de Biología Tropical ISSN Impreso: 0034-7744 ISSN electrónico: 2215-2075

Marine bacteria from the Gulf of California with antimicrofouling activity against colonizing bacteria and microalgae

Diana Elizabeth Sánchez-Rodríguez, Ismael Ortiz-Aguirre, Ruth Noemí Aguila-Ramírez, Erika Guadalupe Rico-Virgen, Bárbara González-Acosta, Claire Hellio



One way of reducing the input of pollutants into the marine environment is to enforce the use of non-toxic antifouling paints in marine protected areas. Thus, the purpose of this study was to detect marine microorganisms that secrete inhibitory substances against bacteria and microalgae to avoid biofouling on man-made structures in La Paz bay, B.C.S., Mexico. The inhibitory potential of 125 bacteria was evaluated against biofilm-forming bacteria. Crude extracts were obtained with methanol and ethyl acetate from 16 bacterial strains that exhibited antagonistic and antibacterial activity in a preliminary screening. Antibacterial and antimicroalgal assays were performed using crude extracts, the minimum inhibitory concentration (MIC) was determined. The highest activity against bacteria and microalgae was found in two strains, Shewanella algae and Staphylococcus sp. The results of this study suggest that extracts of bacteria from the Gulf of California with antimicrobial properties against biofilm-forming bacteria can also prevent the adhesion of microalgae, which may control the development of biofilm formation and, as a consequence, biofouling.


epibionts; extracts; Shewanella; Staphylococcus; biofouling; antifouling

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Alzieu, C. (2000). Impact of tributyltin on marine invertebrates. Ecotoxicology, 9, 71-76. DOI: 10.1023/A:1008968229409

Amsterdam, D. (1996). Susceptibility testing of antimicrobials in liquid media. In V. Loman (Ed.). Antibiotics in laboratory medicine (pp. 52-111). Baltimore Md, USA: Williams & Wilkins.

Armstrong, E., Boyd, K. G., & Burgess, J. G. (2000). Prevention of marine biofouling using natural compounds from marine organisms. Biotechnology Annual Review, 6, 221-241. DOI: 10.1016/S1387-2656(00)06024-5

Balcázar, J. L., Loureiro, S., Da Silva, Y. J., Pintado, J., & Planas, M. (2010). Identification and characterization of bacteria with antibacterial activities isolated from seahorses (Hippocampus guttulatus). Journal of Antibiotics, 63, 271. DOI:

Bernbom, N., Ng, Y. Y., Kjelleberg, S., Harder, T., & Gram, L. (2011). Marine bacteria from Danish coastal waters show antifouling activity against the marine fouling bacterium Pseudoalteromonas sp. Strain S91 and Zoospores of the Green Alga Ulva australis independent of bacteriocidal activity. Applied and Environmental Microbiology, 77, 8557-8567. DOI: 10.1128/AEM.06038-11

Bhosale, S. H., Nagle, V. L., & Jagtap, T. G. (2002). Antifouling potential of some marine organisms from India against species of Bacillus and Pseudomonas. Marine Biotechnology, 4, 111-118. DOI: 10.1007/s10126-001-0087-1

Cassé, F., & Swain, G. W. (2006). The development of microfouling on four commercial antifouling coatings under static and dynamic immersion. International Biodeterioration and Biodegradation, 57, 179-185. DOI: 10.1016/j.ibiod.2006.02.008

Callow, J. A., & Callow, M. E. (2011). Trends in the development of environmentally friendly fouling-resistant marine coatings. Nature communications, 2, 244. DOI:

Chambers, L. D., Hellio, C., Stokes, K. R., Dennington, S. P., Goodes, L. R., Wood R. J. K., & Walsh, F. C. (2011). Investigation of Chondrus crispus as a potential source of new antifouling agents. International Biodeterioration and Biodegradation, 65, 939-946. DOI:

Costerton, J. W., Lewandowski, Z., Caldwell, D. E., Korber, D. R., & Lappin-Scott, H. M. (1995). Microbial biofilms. Annual Review Microbiology, 49, 711-745. DOI:

Ciriminna, R., Bright, F. V., & Pagliaro, M. (2015). Ecofriendly antifouling marine coatings. ACS Sustainable Chemistry & Engineering, 3, 559-565. DOI: 10.1021/sc500845n

Cucarella, C., Solano, C., Valle, J., Amorena, B., Lasa I. I. & Penades, J. R. (2001). Bap, a Staphylococcus aureus surface protein involved in biofilm formation. Journal of Microbiology and Bacteriology, 183, 2888-2896. DOI: 10.1128/JB.183.9.2888-2896.2001

Dobretsov, S., Dahms, H. U., & Qian, P. Y. (2006). Inhibition of biofouling by marine microorganisms and their metabolites. Biofouling, 22, 43-54. DOI: 10.1080/08927010500504784

Dobretsov, S., Abed, R. M. M., & Teplitski, M. (2013). Mini-review: Inhibition of biofouling by marine microorganisms, Biofouling, 29, 423-441. DOI: 10.1080/08927014.2013.776042

Dopazo, C. P., Lemos, M. L., Lodeiros, C., Bolinches, J., Baria J. L., & Toranzo, A. E. (1988). Inhibitory activity of antibiotic-producing marine bacteria against fish pathogens. Journal of Applied Bacteriology, 65, 97-101. DOI:

Egan, S., Harder, T., Burke, C., Steinberg, P., Kjelleberg S., & Thomas, T. (2013). The seaweed holobiont: understanding seaweed–bacteria interactions. FEMS Microbiology Reviews, 37, 462-476. DOI: 10.1111/1574-6976.12011

El Bour, M., Ismail-Ben Ali, A., & Ktari, L. (2013). Seaweeds epibionts: Biodiversity and potential bioactivities. In A. Méndez-Vilas (Ed.), Microbial pathogens and strategies for combating them: Science, technology and education (pp. 1298-1306). Badajoz, Spain: Formatex Research Center.

Fusetani, N., & Clare, A. S. (2006). Preface. In N. Fusetani & A. Clare (Ed.). Antifouling Compounds (pp. VII–VIII). Progress in Molecular and Subcellular Biology- Marine Molecular Biology. Berlin, Germany: Springer-Verlag.

Gomes, J., Grunau, A., Lawrence, A. K., Eberl, L., & Gademann, K. (2013). Bioinspired, releasable quorum sensing modulators. Chemical Communications, 49, 155-157. DOI: 10.1039/C2CC37287H

Guillard, R. R., & Ryther, J. H. (1962). Studies of marine planktonic diatoms: I. Cyclotella nana Hustedt, and Detonula confervacea (Cleve) Gran. Canadian Journal of Microbiology, 8(2), 229-239.

Grossart, H. P., Kiørboe, T., Tang, K., & Ploug, H. (2003). Bacterial Colonization of Particles: Growth and Interactions. Applied Environmental Microbiology, 69, 3500-3509. DOI: 10.1128/AEM.69.6.3500-3509.2003

Hare, C. E., Demir, E., Coyne, K. J., Cary, S. C., Kirchman, D. L., & Hutchins, D. A. (2005). A bacterium that inhibits the growth of Pfiesteria piscicida and other dinoflagellates. Harmful algae, 4, 221-234. DOI:

Hellio, C., Tsoukatou, M., Maréchal, J. P., Aldred, N., Beaupoli, C., Clare, A. S., … Roussis, V. (2005). Inhibitory effects of Mediterranean sponge extracts and metabolites on larval settlement of the barnacle Balanus amphirtite. Marine Biotechnology, 7, 297-305. DOI: 10.1007/s10126-004-3150-x

Hellio, C., Trepos, R., Aguila-Ramírez, R. N., & Hernández-Guerrero, C. J. (2015). Protocol for Assessing antifouling activities of macroalgal extracts. In Natural Products from Marine Algae: Methods and Protocols (pp. 421-435) New York, USA: Humana Press. DOI: 10.1007/978-1-4939-2684-8_27

Hentschel, U., Fieseler, L., Wehrl, M., Gernert, C., Steinert, M., Hacker, J., & Horn, M. (2003). Microbial diversity of sponges. In W. E. G. Müller (Ed.), Sponges (Porifera) (pp. 59-88). Springer, Berlin, Heidelberg. DOI: 10.1007/978-3-642-55519-0_3

International Maritime Organization (IMO). (2003). International Convention on the Control of Harmful Anti-fouling System on Ships AFS/CONF/26. Retrieved from

Id Daoud, G. (2015). Investigation of the antifouling properties of extracts from marine microalgae (PhD Thesis). University of Portsmouth, Portsmouth, U.K.

Jacobson, A., & Willingham, G. (2000). Sea-nine antifoulant: an environmentally acceptable alternative to organotin antifoulants. The Science of the Total Environment, 258, 103-110. DOI:

Kelecom, A. (2002). Secondary metabolites from marine microorganisms. Anais da Academia Brasileira de Ciências, 74, 151-170. DOI: 10.1590/S0001-37652002000100012

Konstantinou, I. K., & Albanis, T. A. (2004). Worldwide occurrence and effects of antifouling paint booster biocides in the aquatic environment. a review. Environment International, 30, 235-248. DOI:

Lasa I. (2004). Biofilm bacterianos. Instituto de Agrobiotecnologia y Recursos Naturales y Departamento de Producción Agraria, 37, 14-18.

León, J., Liza, L., Soto, I., Torres, M., & Orozco, A. (2010). Bacterias marinas productoras de compuestos antibacterianos aisladas a partir de invertebrados intermareales. Revista Peruana de Medicina Experimental y Salud Pública, 27, 215-221.

Mani, P., Dineshkumar, G., Jayaseelan, T., Deepalakshmi, K., Kumar, C. G., & Balan, S. S. (2016). Antimicrobial activities of a promising glycolipid biosurfactant from a novel marine Staphylococcuss aprophyticus SBPS 15. 3 Biotech, 6, 163. DOI: 10.1007/s13205-016-0478-7

Maréchal, J. P., & Hellio, C. (2011). Antifouling activity against barnacle cypris larvae: Do target species matter (Amphibalanus amphitrite versus Semibalanus balanoides)? International Biodeterioration & Biodegradation, 65, 92-101. DOI:

Marhaeni, B., Radjasa, O. K., Khoeri, M. M., Sabdono, A., Bengen, D. G., & Sudoyo, H. (2011). Antifouling activity of bacterial symbionts of seagrasses against marine biofilm-forming bacteria. Journal of Environmental Protection, 2, 1245. DOI: 10.4236/jep.2011.29143

Martín-Rodríguez, A. J., González-Orive, A., Hernández-Creus, A., Morales, A., Dorta-Guerra, R., Norte, M., & Fernández, J. J. (2014). On the influence of the culture conditions in bacterial antifouling bioassays and biofilm properties: Shewanella algae, a case study. BMC Microbiology, 14, 102. DOI: 10.1186/1471-2180-14-102

Martínez-Díaz, Y. R. (2010). Evaluación de un bioensayo para medir la inhibición de biopelículas bacterianas como indicativo de la actividad antifoulling de compuestos e origen natural. (Tesis de Maestría). Universidad Nacional de Colombia, Bogotá, Colombia.

Martínez-Matamoros, D. (2012). Búsqueda de compuestos bioactivos a partir de bacterias del Phyllum firmicutes aisladas del octocoral Pseudopterogorgia elisabethae recolectado en la isla Providencia. (Tesis de Maestría). Universidad Nacional de Colombia. Bogotá, Colombia.

McElroy, D., Hochuli, D., Doblin, M., Murphy, R., Blackburn, R., & Coleman, R. (2017). Effect of copper on multiple successional stages of a marine fouling assemblage. Biofouling, 1-13. DOI: 10.1080/08927014.2017

Mendola, D. (2003). Aquaculture of three phyla of marine invertebrates to yield bioactive metabolites: process developments and economics. Biomolecular Engineering, 4, 441-458. DOI:

Mendola, M. (2006). Agricultural technology adoption and poverty reduction: A propensity –score matching analysis for rural Bangladesh. Food Policy, 32, 372-393. DOI:

Olson, M. E., Ceri, H., Morck, W. M., Buret, A. G., & Read, R. R. (2002). Biofilm: formation and comparative susceptibility to antibiotics. Canadian Journal of Veterinary Research, 66, 86-92.

Penesyan, A., Kjelleberg, S., & Egan, S. (2010). Development of novel drugs from marine surface associated microorganisms. Marine Drugs, 8, 438-459. DOI: 10.3390/md8030438

Pinzón Espinosa, A. C. (2012). Metabolitos mayoritarios y evaluación de actividad antimicrobiana de bacterias aisladas del octocoral Pseudpterogorgia elisabethae del Caribe colombiano. (Tesis Doctoral). Universidad Nacional de Colombia, Bogotá, Colombia.

Popowicz, G. M., Dubin, G., Stec-Niemczyk, J., Czarny, A., Dubin, A., Potempa, J., & Holak, T. A. (2006). Functional and structural characterization of Spl proteases from Staphylococcus aureus. Journal of molecular biology, 358(1), 270-279. DOI:

Rachanamol, R. S., Lipton, A. P., Thankamani, V., Sarika, A. R., & Selvin, J. (2014). Molecular characterization and bioactivity profile of the tropical sponge-associated bacterium Shewanella algae VCDB. Helgoland Marine Research, 68, 263-269. DOI: 10.1007/s10152-014-0386-3

Rakesh, O. D., Pathak, R., Dhaker, A. S., Arora, R., Kumar, R., Rajaram, R., & Gautam, H. K. (2011). Isolation, characterization and bioactivity of deep sea bacteria with special reference to induction of antibacterial and antioxidant metabolites following gamma irradiation. Canadian Journal of Pure and Applied Science, 5, 1363-1370.

Sahoo, K., & Dahl, N. K. (2009). Potential microbial diversity in mangrove ecosystems: a review. Indian Journal of Marine Science, 38, 249-256.

Satheesh, S., Ba-akdah, M. A., & Al-Sofyani, A. (2016). Natural antifouling compound production by microbes associated with marine macroorganisms – A review. Electronic Journal of Biotechnology, 21, 26-35. DOI:

Slattery, M., Starmer, J., & Paul, V. (2001). Temporal and spatial variation in defensive metabolites of the tropical Pacific soft corals Sinularia maxima and S. polydactyla. Marine Biology, 138(6), 1183-1193. DOI: 10.1007/s002270100540

Stepanovic, S., Vukovic, D., Dakic, I., Savic, B., & Svabic-Vlahovic, M. (2000). A modified microtiter-plate test for quantification of staphylococcal biofilm formation. Journal of Microbiological Methods, 40, 175-179.

Supardy, N. A., Ibrahim, D., Nor, S. R. M., & Md, W. N. (2017). Inhibition of fouling bacteria by the marine epiphytes from selected locations in Malaysia. Malaysian Journal of Science, 36, 17-21. DOI: 10.22452/mjs.vol36no1.2

Sutherland I. (2001). Biofilm exopolysaccharides: a strong and sticky framework. Microbiology, 147, 3-9. DOI: 10.1099/00221287-147-1-3

Thatoi, H., Behera, B. C., Mishra, R. R., & Dutta, S. K. (2013). Biodiversity and biotechnological potential of microorganism from mangrove ecosystems, a review. Annals of Microbiology, 63, 1-19. DOI: 10.1007/s13213-012-0442-7

Toledo-Arana, A., Valle, J., Solano, C., Arrizubieta, M. J., Cucarella, C., Lamata, M., … Lasa, I. (2001). The enterococcal surface protein, Esp, is involved in Enterococcus faecalis biofilm formation. Applied Environmental Microbiology, 67, 4538-4545. DOI: 10.1128/AEM.67.10.4538-4545.2001

UNESCO (2017). Islands and Protected Areas of the Gulf of California. Retreived from

Vandecandelaere, I., Depuydt, P., Nelis, H. J., & Coenye, T. (2014). Protease production by Staphylococcus epidermidis and its effect on Staphylococcus aureus biofilms. Pathogens and Disease, 70, 321-331. DOI: 10.1111/2049-632X.12133

Vimala, R. (2016). Marine organisms: A potential source of natural antifouling metabolites. International Journal of ChemTech Research, 9, 208-217.

Yebra, D., Kiil, S., & Dam-Johansen, K. (2004). Antifouling technology: past, present and future steps towards efficient and environmentally friendly antifouling coatings. Progress in Organic Coatings, 75, 104-109. DOI: 10.1016/j.porgcoat.2003.06.001

Zhang, J., Jiang, H., Jiang, J., & Huang, G. (2016). Isolation and identification of Staphylococcus epidermidis S14 screening extracellular antimicrobial metabolites. American Journal of Biochemistry and Biotechnology, 12, 56-63. DOI: 10.3844/ajbbsp.2016.56.63


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