Hard and soft coral-associated bacteria with pathogenic and probiotic potential
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Keywords

Coral reefs
culturable bacteria
microorganisms
octocorals
Eastern Pacific

Métricas de PLUMX 

Abstract

Microorganisms associated with coral reefs play a critical role in coral health and survival. The objective of this study was to identify difficult-to-grow bacterial isolates associated with the octocorals Carijoa riisei and Leptogorgia alba, and hermatypic corals Pocillopora damicornis and Pocillopora verrucosa. Isolates were identified through 16S rRNA sequencing and 18 were identified, including several pathogenic bacteria, Vibrio sp., Grimontia indica and Pseudoalteromonas piratica. In addition, isolates associated with pathogen inhibition, Ruegeria profundi, Ruegeria conchae, Pseudoalteromonas luteoviolacea, and Pseudoalteromonas gelatinilytica were identified. The vulnerability of marine organisms to microbial changes is shown and information is provided on their response to environmental stress.

https://doi.org/10.15741/revbio.12.e1890
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References

Ameen, F., AlNadhari, S., & Al-Homaidan. A. A. (2021). Marine microorganisms as an untapped source of bioactive compounds. Saudi Journal of Biological Sciences, 28, 224-231. https://doi.org/10.1016/j.sjbs.2020.09.052

Ben-Haim, Y., Thompson, F. L., Thompson, C. C., Cnockaert, M. C., Hoste, B., Swings, J., & Rosenberg, E. (2003a). Vibrio coralliilyticus sp. nov., a temperature-dependent pathogen of the coral Pocillopora damicornis. International Journal of Systematic and Evolutionary Microbiology, 53, 309-315. https://doi.org/10.1099/ijs.0.02402-0

Ben-Haim, Y., Zicherman-Keren, M., & Rosenberg, E. (2003b). Temperature-regulated bleaching and lysis of the coral Pocillopora damicornis by the novel pathogen Vibrio coralliilyticus. Applied and Environmental Microbiology, 69, 4236-4242. https://doi.org/10.1128/AEM.69.7.4236-4242.2003

Beurmann, S., Ushijima, B., Svoboda, C. M., Videau, P., Smith, A. M., Donachie, S. P., Aeby, G. S., & Callahan, S. M. (2017). Pseudoalteromonas piratica sp. nov., a budding, prosthecate bacterium from diseased Montipora capitata, and emended description of the genus Pseudoalteromonas. International Journal of Systematic and Evolutionary Microbiology, 67, 2683-2688. https://doi.org/10.1099/ijsem.0.001995

Bonnet, M., Lagier, J. C., Raoult, D., & Khelaifia, S. (2019). Bacterial culture through selective and non-selective conditions: the evolution of culture media in clinical microbiology. New Microbes New Infect, 34, 100622. https://doi.org/10.1016/j.nmni.2019.100622

Bourne, D. G., Morrow, K. M., & Webster, N. S. (2016). Insights into the coral microbiome: underpinning the health and resilience of reef ecosystems. Annual Review of Microbiology, 70, 317-40. https://doi.org/10.1146/annurev-micro-102215-095440

Carlson, R. R., Crowder, L. B., Martin, R. E., & Asner, G. P. (2024). The effect of reef morphology on coral recruitment at multiple spatial scales. The Proceedings of the National Academy of Sciences, 121, e2311661121. https://doi.org/10.1073/pnas.2311661121

Caycedo Lozano, L., Ramírez, L. C. C., & Suárez, D. M. T. (2021). Las bacterias, su nutrición y crecimiento: una mirada desde la química. Nova, 19, 49-94. https://doi.org/10.22490/24629448.5293

Cheng, K., Tong, M., Cai, Z., Jong, M. C., Zhou, J., & Xiao, B. (2023). Prokaryotic and eukaryotic microbial communities associated with coral species have high host specificity in the South China Sea. Science of the Total Environment, 867, 161185. https://doi.org/10.1016/j.scitotenv.2022.161185

Cocolin, L. S. (2010). Métodos independientes y dependientes de cultivo para estudiar y caracterizar la ecología microbiana en la fermentación vínica. ACE: Revista de Enología, 120, 1.

Falkowski, P. G., Fenchel, T., & Delong, E. F. (2008). The microbial engines that drive Earth's biogeochemical cycles. Science, 320, 1034-1039. https://doi.org/10.1126/science.1153213

Fazeli, N., Naeemi, A. S., Jalali, S. A. H., & Zamani, H. (2021). Antibacterial and Antibiofilm Potential of Sea Anemone (Stichodactyla haddoni) Isolated Vibrio (V. parahaemolyticus and V. alginolyticus), and Pseudoalteromonas (P. gelatinilytica and P. piscicida) Against Staphylococcus aureus and Pseudomonas aeruginosa. Journal of Kermanshah University of Medical Sciences, 25, e108653. https://doi.org/10.5812/jkums.108653

Freire, I., Gutner-Hoch, E., Muras, A., Benayahu, Y., & Otero, A. (2019). The effect of bacteria on planula-larvae settlement and metamorphosis in the octocoral Rhytisma fulvum fulvum. PLoS One, 14(9), e0223214. https://doi.org/10.1371/journal.pone.0223214

Gerhardt, P., Murray, R. G. E., Costilow, R. N., Nester, E. W., Wood, W. A., Krieg, N. R., & Phillips, G. B. (1981). Manual of methods for general bacteriology. Washington, DC: American Society for Microbiology, pp l0.

Gibbin, E., Gavish, A., Krueger, T., Kramarsky-Winter, E., Shapiro, O., Guiet, R., Jensen, L., Vardi, A., & Meibom, A. (2019). Vibrio coralliilyticus infection triggers a behavioural response and perturbs nutritional exchange and tissue integrity in a symbiotic coral. Multidisciplinary Journal of Microbial Ecology, 13, 989–1003. https://doi.org/10.1038/s41396-018-0327-2

Grottoli, A. G., Dalcin Martins, P., Wilkins, M. J., Johnston, M. D., Warner, M. E., Cai, W. J., Melman, T. F., Hoadley, K. D., Pettay, D. T., Levas, S., & Schoepf, V. (2018). Coral physiology and microbiome dynamics under combined warming and ocean acidification. PLoS One, 13, e0191156. https://doi.org/10.1371/journal.pone.0191156

He, X., Zou, J., Chen, Q., Qin, X., Liu, Y., Zeng, L., & Su, H. (2024). Microbial and transcriptional response of Acropora valida and Turbinaria peltata to Vibrio coralliilyticus challenge: insights into corals disease resistance. BMC microbiology, 24(1), 288. https://doi.org/10.1186/s12866-024-03438-7

Hernández-Zulueta, J., Araya, R., Vargas-Ponce, O., Díaz-Pérez, L., Rodríguez-Troncoso, A. P., Ceh, J., Ríos-Jara, E., & Rodríguez-Zaragoza, F. A. (2016). First deep screening of bacterial assemblages associated with corals of the Tropical Eastern Pacific. FEMS Microbiology Ecology, 92, fiw196. https://doi.org/10.1093/femsec/fiw196

Hoffmann, F., & Panknin, M. (2020). Host-microbe interactions in octocoral holobionts recent advances and perspectives. Microbiome, 8, 1-19. https://doi.org/10.1186/s40168-020-00896-4

Hughes, T. P., Graham, N. A. J., Jackson, J. B. C., Mumby, P. J., & Steneck, R. S. (2010). Rising to the challenge of sustaining coral reef resilience. Trends Ecology and Evolution, 25, 633-642. https://doi.org/10.1016/j.tree.2010.07.011

Isnansetyo, A., & Kamei, Y. (2003). MC21-A, a bactericidal antibiotic produced by a new marine bacterium, Pseudoalteromonas phenolica sp. nov. O-BC30T, against methicillin-resistant Staphylococcus aureus. Journal of Antimicrobial Chemotherapy, 47, 480-488. https://doi.org/10.1128/AAC.47.2.480-488.2003

Jayasreea, V. S., Sobhana, K. S., Priyankaa, P., Keerthia, K. R., Jasminea, S., Ranjitha, L., Ramkumara, S., Saravanana, R., Kingsleya, H. J., Sreenatha, K. R., Georgea, R. M, Joshia, K. K., & Gopalakrishnana, A. (2021). Characterization and antibacterial activity of violacein producing deep purple pigmented bacterium Pseudoalteromonas luteoviolacea (Gauthier, 1982) isolated from coral reef ecosystems. Indian Journal of Geo Marine Sciences, 50, 620-634. http://op.niscpr.res.in/index.php/IJMS/article/viewFile/40727/465481610

Jia, Y., Lu, J., Wang, M., Qin, W., Chen, B., Xu, H., & Ma, Z. (2023). Algicidal bacteria in phycosphere regulate free-living Symbiodinium fate via triggering oxidative stress and photosynthetic system damage. Ecotoxicology and Environmental Safety, 263, 115369. https://doi.org/10.1016/j.ecoenv.2023.115369

John, J., Siva, V., Kumari, R., Arya, A., & Kumar, A. (2020). Unveiling cultivable and uncultivable halophilic bacteria inhabiting Marakkanam saltpan, India and their potential for biotechnological applications. Geomicrobiology Journal, 37, 691-701. https://doi.org/10.1080/01490451.2020.1764676

Kogure, K., Simidu, U., & Taga, N. (1979). A tentative direct microscopic method for counting living marine bacteria. Canadian Journal of Microbiology, 25, 415-420. https://doi.org/10.1139/m79-063

Lema, K. A., Willis, B. L., & Bourne, D. G. (2012). Corals form characteristic associations with symbiotic nitrogen-fixing bacteria. Applied and Environmental Microbiology, 18, 3136–44.

Lampert, Y., Kelman, D., Dubinsky, Z., Nitzan, Y., & Hill, R. T. (2006). Diversity of culturable bacteria in the mucus of the Red Sea coral Fungia scutaria. FEMS microbiology ecology, 58(1), 99-108. https://doi.org/10.1111/j.1574-6941.2006.00136.x

Lewis, W. H., Tahon, G., Geesink, P., Sousa, D. Z., & Ettema, T. J. (2021). Innovations to culturing the uncultured microbial majority. Nature Reviews Microbiology, 19, 225-240. https://doi.org/10.1038/s41579-020-00458-8

Miura, N., Motone, K., Takagi, T., Aburaya, S., Watanabe, S., Aoki, W., & Ueda, M. (2019). Ruegeria sp. Strains isolated from the reef-building coral Galaxea fascicularis inhibit growth of the temperature-dependent pathogen Vibrio coralliilyticus. Marine Biotechnology, 21, 1-8. https://doi.org/10.1007/s10126-018-9853-1.

McDevitt-Irwin, J. M., Baum, J. K., Garren, M., & Vega Thurber, R. L. (2017). Responses of coral-associated bacterial communities to local and global stressors. Frontiers in Marine Science, 4, 262. https://doi.org/10.3389/fmars

Mohamed, A. R., Ochsenkühn, M. A., Kazlak, A. M., Moustafa, A., & Amin, S. A. (2023). The coral microbiome: towards an understanding of the molecular mechanisms of coral-microbiota interactions. FEMS Microbiol Reviews, 47, fuad005. https://doi.org/10.1093/femsre/fuad005

O'Brien, P. A., Tan, S., Yang, C., Frade, P. R., Andreakis, N., Smith, H. A., Miller, D. J., Webster, N. S., Zhang, G., & Bourne, D. G. (2020). Diverse coral reef invertebrates exhibit patterns of phylosymbiosis. Multidisciplinary Journal of Microbial Ecology, 14, 2211-2222. https://doi.org/10.1038/s41396-020-0671-x

Overmann, J., Abt, B., & Sikorski, J. (2017). Present and future of culturing bacteria. Annual Review of Microbiology, 71, 711-730. https://doi.org/10.1146/annurev-micro-090816-093449

Peixoto, R. S., Sweet, M., Villela, H. D. M., Cardoso, P., Thomas, T., Voolstra, C. R., Høj, L., Bourne, & D. G. (2021). Coral Probiotics: Premise, Promise, Prospects. Annual Review of Animal Biosciences, 9, 265-288. https://doi.org/10.1146/annurev-animal-090120-115444

Peng, Q., Xie, S. P., Passalacqua, G. A., Miyamoto, A., & Deser, C. (2024). The 2023 extreme coastal El Niño: Atmospheric and air-sea coupling mechanisms. Science Advances, 10, eadk8646. https://doi.org/10.1126/sciadv.adk8646

Pérez de-Silva, C. V., Cupul-Magaña, A. L., Rodríguez-Troncoso, A. P., & Rodríguez-Zaragoza, F. A. (2022). Reef Fish assemblage in two insular zones within the Mexican Central Pacific. Oceans, 3, 204-217. https://doi.org/10.3390/oceans3020015

Rappé, M. S., & Giovannoni, S. J. (2003). The uncultured microbial majority. Annual Review of Microbiology, 57(1), 369-394. https://doi.org/10.1146/annurev.micro.57.090502.093703.

Reimer, J. D., Peixoto, R. S., Davies, S. W., Traylor-Knowles, N., Short, M. L., Cabral-Tena, R. A., Burt, J. A., Pessoa, I., Banaszak, A. T., Winters, R. S., Moore, T., Schoepf, V., Kaullysing, D., Calderon–Aguilera, L. E., Worheide, G., Harding, S., Munbodhe, V., Mayfield, A., Ainsworth, T., Vardi, T., Eakin, C. M., Pratchett, M. S., & Voolstra, C. R. (2024). The Fourth Global Coral Bleaching Event: Where do we go from here?. Coral Reefs, 43, 1-5. https://doi.org/10.1007/s00338-024-02504-w

Rosenberg, E., Kellogg, C. A., & Rohwer, F. (2007). Coral microbiology. Oceanography, 20, 146–154. https://doi.org/10.5670/oceanog.2007.60

Samper, J., Raina, J. B., Humphrey, C., Høj, L., & Bourne, D. G. (2025). Microbial processes and nutrient uptake in the coral holobiont and reef ecosystems. In Coral Reef Microbiome (pp. 113-130). Cham: Springer Nature Switzerland.

Shleeva, M. O., Kudykina, Y. K., Vostroknutova, G. N., Suzina, N. E., Mulyukin, A. L., & Kaprelyants, A. S. (2011). Dormant ovoid cells of Mycobacterium tuberculosis are formed in response to gradual external acidification. Tuberculosis, 91(2), 146-154.

Singh, A., Vaidya, B., Khatri, I., Srinivas, T. N. R., Subramanian, S., Korpole, S., & Pinnaka, A. K. (2014). Grimontia indica AK16T, sp. nov., isolated from a seawater sample reports the presence of pathogenic genes similar to Vibrio Genus. PLoS One, 9, e85590. https://doi.org/10.1371/journal.pone.0085590

Spalding, M. D., Ravilious, C., & Green, E. P. (2001). World atlas of coral reefs. University of California Press. https://doi.org/10.5860/choice.39-2540

Thompson, J. R., Rivera, H. E., Closek, C. J., & Medina, M. (2015). Microbes in the coral holobiont: partners through evolution, development, and ecological interactions. Frontiers in cellular and infection microbiology, 4, 176. https://doi.org/10.3389/fcimb.2014.00176

Tout, J., Siboni, N., Messer, L. F., Garren, M., Stocker, R., Webster, N. S., Ralph, P. J., & Seymour, J. R. (2015). Increased seawater temperature increases the abundance and alters the structure of natural Vibrio populations associated with the coral Pocillopora damicornis. Frontiers in Microbial, 6, 432. https://doi.org/10.3389/fmicb.2015.00432

van de Water, J. A., Allemand, D., & Ferrier-Pagès, C. (2018). Host-microbe interactions in octocoral holobionts-recent advances and perspectives. Microbiome, 6, 1-28. https://doi.org/10.1186/s40168-018-0431-6

van Oppen, M. J. H., & Medina, M. (2020). Coral evolutionary responses to microbial symbioses. Philosophical Transactions of the Royal Society Biological Sciences, 375, 20190591. https://doi.org/10.1098/rstb.2019.0591

Vidal-Dupiol, J., Ladrière, O., Meistertzheim, A-L., Fouré, L., Adjeroud, M., & Mitta, G. (2011). Physiological responses of the scleractinian coral Pocillopora damicornis to bacterial stress from Vibrio coralliilyticus. Journal of Experimental Biology, 214, 1533–45. https://doi.org/10.1242/jeb.053165

Wang, X., Isbrandt, T., Christensen, E. Ø., Melchiorsen, J., Larsen, T. O., Zhang, S., & Gram, L. (2021). Identification and verification of the prodigiosin biosynthetic gene cluster (BGC) in Pseudoalteromonas rubra S4059. Microbiology Spectrum, 9, e01171-21. https://doi.org/10.1128/Spectrum.01171-21

Weil, E., Rogers, C. S., & Croquer, A. (2017). Octocoral diseases in a changing ocean. In: Rossi S, Bramanti L, Gori A, Orejas Saco del Valle C, editors. Marine animal forests: the ecology of benthic biodiversity hotspots. Springer: Cham pp. 1-55. https://doi.org/10.1007/978-3-319-17001-5_43-1

Xiang, N., Hassenrück, C., Pogoreutz, C., Rädecker, N., Simancas-Giraldo, S. M., Voolstra, C. R., Wild, C., & Gärdes, A. (2022). Contrasting microbiome dynamics of putative denitrifying bacteria in two octocoral species exposed to dissolved organic carbon (DOC) and warming. Applied and Environmental Microbiology, 88, e0188621. https://doi.org/10.1128/AEM.01886-21

Xu, M., Cai, Z., Cheng, K., Chen, G., & Zhou, J. (2024). Mitigation of Vibrio coralliilyticus-induced coral bleaching through bacterial dysbiosis prevention by Ruegeria profundi. Applied and Environmental Microbiology, 90, e02274-23. https://doi.org/10.1128/aem.02274-23

Zhang, J., Liang, Q. Y., Mu, D. S., Lian, F., Gong, Y., Ye, M., & Du, Z. J. (2024). Cultivating the uncultured: Harnessing the “sandwich agar plate” approach to isolate heme‐dependent bacteria from marine sediment. Mlife, 3, 143-155. https://doi.org/10.1002/mlf2.12093

Zhang, Z., van Kleunen, M., Becks, L., & Thakur, M. P. (2020). Towards a general understanding of bacterial interactions. Trends Microbiology, 28, 783-785. https://doi.org/10.1016/j.tim.2020.05.010

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