Antifouling activity of marine bacterial extracts: A non-toxic alternative as biocide
DOI:
https://doi.org/10.22370/rbmo.2024.59.1.4456Palabras clave:
Bacteria, antifouling, epibionts, diatoms, extractsResumen
Biofouling is generated by the biochemical condition of the substrate to form complex communities; this could be negative at an ecological and industrial level. To inhibit this process, coatings based on heavy metals are used. Microorganisms are promising sources of antifouling compounds that are non-toxic or less toxic than the commercial chemicals in use today. In order to evaluate the antifouling effectiveness of bacterial extracts, seven crude extracts from cultures of bacteria isolated from marine organisms were obtained. They were subjected to a toxicity test with Artemia nauplii, at different concentrations. Non-toxic extracts were incorporated into a gelling agent (Phytagel™) and exposed to the sea for 30 days to evaluate the inhibition of diatoms and macroorganisms adhesion. Sixty-seven diatoms’ taxa were identified, belonging to 45 genera, besides four groups of non-photosynthetic macroorganisms were identified; these are sea squirts, barnacles, bryozoans, and polychaetes. Toxicity test showed that only Bacillus safensis (C2) extract was toxic, and it was excluded from subsequent tests. There are significant differences between treatments, the extracts with the best activity are Shewanella algae (18) and Staphylococcus aureus (28). These extracts contain different organic compounds such as saponins, terpenes, sterols, and proteins, which could be responsible for their activity. These results suggest that microorganisms are an effective alternative to replace harmful chemical substances currently used in antifouling coatings. The extracts, being less toxic, are potential inhibitors or retardants of the epibiotic colonization process.
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Al-Lihaibi SS, A Abdel-Lateff, WM Alarif, HS Alorfi, Y Nogata & T Okino. 2019. Environmentally friendly antifouling metabolites from Red Sea Organisms. Journal of Chemistry 2019, 3278394. <https://doi.org/10.1155/2019/3278394>
Almeida R & V Vasconcelos. 2015. Natural antifouling compounds: Effectiveness in preventing invertebrate settlement and adhesion. Biotechnology Advances 33: 343-357.
Arias J, S Zea, F Newmark & M Santos-Acevedo. 2006. Determinación de la capacidad antiepibiótica de los extractos orgánicos crudos de las esponjas marinas Cribrochalina infundibulum y Biemna cribaria. Boletín de Investigaciones Marinas y Costeras-INVEMAR 35: 91-101.
Armstrong E, KG Boyd & JG Burgess. 2000. Prevention of marine biofouling using natural compounds from marine organisms. Biotechnology Annual Review 6: 221-241.
Balcázar JL, NM Lee, J Pintado & M Planas. 2010. Phylogenetic characterization and in situ detection of bacterial communities associated with seahorses (Hippocampus guttulatus) in captivity. Systematic and Applied Microbiology 33: 71-77.
Bartolomé-Camacho M & RS Sánchez-Fortún. 2007. Valoración de la toxicidad aguda de biocidas utilizados en ambientes de la vida privada y la salud pública sobre Artemia franciscana. Revista Latinoamericana de Recursos Naturales 3(1): 90-97.
Blunt JW, BR Copp, WP Hu, MHG Munro, PT Northcote & MR Prinsep. 2007. Marine natural products. Natural Products Report 24: 31-86.
Brusca RC. 2010. The Gulf of California biodiversity and conservation, 354 pp. The University of Arizona Press and The Arizona-Sonora Desert Museum, Tucson.
Burgess JG, KG Boyd, E Armstrong, Z Jiang, L Yan, M Berggren, U May, T Pisacane, A Granmo & DR Adams. 2003. The development of a marine natural product-based antifouling paint. Biofouling 19(S1): 197-205.
Camarillo-Márquez O, I Córdova-Alcántara, C Hernández-Rodríguez, B García-Pérez, M Martínez-Rivera & A Rodríguez-Tovar. 2018. Antagonistic interaction of Staphylococccus aureus toward Candida glabrata during in vitro biofilm formation is caused by an apoptotic mechanism. Frontier in Microbiology 9: 2031.
Cao S, J Wang, H Chen & D Chen. 2011. Progress of marine biofouling and antifouling technologies. Chinese Science Bulletin 56(7): 598-612.
Cassè F & GW Swain. 2006. The development of microfouling on four commercial antifouling coatings under static and dynamic immersion. International Biodeterioration & Biodegradation 57(3): 179-185.
Ciriminna R, FV Bright & M Pagliaro. 2015. Ecofriendly antifouling marine coatings. ACS Sustainable Chemistry Engineering 3(4): 559-565.
Dahms HU & S Dobretsov. 2017. Antifouling compounds from marine macroalgae. Marine Drugs 15(9): 265.
Dobretsov S, HU Dahms & PY Qian. 2006. Inhibition of biofouling by marine microorganisms and their metabolites. Biofouling 22: 43-54.
Doiron K, Beaulieu L, R St-Louis & K Lemarch. 2018. Reduction of bacterial biofilm formation using marine natural antimicrobial peptides. Colloids and Surfaces B: Biointerfaces 167: 524-530.
Faulkner DJ. 1994. Marine natural products. Natural Products in Chemical Biology 11: 355-394.
Foged N. 1975. Some littoral diatoms from the coast of Tanzania. Bibliotheca Phycologica 16: 1-127. J Cramer, Vaduz.
Foged N. 1984. Freshwater and littoral diatoms from Cuba. Bibliotheca Diatomologica 5: 1-243. Lubrecht & Cramer, Vaduz.
Fried B & J Sherma. 1996. Practical thin-layer chromatography: a multidisciplinary approach, 288 pp. CRC Press, Boca Raton.
Fusetani N. 2004. Biofouling and antifouling. Natural Products Reports 21: 94-104.
García MT, MC Pérez, ME Stupak & G Blustein. 2015. Hacia una reducción del contenido de cobre en pinturas antiincrustantes. Matéria 20(3): 691-698.
García-Madrigal MS. 2007. Clave ilustrada para las familias de anfípodos gamáridos (Peracarida: Amphipoda) litorales del Pacífico oriental tropical y glosario de términos. Ciencia y Mar 11: 3-27.
Guiry MD & GM Guiry. 2023. AlgaeBase. World-wide electronic publication, National University of Ireland, Galway. <http://www.algaebase.org>
Holmström C & S Kjelleberg. 1999. Marine Pseudoalteromonas species are associated with higher organisms and produce biologically active extracellular agents. FEMS Microbiology Ecology 30: 285-293.
Hellio C, M Tsoukatou, JP Maréchal, N Aldred, C Beaupoil, AS Clare, C Vagias & V Roussis. 2005. Inhibitory effects of Mediterranean sponge extracts and metabolites on larval settlement of barnacle Balanus amphitrite. Marine Biotechnology 7: 297-305.
Henrikson AA & JR Pawlik. 1995. A new antifouling assay method: results from field experiments using extracts of four marine organisms. Journal of Experimental Marine Biology and Ecology 194(2): 157-165.
Hunsucker KZ, A Koka, G Lund & G Swain. 2014. Diatom community structure on in-service cruise ship hulls. Biofouling 30(9): 1133-1140.
Hustedt F. 1930. Bacillariophyta (Diatomeae). In: Pascher A (ed). Süßwasserflora von Mitteleuropas, 466 pp. Gustav Fischer, Jena.
Hustedt F. 1955. Marine littoral diatoms of Beaufort North Carolina. Duke University Marine Station Bulletin 6: 1-67.
Hustedt F. 1959. Die Kieselalgen Deutschlands, Österreichs und der Schweiz unter Berücksichtigung der übrigen Länder Europas sowie der angrenzenden Meeresgebiete. In: Anonym (ed). Rabenhorst‘s Kryptogamen Flora von Deutschland, Österreich und der Schweiz 7(2, sec. 6): 737-845. Akademische Verlagsgesellschaft m.b.h, Leipzig.
Hustedt F. 1961-1966 Die Kieselalgen Deutschlands, Österreichs und der Schweiz unter Berücksichtigung der übrigen Länder Europas sowie der angrenzenden Meeresgebiete. In: Anonym (ed). Rabenhorst‘s Kryptogamen Flora von Deutschland, Österreich und der Schweiz 7(3): 1-816. Akademische Verlagsgesellschaft m.b.h, Leipzig.
Ivanova EP, MV Vysotskii, VI Svetashev, OI Nedashkovskaya, NM Gorshkova, VV Mikhailov & S Yoshikawa. 1999. Characterization of Bacillus strains of marine origin. International Microbiology 2(4): 267-271.
Jeong SY, K Ishida, Y Ito, S Okada & M Murakami. 2003. Bacillamide, a novel algicide from the marine bacterium, Bacillus sp. SY-1, against the harmful dinoflagellate, Cochlodinium polykrikoides. Tetrahedron Letters 44(43): 8005-8007.
Jones G. 2009. The battle against marine biofouling: a historical review. In: Hellio C & Y Yebra (eds). Advances in marine antifouling coatings and technologies, pp. 19-45. Woodshead Publishing, Cambridge.
Kelecom A. 2002. Secondary metabolites from marine microorganisms. Anais da Academia Brasileira de Ciências 74(1): 151-170.
Kerstitch A & H Bertsch. 2007. Sea of Cortez marine invertebrates: a guide for the Pacific coast, Mexico to Peru, 124 pp. Sea Challengers, Monterey.
Kohler KE & SM Gill. 2006. Coral Point Count with Excel extensions (CPCe): A Visual Basic program for the determination of coral and substrate coverage using random point count methodology. Computers and Geosciences 32(9): 1259-1269.
Lee SO, J Kato, N Takiguchi, A Kuroda, T Ikeda, A Mitsutani & H Ohtake. 2000. Involvement of an extracellular protease in algicidal activity of the marine bacterium Pseudoalteromonas sp. strain A28. Applied and Environmental Microbiology 6(10): 4334-4339.
León J, L Liza, I Soto, M Torres & A Orosco. 2010. Bacterias marinas productoras de compuestos antibacterianos aisladas a partir de invertebrados intermareales. Revista Peruana de Medicina Experimental y Salud Pública 27(2): 215-221.
López-Fuerte FO, DA Siqueiros-Beltrones & N Navarro. 2010. Benthic diatoms associated with mangrove environments in the northwest region of Mexico, 206 pp. CONABIO-UABCS-IPN, Ciudad de México.
Martínez-Díaz YR. 2010. Evaluación de un bioensayo para medir la inhibición de biopelículas bacterianas como indicativo de la actividad antifouling de compuestos de origen natural. Tesis Doctoral, Universidad Nacional de Colombia, Bogotá, 103 pp. <https://repositorio.unal.edu.co/handle/unal/8461>
Medina-López MA. 1999. Estructura de la criptofauna asociada a mantos de rodolitos en el suroeste del Golfo de California, México. Tesis de Licenciatura, Universidad Autónoma de Baja California Sur, La Paz, 60 pp.
Mitbavkar S & A Chandrashekar. 2006. Diatoms of the microphytobenthic community in a tropical intertidal sand flat influenced by monsoons: spatial and temporal variations. Marine Biology 148: 693-709.
Moreno JL, S Licea & H Santoyo. 1996. Diatomeas del Golfo de California, 273 pp. UABCS. SEP-FOMES-PROMARCO, Ciudad de México.
Muscholl-Silberhorn A, V Thiel & JF Imhoff. 2008. Abundance and bioactivity of cultured sponge-associated bacteria from the Mediterranean Sea. Microbial Ecology 55(1): 94-106.
Navarro JN. 1982. Marine diatoms associated with mangrove prop roots in the Indian River, Florida, USA. Bibliotheca Phycologica 61: 1-151.
Navarro NJ & R Torres. 1987. Distribution and community structure of marine diatoms associated with mangrove prop roots in the Indian River, Florida, USA. Nova Hedwigia 45: 101-112.
Nguta JM, JM Mbaria, DW Gakuya, PK Gathumbi, JD Kabasa & SG Kiama. 2012. Evaluation of acute toxicity of crude plant extracts from Kenyan biodiversity using brine shrimp, Artemia salina L. (Artemiidae). The Open Conference Proceedings Journal 3: 30-34.
Nurioglu AG & ACC Esteves. 2015. Non-toxic, non-biocide-release antifouling coatings based on molecular structure design for marine applications. Journal of Materials Chemistry 3(32): 6547-6570.
Pabel CT, J Vater, C Wilde, P Franke, J Hofemeister, B Adler & U Hentschel. 2003. Antimicrobial activities and matrix-assisted laser desorption/ionization mass spectrometry of Bacillus isolates from the marine sponge Aplysina aerophoba. Marine Biotechnology 5(5): 424-434.
Patil JS & A Chandrashekar. 2005. Biofilm diatom community structure: influence of temporal and substratum variability. Biofouling 21: 189-206.
Péragallo H & M Péragallo. 1908. Diatomées marines de France et des districts maritimes voisins. 491 pp. M.J. Tempére, Grez sur Loing.
Pinzón-Espinosa AC. 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, 126 pp. <https://repositorio.unal.edu.co/handle/unal/11423>
Prado-Navarro A, V Díaz-Castañeda, A Leija-Tristán & JA de León-González. 2016. Composición y estructura de las comunidades de poliquetos (Annelida) asociadas a fondos blandos de la costa occidental de la península de Baja California, México. Revista Mexicana de Biodiversidad 87: 74-85.
Qi S-H & X Ma. 2017. Antifouling compounds from marine invertebrates. Marine Drugs 15(9): 263.
Ramírez-Granillo A, MGM Canales, MES Espíndola, MAM Rivera, VMV DeLucio & AVR Tovar. 2015. Antibiosis interaction of Staphylococccus aureus on Aspergillus fumigatus assessed in vitro by mixed biofilm formation. BMC Microbiology 15(1): 33.
Rittschof D. 2001. Natural product antifoulants and coatings development. In: McClintock J & B Baker (eds). Marine chemical ecology, pp. 543-566. CRC Press, New York.
Sánchez-Lozano I, CJ Hernández-Guerrero, M Muñoz-Ochoa & C Hellio. 2019. Biomimetic approaches for the development of new antifouling solutions: Study of incorporation of macroalgae and sponge extracts for the development of new environmentally-friendly coatings. International Journal of Molecular Sciences 20(19): 4863.
Sánchez-Rodríguez DE, I Ortiz-Aguirre, RN Aguila-Ramírez, EG Rico-Virgen, B González-Acosta & C Hellio. 2018. Marine bacteria from the Gulf of California with antimicrofouling activity against colonizing bacteria and microalgae. Revista de Biología Tropical 66(4): 1649-1663.
Satheesh S & SG Wesley. 2012. Temporal changes of diatoms in marine biofilm developed on acrylic panels submerged in a tropical coast. Ocean Science Journal 47(4): 509-517.
Sayem SA, E Manzo, L Ciavatta, A Tramice, A Cordone, A Zanfardino & M Varcamonti. 2011. Anti-biofilm activity of an exopolysaccharide from a sponge-associated strain of Bacillus licheniformis. Microbial Cell Factories 10(1): 74.
Siqueiros-Beltrones DA. 2002. Diatomeas bentónicas de la península de Baja California; diversidad y potencial ecológico, 102 pp. Oceánides- CICIMAR-IPN-UABCS, México.
Solís-Marín FA, H Reyes-Bonilla, MD Herrero-Pérezrul, O Arizpe-Covarrubias & A Laguarda-Figueras. 1997. Sistemática y distribución de los equinodermos de la bahía de La Paz. Ciencias Marinas 23: 249-263.
Tovar-Hernández AM & B Yañes-Rivera. 2012. Actualización de las especies de invertebrados marinos exóticos en el Pacífico Mexicano. In: Low-Pfeng AM & EM Peter-Recagno (eds). Invertebrados marinos exóticos en el Pacífico Mexicano, pp. 1-9. Geomare, INE-SEMARNAT, México.
Trepos R, E Pinori, PR Jonsson, M Berglin, J Svenson & R Coutinho. 2014. Innovative approaches for the development of new copper-free marine antifouling paints. Journal of Ship and Ocean Technology 9(4): 7-18.
Valle J, S Da-Re, N Henry, T Fontaine, D Balestrino, P Latour-Lambert & JM Ghigo. 2006. Broad-spectrum biofilm inhibition by a secreted bacterial polysaccharide. Proceedings of the National Academy of Sciences 103(33): 12558-12563.
Vandecandelaere I, P Depuydt, H Nelis & T Coenye. 2014. Protease production by Staphylococcus epidermidis and its effect on Staphylococcus aureus biofilms. Pathogen and Disease 70: 321-331.
Viju N, SMJ Punitha & S Satheesh. 2019. Antifouling potential of symbiotic marine bacterium Bacillus subtilis MUT: M15 associated with the cuttlefish Sepia sp. Indian Journal of Geo Marine Sciences 48(5): 685-697.
Witkowski A, H Lange-Bertalot & D Metzeltin. 2000. Diatom flora of marine coasts I, 925 pp. Gantner Verlag, Ruggell.
WoRMS 2022. World Register of Marine Species. Editorial Board. VLIZ - Flanders Marine Institute, Oostende. <https://www.marinespecies.org>
Xu J, J Kim, T Danhorn, PM Merritt & C Fuqua. 2012. Phosphorus limitation increases attachment in Agrobacterium tumefaciens and reveals a conditional functional redundancy in adhesion biosynthesis. Research in Microbiology 163: 674-684.
Zargiel KA & GW Swain. 2014. Static vs dynamic settlement and adhesion of diatoms to ship hull coatings. Biofouling 30: 115-129.
Zhang J, H Jiang, J Jiang & G Huang. 2016. Isolation and identification of Staphylococcus epidermidis S14 screening extracellular antimicrobial metabolites. American Journal of Biochemistry and Biotechnology 12(1): 56-63.
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Derechos de autor 2024 Erika Guadalupe Rico-Virgen, Ismael Ortiz-Aguirre, Claire Hellio, Carlos Rangel-Dávalos, Anahí Escobedo-Fregoso, Francisco Omar López-Fuerte, María Concepción Lora-Vilchis, Ruth Noemí Aguila-Ramírez
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