolates	Spores of Ulva sp.	Water column	Baltic Sea	NI	Bernbom et al. (2011)	Strongest activity among Pseudoalteromonas strains
Pseudoalteromonas haloplanktis CI4	Spores of U. pertusa	Seawater	South China Sea	Heat sensitive 3–10 kDa, not protein	Ma et al. (2010)
Pseudoalteromonas tunicata and Phaeobacter sp. strain 2.10	Polysiphonia sp.	Ulva australis	Pacific Ocean	NI	Rao et al. (2007)
Note: Bacterial strains are classified by their activity. NI = compound has not been identified.

Table 5. Inhibition of the settlement of invertebrate larvae by marine bacteria.

Bacteria	Effective against	Source (host)	Location	Inhibitive compound	Reference	Comments
Heterotrophic bacteria
Pseudoalteromonas tunicata and Phaeobacter sp. strain 2.10	Bugula neritina	Ulva australis	Pacific Ocean	NI	Rao et al. (2007)
Pseudoalteromonas issachenkonii UST041101–043	B. neritina	Deep sea sediments	Pacific Ocean	Protease	Dobretsov et al. (2007)	Active in laboratory and field experiments
Natural communities, Photobacterium halotolerans and Ulvibacter litoralis, Shewanella basaltis Pseudoalteromonas arctica, Shewanella baltica and Bacillus foraminis	Amphibalanus improvisus	Fucus cerratus, F. vesiculosus and Polysiphonia stricta	Baltic Sea	NI	Nasrolahi et al. (2012)
Streptomyces fungicidicus	Balanus amphitrite	Deep sea sediments	West Pacific Ocean	Five Diketopiperazines	Li et al. (2006)
Pseudomonas rhizosphaerae	B. amphitrite; B. neritina	Deep sea	Pacific Ocean Province A	Bis(2-ethylhexyl)phthalate, cyclo(Tyr-Ile), cyclo(Phe-Pro), cyclo(Val-Pro) 3-phenyl-2-propenoic acid	Qi, Xu, Gao (2009)	Both antimicrobial and antilarval activities
Pseudoalteromonas sp. sf57	Hydroides elegans	Natural biofilms	South China Sea	NI	Huang et al. (2011)	Inhibition correlates with bacterial pigmentation
Streptomyces sp. UST040711–290	H. elegans	Deep sea sediments	Pacific Ocean Province A	Fatty acid 12-methyltetradecanoid acid	Xu et al. (2009)	Demonstrated effect of this compound on larval gene expression
Winogradskyella poriferorum	H. elegans; B. amphitrite	Lissodendoryx isodictyalis	Caribbean, Atlantic Ocean	Poly-ether A-E	Dash et al. (2009); Dash et al. (2011)	Inhibitive concentrations of 70 and 60 g ml^−1
Streptomyces sp.	H. elegans; B. neritina and B. amphitrite	Deep sea sediments, seawater	West Pacific Ocean	Five compounds belonging to α, β unsaturated lactones	Xu et al. (2010)	Based on structure relations antifouling compound was synthesised
Macrococcus sp., Bacillus sp., Pseudoalteromonas sp.	Aulacomya maoriana	Biofilms	South-West Pacific Ocean, New Zealand	NI	Alfaro et al. (2011)	Highest inhibition for bacterial exudates
Shewanella oneidensis SCH0402	Barnacles, mussels	Seawater	Yellow Sea, Korea	2-Hydroxymyristic acid and cis-9-oleic acid	Bhattarai et al. (2007)	Field experiments showed good AF effect after 1.5 years
Cyanobacteria
Oscillatoria sp. and Hormoscilla sp.	Biomphalaria glabrata	Seawater	Palmyra Atoll, Northern Pacific Ocean	Thiopalmyrone and palmyrrolinone	Pereira et al. (2011)	LC50 = 6–8.3 M
Lyngbya bouillonii	B. glabrata	Seawater	Papua New Guinea, South Pacific Ocean	Cyanolide A	Pereira et al. (2010)	LC50 = 1.2 M
L. majuscula	Amphibalanus (Balanus) amphitrite	Seawater	Caribbean, Atlantic Ocean	Isolmajusculamide, majusculamide A and hanutupeptin C	Tan and Goh (2009)
Note: Bacterial strains are classified by their activity. NI = compound has not been identified.

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