Characterization of the core microbiome and rare bacterial biosphere in three coral species across an environmental gradient in the Mexican Caribbean, using high-throughput 16S rRNA sequencing
DOI:
https://doi.org/10.15517/s9m3zg81Keywords:
Microbial ecology; bacteriome; 16S rRNA; reef; high-throughput sequencing.Abstract
Introduction: The coral microbiome comprises a stable core microbiome that supports host health and homeostasis, as well as a rare biosphere that enhances the capacity to respond to environmental disturbances.
Objective: To characterize the core microbiome and rare bacterial biosphere associated with Acropora palmata, Orbicella faveolata, and Porites porites from the Mexican Caribbean across sites with different levels of anthropogenic stress.
Methods: The composition of the core microbiome and rare bacterial biosphere was analyzed using high-throughput sequencing of the 16S rRNA gene.
Results: The core microbiome represented 9.7% of the total sequences (50 ASVs) and was dominated by Amoebophilaceae, Rhodobacteraceae, and Woeseiaceae. At the genus level, Candidatus_Amoebophilus was prevalent across all coral species, while Delftia characterized A. palmata and P. porites, and Pelagibius and Woeseia dominated in O. faveolata and P. porites. The rare biosphere was more diverse (1,585 ASVs; 11.9%), with O. faveolata showing the highest richness and dominated by Rhodobacteraceae, Kiloniellaceae, and Vibrionaceae, including Vibrio, Woeseia, Limibaculum, and Desulforhopalus. Beta diversity analyses revealed significant differences among coral species and across anthropogenic gradients, with host identity explaining most of the variation in core microbiomes. The rare biosphere also showed significant variation, although much of this variability remains unexplained. SIMPER analysis identified the ASVs that contributed most to the observed differences. In the core microbiome, the main contributing ASVs were affiliated with the genera Candidatus_Amoebophilus, Delftia, Pelagibius, and Woeseia, whereas, in the rare biosphere, the ASVs contributing most to the observed differences were affiliated with Pelagibius, Tistlia, Woeseia, Desulforhopalus, and Vibrio. Additionally, 23 putative metabolic functions were predicted, with aerobic chemoheterotrophy, fermentation, and sulfur respiration being the most common.
Conclusions: These findings highlight the complementary roles of the core microbiome and rare biosphere in structuring coral microbial communities, supporting resilience, and serving as potential candidates bioindicators of environmental change in the Mexican Caribbean.
Downloads
References
Abdelghany, S., Simancas-Giraldo, S. M., Zayed, A., & Farag, M. A. (2025). How does the coral microbiome mediate its natural host fitness under climate stress conditions? Physiological, molecular, and biochemical mechanisms. Marine Environmental Research, 204, 106920. https://doi.org/10.1016/j.marenvres.2024.106920. DOI: https://doi.org/10.1016/j.marenvres.2024.106920
Ainsworth, T. D., Fordyce, A. J., & Camp, E. F. (2017). The other microeukaryotes of the coral reef microbiome. Trends in Microbiology, 25(12), 980–991. https://doi.org/10.1016/j.tim.2017.06.007. DOI: https://doi.org/10.1016/j.tim.2017.06.007
Ainsworth, T. D., Krause, L., Bridge, T., Torda, G., Raina, J. B., Zakrzewski, M., Gates, R. D., Padilla-Gamiño, J. L., Spalding, H. L., Smith, C., Woolsey, E. S., Bourne, D. G., Bongaerts, P., Hoegh-Guldberg, O., & Leggat, W. (2015). The coral core microbiome identifies rare bacterial taxa as ubiquitous endosymbionts. The ISME Journal, 9(10), 2261–2274. https://doi.org/10.1038/ismej.2015.39. DOI: https://doi.org/10.1038/ismej.2015.39
Alvarado-Cerón, V., Gómez-Corrales, M., Padilla-Souza, A. C., León-Pech, M. G., Rivera-Madrid, R., Arias-González, J. E., & Prada, C. (2026). Genomic insights into natural and restored populations of Acropora palmata: Implications for genetic diversity and conservation strategies. Marine Environmental Research, 215, 107779. https://doi.org/10.1016/j.marenvres.2025.107779. DOI: https://doi.org/10.1016/j.marenvres.2025.107779
Alves, N., Neto, O. S. M., Silva, B. S. O., De-Moura, R. L., Francini-Filho, R. B., Barreira-Castro, C., Paranhos, R., Bitner-Mathé, B. C., Kruger, R. H., Vicente, A. C. P., Thompson, C. C., & Thompson, F. L. (2010). Diversity and pathogenic potential of vibrios isolated from Abrolhos Bank corals. Environmental Microbiology Reports, 2, 90–95. https://doi.org/10.1111/j.1758-2229.2009.00101.x. DOI: https://doi.org/10.1111/j.1758-2229.2009.00101.x
Anderson, M. J., Gorley, R. N., & Clarke, K. R. (2008). Permanova for Primer Guide to Software and Statistical Methods. PRIMER-E.
Apprill, A., Weber, L. G., & Santoro, A. E. (2016). Distinguishing between microbial habitats unravels ecological complexity in coral microbiomes. mSystems, 1(5), e00143-16. https://doi.org/10.1128/msystems.00143-16. DOI: https://doi.org/10.1128/mSystems.00143-16
Arias-González, J. E., Fung, T., Seymour, R. M., Garza-Pérez, J. R., Acosta-González, G., Bozec, Y. M., & Johnson, C. R. (2017). A coral–algal phase shift in Mesoamerica not driven by changes in herbivorous fish abundance. PLOS One, 12(4), e0174855. https://doi.org/10.1371/journal.pone.0174855. DOI: https://doi.org/10.1371/journal.pone.0174855
Arriaga-Piñón, Z. P., Aguayo-Leyva, J. E., Álvarez-Filip, L., Banaszak, A. T., Aguirre-Macedo, M. L., Paz-García, D. A., & García-Maldonado, J. Q. (2024). Microbiomes of three coral species in the Mexican Caribbean and their shifts associated with the Stony Coral Tissue Loss Disease. PLOS One, 19(8), e0304925. https://doi.org/10.1371/journal.pone.0304925. DOI: https://doi.org/10.1371/journal.pone.0304925
Barranco, L. M., Carriquiry, J. D., Rodríguez-Zaragoza, F. A., Cupul-Magaña, A. L., Villaescusa, J. A., & Calderón-Aguilera, L. E. (2016). Spatiotemporal variations of live coral cover in the northern Mesoamerican Reef System, Yucatan Peninsula, Mexico. Scientia Marina, 80, 143–150. https://doi.org/10.3989/scimar.04294.23A. DOI: https://doi.org/10.3989/scimar.04294.23A
Bayer, T., Neave, M. J., Alsheikh-Hussain, A., Aranda, M., Yum, L. K., Mincer, T., Hughen, K., Apprill, A., & Voolstra, C. R. (2013). The microbiome of the Red Sea coral Stylophora pistillata is dominated by tissue-associated Endozoicomonas bacteria. Applied and Environmental Microbiology, 79(15), 4759–4762. https://doi.org/10.1128/aem.00695-13. DOI: https://doi.org/10.1128/AEM.00695-13
Bernasconi, R., Stat, M., Koenders, A., Paparini, A., Bunce, M., & Huggett, M. J. (2019). Establishment of coral-bacteria symbioses reveal changes in the core bacterial community with host ontogeny. Frontiers in Microbiology, 10, 1529. https://doi.org/10.3389/fmicb.2019.01529. DOI: https://doi.org/10.3389/fmicb.2019.01529
Blanchon, P., Richards, S., Bernal, J. P., Cerdeira-Estrada, S., Ibarra, M. S., Corona-Martínez, L., & Martell-Dubois, R. (2017). Retrograde accretion of a Caribbean fringing reef controlled by hurricanes and sea-level rise. Frontiers in Earth Science, 5, 78. https://doi.org/10.3389/feart.2017.00078. DOI: https://doi.org/10.3389/feart.2017.00078
Bokulich, N. A., Kaehler, B. D., Rideout, J. R., Dillon, M., Bolyen, E., Knight, R., Huttley, G. A., & Caporaso, G. J. (2018). Optimizing taxonomic classification of marker-gene amplicon sequences with QIIME 2’s q2-feature-classifier plugin. Microbiome, 6, 90. https://doi.org/10.1186/s40168-018-0470-z. DOI: https://doi.org/10.1186/s40168-018-0470-z
Bolyen, E., Rideout, J. R., Dillon, M. R., Bokulich, N. A., Abnet, C. C., Al-Ghalith, G. A., Alexander, H., Alm, E. J., Arumugam, M., Asnicar, F., Bai, Y., Bisanz, J. E., Bittinger, K., Brejnrod, A., Brislawn, C. J., Brown, C. T., Callahan, B. J., Caraballo-Rodríguez, A. M., Chase, J., & Caporaso, J. G. (2019). Reproducible, interactive, scalable and extensible microbiome data science using QIIME 2. Nature Biotechnology, 37(8), 852–857. https://doi.org/10.1038/s41587-019-0209-9. DOI: https://doi.org/10.1038/s41587-019-0209-9
Bourne, D. G., & Munn, C. B. (2005). Diversity of bacteria associated with the coral Pocillopora damicornis from the Great Barrier Reef. Environmental Microbiology, 7, 1162–1174. https://doi.org/10.1111/j.1462-2920.2005.00793.x. DOI: https://doi.org/10.1111/j.1462-2920.2005.00793.x
Caballero-Aragón, H., Perera-Valderrama, S., Cerdeira-Estrada, S., Martell-Dubois, R., Rosique-de-la-Cruz, L., Álvarez-Filip, L., Pérez-Cervantes, E., Estrada-Saldívar, N., & Ressl, R. (2020). Puerto Morelos coral reefs, their current state and classification by a scoring system. Diversity, 12(7), 272. https://doi.org/10.3390/d12070272. DOI: https://doi.org/10.3390/d12070272
Caballero-Aragón, H., Perera-Valderrama, S., Cerdeira-Estrada, S., Martell-Dubois, R., Rosique-de-la-Cruz, L., Álvarez-Filip, L., Pérez-Cervantes, E., Estrada-Saldivar, N., & Ressl, R. (2022). Dataset of coral reefs monitoring, Puerto Morelos, Mexico, 2019. Data in Brief, 42, 108253. https://doi.org/10.1016/j.dib.2022.108253. DOI: https://doi.org/10.1016/j.dib.2022.108253
Callahan, B. J., McMurdie, P. J., Rosen, M. J., Han, A. W., Johnson, A. J., & Holmes, S. P. (2016). DADA2: High-resolution sample inference from Illumina amplicon data. Nature Methods, 13, 581–583. https://doi.org/10.1038/nmeth.3869. DOI: https://doi.org/10.1038/nmeth.3869
Camacho-Cruz, K., Rey-Villiers, N., Ortiz-Hernández, M. C., González-Jones, P., Galán-Caamal, R. J., Matus-Hernández, M., & Sánchez, A. (2022). Changes in the enrichment of dissolved inorganic nutrients in the coastal waters of the Mexican Caribbean, influenced by submarine groundwater discharges 2016–2019. Marine Pollution Bulletin, 185(Part A), 114308. https://doi.org/10.1016/j.marpolbul.2022.114308. DOI: https://doi.org/10.1016/j.marpolbul.2022.114308
Caporaso, J. G., Lauber, C. L., Walters, W. A., Berg-Lyons, D., Huntley, J., Fierer, N., Owens, S. M., Betley, J., Fraser, L., Bauer, M., Gormley, N., Gilbert, J. A., Smith, G., & Knight, R. (2012). Ultra-high-throughput microbial community analysis on the Illumina HiSeq and MiSeq platforms. The ISME Journal, 6(8), 1621–1624. https://doi.org/10.1038/ismej.2012.8. DOI: https://doi.org/10.1038/ismej.2012.8
Carranza-Ramirez, A., Calva-Benítez, L. G., & Núñez-Reséndiz, M. L. (2023). Taxonomic composition and substrate affinity of conspicuous marine macroalgae of the Parque Nacional Arrecifes de Cozumel, Quintana Roo, Mexico. Acta botánica mexicana, 130, e2249. https://doi.org/10.21829/abm130.2023.2249. DOI: https://doi.org/10.21829/abm130.2023.2249
Castañeda-Chávez, M. R., Lango-Reynoso, F., García-Fuentes, J. L., & Reyes-Aguilar, Á. R. (2018). Bacteria that affects coral health with an emphasis on the Gulf of Mexico and the Caribbean Sea. Latin American Journal of Aquatic Research, 46(5). https://dx.doi.org/10.3856/vol46-issue5-fulltext-2. DOI: https://doi.org/10.3856/vol46-issue5-fulltext-2
Choi, D. H., Hwang, C. Y., & Cho, B. C. (2009). Pelagibius litoralis gen. nov., sp. nov., a marine bacterium in the family Rhodospirillaceae isolated from coastal seawater. International Journal of Systematic and Evolutionary Microbiology, 59, 818–823. https://doi.org/10.1099/ijs.0.002774-0. DOI: https://doi.org/10.1099/ijs.0.002774-0
Chu, N. D., & Vollmer, S. V. (2016). Caribbean corals house shared and host-specific microbial symbionts over time and space. Environmental Microbiology Reports, 8, 493–500. https://doi.org/10.1111/1758-2229.12412. DOI: https://doi.org/10.1111/1758-2229.12412
Clarke, K. R., & Gorley, R. N. (2015). Primer v7: User manual/tutorial. Primer-E.
Correa, D., Villegas-Sánchez, C. A., Pérez-España, H., & Álvarez-Filip, L. (2025). Reef health status of the southwestern Gulf of Mexico and Mexican Caribbean coral reefs. Ciencias Marinas, 50(1B), e3501. https://doi.org/10.7773/cm.y2025.3501. DOI: https://doi.org/10.7773/cm.y2025.3501
Coskun, Ö. K., Orsi, W. D., D’Hondt, S., & Gomez-Saez, G. V. (2025). Identifying the active microbes driving organosulfur cycling from taurine and methionine in marine sediment. ISME Communications, 5(1), ycaf033. https://doi.org/10.1093/ismeco/ycaf033. DOI: https://doi.org/10.1093/ismeco/ycaf033
Custer, G. F., Gans, M., van-Diepen, L. T. A., Dini-Andreote, F., & Buerkle, C. A. (2023). Comparative analysis of core microbiome assignments: Implications for ecological synthesis. mSystems, 8(1), e01066-22. https://doi.org/10.1128/msystems.01066-22. DOI: https://doi.org/10.1128/msystems.01066-22
Daims, H., Lücker, S., & Wagner, M. (2016). A new perspective on microbes formerly known as nitrite-oxidizing bacteria. Trends in Microbiology, 24(9), 709–715. https://doi.org/10.1016/j.tim.2016.05.004. DOI: https://doi.org/10.1016/j.tim.2016.05.004
De-Almeida, L. R., Ávila-Mosqueda, S. V., Mendoza, E., van-Tussenbroek, B. I., & Silva, R. (2024). Beyond the beach: Multi-parameter interpretation of shore deterioration in a Caribbean reef system. Diversity, 16(5), 266. https://doi.org/10.3390/d16050266. DOI: https://doi.org/10.3390/d16050266
Dubé, M. K., Barradas-Ortiz, C., Negrete-Soto, F., Álvarez-Filip, L., Lozano-Álvarez, E., & Briones-Fourzán, P. (2023). A shift in communities of conspicuous macrocrustaceans associated with Caribbean coral reefs following a series of environmental stressors. Diversity, 15(7), 809. https://doi.org/10.3390/d15070809. DOI: https://doi.org/10.3390/d15070809
Durham, B. P., Grote, J., Whittaker, K. A., Bender, S. J., Luo, H., Grim, S. L., Brown, J. M., Casey, J. R., Dron, A., Florez-Leiva, L., Krupke, A., Luria, C. M., Mine, A. H., Nigro, O. D., Pather, S., Talarmin, A., Wear, E. K., Weber, T. S., Wilson, J. M., Rappé, M. S. (2014). Draft genome sequence of marine alphaproteobacterial strain HIMB11, the first cultivated representative of a unique lineage within the Roseobacter clade possessing an unusually small genome. Standards in Genomic Sciences, 9(3), 632–645. https://doi.org/10.4056/sigs.4998989. DOI: https://doi.org/10.4056/sigs.4998989
Galand, P. E., Casamayor, E. O., Kirchman, D. L., & Lovejoy, C. (2009). Ecology of the rare microbial biosphere of the Arctic Ocean. Proceedings of the National Academy of Sciences of the USA, 106, 22427–22432. https://doi.org/10.1073/pnas.0908284106. DOI: https://doi.org/10.1073/pnas.0908284106
Galperin, M. Y. (2013). Genome diversity of spore-forming firmicutes. Microbiology Spectrum, 1(2), TBS-0015-2012. https://doi.org/10.1128/microbiolspectrum.tbs-0015-2012. DOI: https://doi.org/10.1128/microbiolspectrum.TBS-0015-2012
Glasl, B., Bourne, D. G., Frade, P. R., Thomas, T., Schaffelke, B., & Webster, N. S. (2019). Microbial indicators of environmental perturbations in coral reef ecosystems. Microbiome, 7, 94. https://doi.org/10.1186/s40168-019-0705-7. DOI: https://doi.org/10.1186/s40168-019-0705-7
Hernández-Agreda, A., Gates, R. D., & Ainsworth, T. D. (2017). Defining the core microbiome in corals’ microbial soup. Trends in Microbiology, 25, 125–140. https://doi.org/10.1016/j.tim.2016.11.003. DOI: https://doi.org/10.1016/j.tim.2016.11.003
Hernández-Agreda, A., Leggat, W., Bongaerts, P., & Ainsworth, T. D. (2016). The microbial signature provides insight into the mechanistic basis of coral success across reef habitats. mBio, 7, e00560-16. https://doi.org/10.1128/mbio.00560-16. DOI: https://doi.org/10.1128/mBio.00560-16
Hernández-Agreda, A., Leggat, W., Bongaerts, P., Herrera, C., & Ainsworth, T. D. (2018). Rethinking the coral microbiome: Simplicity exists within a diverse microbial biosphere. mBio, 9(5), e00812-18. https://doi.org/10.1128/mbio.00812-18. DOI: https://doi.org/10.1128/mBio.00812-18
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, 196. https://doi.org/10.1093/femsec/fiw196. DOI: https://doi.org/10.1093/femsec/fiw196
Hernández-Zulueta, J., Araya, R., Vargas-Ponce, O., Rodríguez-Troncoso, A. P., Echeverria-Vega, A., López-Pérez, A., Ríos-Jara, E., & Rodríguez-Zaragoza, F. A. (2025). Underexplored rare bacterial biosphere associated with corals of the northeastern Tropical Eastern Pacific. Discover Oceans, 2(1), 4. https://doi.org/10.1007/s44289-024-00040-7. DOI: https://doi.org/10.1007/s44289-024-00040-7
Hernández-Zulueta, J., Díaz-Pérez, L., Echeverría-Vega, A., Nava-Martínez, G. G., García-Salgado, M. Á., & Rodríguez-Zaragoza, F. A. (2023). An update of knowledge of the bacterial assemblages associated with the Mexican Caribbean corals Acropora palmata, Orbicella faveolata, and Porites porites. Diversity, 15(9), 964. https://doi.org/10.3390/d15090964. DOI: https://doi.org/10.3390/d15090964
Hester, E. R., Barott, K. L., Nulton, J., Vermeij, M. J., & Rohwer, F. L. (2015). Stable and sporadic symbiotic communities of coral and algal holobionts. The ISME Journal, 10, 1157–1169. https://doi.org/10.1038/ismej.2015.190. DOI: https://doi.org/10.1038/ismej.2015.190
Hoffmann, K., Bienhold, C., Buttigieg, P. L., Knittel, K., Laso-Pérez, R., Rapp, J. Z., Boetius, A., & Offre, P. (2020). Diversity and metabolism of Woeseiales bacteria, global members of marine sediment communities. The ISME Journal, 14(4), 1042–1056. https://doi.org/10.1038/s41396-020-0588-4. DOI: https://doi.org/10.1038/s41396-020-0588-4
Hutchings, B., López-Legentil, S., Stefaniak, L. M., Nydam, M. L., & Erwin, P. M. (2025). Depuration of a solitary ascidian depletes transient bacteria without altering microbiome alpha-diversity. FEMS Microbiology Ecology, 101(8), fiaf078. https://doi.org/10.1093/femsec/fiaf078. DOI: https://doi.org/10.1093/femsec/fiaf078
Hutchins, D. A., Jansson, J. K., Remais, J. V., Rich, V. I., Singh, B. K., & Trivedi, P. (2019). Climate change microbiology – problems and perspectives. Nature Reviews Microbiology, 17(6), 391–396. https://doi.org/10.1038/s41579-019-0178-5. DOI: https://doi.org/10.1038/s41579-019-0178-5
Irudayarajan, L., Ravindran, C., & Raveendran, H. P. (2023). Antimicrobial activity of coral-associated beneficial bacteria against coral disease-causing microbial pathogens. Journal of Basic Microbiology, 63. https://doi.org/10.1002/jobm.202300338. DOI: https://doi.org/10.1002/jobm.202300338
Jousset, A., Bienhold, C., Chatzinotas, A., Gallien, L., Gobet, A., Kurm, V., Küsel, K., Rillig, M. C., Rivett, D. W., Salles, J. F., van der Heijden, M. G., Youssef, N. H., Zhang, X., Wei, Z., & Hol, W. H. (2017). Where less may be more: How the rare biosphere pulls ecosystems strings. The ISME Journal, 11(4), 853–862. https://doi.org/10.1038/ismej.2016.174. DOI: https://doi.org/10.1038/ismej.2016.174
Kellogg, C. A. (2019). Microbiomes of stony and soft deep-sea corals share rare core bacteria. Microbiome, 7, 90. https://doi.org/10.1186/s40168-019-0697-3. DOI: https://doi.org/10.1186/s40168-019-0697-3
Kemp, K. M., Westrich, J. R., Alabady, M. S., Edwards, M. L., & Lipp, E. K. (2018). Abundance and multilocus sequence analysis of Vibrio bacteria associated with diseased elkhorn coral (Acropora palmata) of the Florida Keys. Applied and Environmental Microbiology, 84(2), e01035-17. https://doi.org/10.1128/aem.01035-17. DOI: https://doi.org/10.1128/AEM.01035-17
Khalil, H., Mahmoud, M., Kotb, M., & Eissa, A. E. (2024). Marine pollution as a trigger of discoloration phenomenon in the hard coral Pocillopora species at the Gulf of Aqaba, Red Sea, Egypt: Pathological and molecular evidences. Journal of Applied Veterinary Sciences, 9(4), 42–53.
https://doi.org/10.21608/javs.2024.302491.1369. DOI: https://doi.org/10.21608/javs.2024.302491.1369
Kuek, F. W. I., Motti, C. A., Zhang, J., Cooke, I. R., Todd, J. D., Miller, D. J., Bourne, D. G., & Raina, J. B. (2022). DMSP production by coral-associated bacteria. Frontiers in Marine Science, 9, 869574. https://doi.org/10.3389/fmars.2022.869574. DOI: https://doi.org/10.3389/fmars.2022.869574
Lamy, D., Obernosterer, I., Laghdass, M., Artigas, L. F., Breton, E., Grattepanche, J. D., Lecuyer, E., Degros, N., Lebaron, P., & Christaki, U. (2009). Temporal changes of major bacterial groups and bacterial heterotrophic activity during a Phaeocystis globosa bloom in the eastern English Channel. Aquatic Microbial Ecology, 58, 95–107. https://doi.org/10.3354/ame. DOI: https://doi.org/10.3354/ame01359
Lee, O. O., Yang, J., Bougouffa, S., Wang, Y., Batang, Z., Tian, R., Al-Suwailem, A., & Qian, P. Y. (2012). Spatial and species variations in bacterial communities associated with corals from the Red Sea as revealed by pyrosequencing. Applied and Environmental Microbiology, 78(20), 7173–7184. https://doi.org/10.1128/aem.01111-12. DOI: https://doi.org/10.1128/AEM.01111-12
Lema, K. A., Clode, P. L., Kilburn, M. R., Thornton, R., Willis, B. L., & Bourne, D. G. (2015). Imaging the uptake of nitrogen-fixing bacteria into larvae of the coral Acropora millepora. The ISME Journal, 10, 1–5. https://doi.org/10.1038/ismej.2015.229. DOI: https://doi.org/10.1038/ismej.2015.229
Litchman, E., Villéger, S., Zinger, L., Auguet, J. C., Thuiller, W., Munoz, F., Kraft, N. J. B., Philippot, L., & Violle, C. (2024). Refocusing the microbial rare biosphere concept through a functional lens. Trends in Ecology & Evolution, 39(10), 923–936. https://doi.org/10.1016/j.tree.2024.06.005. DOI: https://doi.org/10.1016/j.tree.2024.06.005
Liu, Y., Hua, Y., Yi, Y., Liu, J., & Fu, P. (2025). Coral-associated bacteria provide alternative nitrogen source for Symbiodiniaceae growth in oligotrophic environment. Microorganisms, 13(4), 748. https://doi.org/10.3390/microorganisms13040748. DOI: https://doi.org/10.3390/microorganisms13040748
Lorenzo-Jiménez, Y., Gutiérrez-Estrada, G., Carricart-Ganivet, J. P., & Tortolero-Langarica, J. A. (2024). Effect of environmental light conditions on the growth of the coral Orbicella faveolata in the Mexican Caribbean. Ciencias Marinas, 50(1B). https://doi.org/10.7773/cm.y2024.3497. DOI: https://doi.org/10.7773/cm.y2024.3497
Louca, S., Jacques, S. M. S., Pires, A. P. F., Leal, J. S., González, A. L., Doebeli, M., & Farjalla, V. F. (2017). Functional structure of the bromeliad tank microbiome is strongly shaped by local geochemical conditions. Environmental Microbiology, 19(8), 3132–3151. https://doi.org/10.1111/1462-2920.13788. DOI: https://doi.org/10.1111/1462-2920.13788
Louca, S., Jacques, S. M. S., Pires, A. P. F., Leal, J. S., Srivastava, D. S., Parfrey, L. W., & Doebeli, M. (2016). High taxonomic variability despite stable functional structure across microbial communities. Nature Ecology & Evolution, 1(1), 0015. https://doi.org/10.1038/s41559-016-0015. DOI: https://doi.org/10.1038/s41559-016-0015
Lynch, M. D. J., & Neufeld, J. D. (2015). Ecology and exploration of the rare biosphere. Nature Reviews Microbiology, 13(4), 217–229. https://doi.org/10.1038/nrmicro3400. DOI: https://doi.org/10.1038/nrmicro3400
Maire, J., & van-Oppen, M. J. H. (2022). A role for bacterial experimental evolution in coral bleaching mitigation? Trends in Microbiology, 30, 217–228. https://doi.org/10.1016/j.tim.2021.07.006. DOI: https://doi.org/10.1016/j.tim.2021.07.006
Martínez-Servín, F., López-Arroyo, Y. M., Moreno-Vázquez, A. L., Robertson, D. R., Arredondo-Chávez, A. T., Sánchez-Jiménez, J. A., Ávila-Morales, O. G., Madrigal-Guridi, X., Caballero-Vázquez, J. A., Schmitter-Soto, J. J., Domínguez-Domínguez, O., & Solís-Guzmán, M. G. (2023). New records of ray-finned fishes (Actinopterygii) from Puerto Morelos Reef National Park (Mexican Caribbean). Acta Ichthyologica et Piscatoria, 53, 107–122. https://doi.org/10.3897/aiep.53.101239. DOI: https://doi.org/10.3897/aiep.53.101239
Medina-Valmaseda, A. E., Rodríguez-Martínez, R. E., Álvarez-Filip, L., Jordan-Dahlgren, E., & Blanchon, P. (2020). The role of geomorphic zonation in long-term changes in coral-community structure on a Caribbean fringing reef. PeerJ, 11, 1–23. https://peerj.com/articles/10103.pdf. DOI: https://doi.org/10.7717/peerj.10103
Messer, L. F., Bourne, D. G., Robbins, S. J., Clay, M., Bell, S. C., McIlroy, S. J., & Tyson, G. W. (2024). A genome-centric view of the role of the Acropora kenti microbiome in coral health and resilience. Nature Communications, 15, 2902. https://doi.org/10.1038/s41467-024-46905-5. DOI: https://doi.org/10.1038/s41467-024-46905-5
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 Microbiology Reviews, 47(2), fuad005. https://doi.org/10.1093/femsre/fuad005. DOI: https://doi.org/10.1093/femsre/fuad005
Neave, M. J., Rachmawati, R., Xun, L., Michell, C. T., Bourne, D. G., Apprill, A., & Voolstra, C. R. (2017). Differential specificity between closely related corals and abundant Endozoicomonas endosymbionts across global scales. The ISME Journal, 11, 186–200. https://doi.org/10.1038/ismej.2016.95. DOI: https://doi.org/10.1038/ismej.2016.95
Neu, A. T., Allen, E. E., & Roy, K. (2021). Defining and quantifying the core microbiome: Challenges and prospects. Proceedings of the National Academy of Sciences of the United States of America, 118(51), e2104429118. https://doi.org/10.1073/pnas.2104429118. DOI: https://doi.org/10.1073/pnas.2104429118
Ostria-Hernández, M. L., Hernández-Zulueta, J., Vargas-Ponce, O., Díaz-Pérez, L., Araya, R., Rodríguez-Troncoso, A. P., Ríos-Jara, E., & Rodríguez-Zaragoza, F. A. (2022). Core microbiome of corals Pocillopora damicornis and Pocillopora verrucosa in the northeastern tropical Pacific. Marine Ecology, e12729. https://doi.org/10.1111/maec.12729. DOI: https://doi.org/10.1111/maec.12729
Pascoal, F., Branco, P., Torgo, L., Costa, R., & Magalhães, C. (2025). Definition of the microbial rare biosphere through unsupervised machine learning. Communications Biology, 8, 544. https://doi.org/10.1038/s42003-025-07912-4. DOI: https://doi.org/10.1038/s42003-025-07912-4
Pascoal, F., Costa, R., & Magalhães, C. (2021). The microbial rare biosphere: Current concepts, methods and ecological principles. FEMS Microbiology Ecology, 97(1), fiaa227. https://doi.org/10.1093/femsec/fiaa227. DOI: https://doi.org/10.1093/femsec/fiaa227
Pascoal, F., Magalhães, C., & Costa, R. (2020). The link between the ecology of the prokaryotic rare biosphere and its biotechnological potential. Frontiers in Microbiology, 11, 231. https://doi.org/10.3389/fmicb.2020.00231. DOI: https://doi.org/10.3389/fmicb.2020.00231
Pedrós-Alió, C. (2012). The rare bacterial biosphere. Annual Review of Marine Science, 4, 449–466. https://doi.org/10.1146/annurev-marine-120710-100948. DOI: https://doi.org/10.1146/annurev-marine-120710-100948
Pérez-Gómez, J. A., García-Mendoza, E., Olivos-Ortiz, A., Paytan, A., Rebolledo-Vieyra, M., Delgado-Pech, B., & Almazán-Becerril, A. (2020). Indicators of nutrient enrichment in coastal ecosystems of the northern Mexican Caribbean. Ecological Indicators, 118, 106756. https://doi.org/10.1016/j.ecolind.2020.106756. DOI: https://doi.org/10.1016/j.ecolind.2020.106756
Pester, M., Bittner, N., Deevong, P., Wagner, M., & Loy, A. (2010). A “rare biosphere” microorganism contributes to sulfate reduction in a peatland. The ISME Journal, 4(12), 1591–1602. https://doi.org/10.1038/ismej.2010.75. DOI: https://doi.org/10.1038/ismej.2010.75
Pollock, F. J., McMinds, R., Smith, S., Bourne, D. G., Willis, B. L., Medina, M., Thurber, R. V., & Zaneveld, J. R. (2018). Coral-associated bacteria demonstrate phylosymbiosis and cophylogeny. Nature Communications, 9, 4921. https://doi.org/10.1038/s41467-018-07275-x. DOI: https://doi.org/10.1038/s41467-018-07275-x
Pootakham, W., Mhuantong, W., Yoocha, T., Putchim, L., Sonthirod, C., Naktang, C., Thongtham, N., & Tangphatsornruang, S. (2017). High resolution profiling of coral-associated bacterial communities using full-length 16S rRNA sequence data from PacBio SMRT sequencing system. Scientific Reports, 7, 214. https://doi.org/10.1038/s41598-017-03139-4. DOI: https://doi.org/10.1038/s41598-017-03139-4
Prioux, C., Ferrier-Pagès, C., Lamarca, T., Allemand, D., & Tignat-Perrier, R. (2025). Heatwave-driven persistent microbes threaten the resilience of Mediterranean coral holobionts. Environmental Microbiome, 20, 107. https://doi.org/10.1186/s40793-025-00765-8. DOI: https://doi.org/10.1186/s40793-025-00765-8
Quast, C., Pruesse, E., Yilmaz, P., Gerken, J., Schweer, T., Yarza, P., Peplies, J., & Glöckner, F. O. (2013). The SILVA ribosomal RNA gene database project: Improved data processing and web-based tools. Nucleic Acids Research, 41(D1), D590–D596. https://doi.org/10.1093/nar/gks1219. DOI: https://doi.org/10.1093/nar/gks1219
Quintanilla, E., Rodrigues, C. F., Henriques, I., & Hilário, A. (2022). Microbial associations of abyssal gorgonians and anemones (>4,000 m depth) at the Clarion-Clipperton Fracture Zone. Frontiers in Microbiology, 13, 828469. https://doi.org/10.3389/fmicb.2022.828469. DOI: https://doi.org/10.3389/fmicb.2022.828469
Raina, J. B., Dinsdale, E. A., Willis, B. L., & Bourne, D. G. (2010). Do the organic sulfur compounds DMSP and DMS drive coral microbial associations? Trends in Microbiology, 18, 101–108. https://doi.org/10.1016/j.tim.2009.12.002. DOI: https://doi.org/10.1016/j.tim.2009.12.002
Randazzo-Eisemann, Á., Garza-Pérez, J. R., Penié-Rodríguez, I., & Figueroa-Zavala, B. (2021). 25 years of multiple stressors driving the coral–algae phase shift in Akumal, Mexico. Ocean & Coastal Management, 214, 105917. https://doi.org/10.1016/j.ocecoaman.2021.105917. DOI: https://doi.org/10.1016/j.ocecoaman.2021.105917
Rioja-Nieto, R., & Álvarez-Filip, L. (2019). Coral reef systems of the Mexican Caribbean: Status, recent trends and conservation. Marine Pollution Bulletin, 140, 615–625. https://doi.org/10.1016/j.marpolbul.2018.07.005. DOI: https://doi.org/10.1016/j.marpolbul.2018.07.005
Risely, A. (2020). Applying the core microbiome to understand host–microbe systems. Journal of Animal Ecology, 89(7), 1549–1558. https://doi.org/10.1111/1365-2656.13229. DOI: https://doi.org/10.1111/1365-2656.13229
Roche, R. C., Williams, G. J., & Turner, J. R. (2018). Towards developing a mechanistic understanding of coral reef resilience to thermal stress across multiple scales. Current Climate Change Reports, 4, 51–64. https://doi.org/10.1007/s40641-018-0087-0. DOI: https://doi.org/10.1007/s40641-018-0087-0
Rodrigues, J. L. M., Pellizari, V. H., Mueller, R., Baek, K., Jesus, E. da C., Paula, F. S., Mirza, B., Hamaoui, G. S., Jr., Tsai, S. M., Feigl, B., Tiedje, J. M., Bohannan, B. J. M., & Nüsslein, K. (2013). Conversion of the Amazon rainforest to agriculture results in biotic homogenization of soil bacterial communities. Proceedings of the National Academy of Sciences, 110(3), 988–993. https://doi.org/10.1073/pnas.1220608110. DOI: https://doi.org/10.1073/pnas.1220608110
Rodríguez-Zaragoza, F. A., & Arias-González, J. E. (2015). Coral biodiversity and bio-construction in the northern sector of the Mesoamerican Reef System. Frontiers in Marine Science, 2, 13. https://doi.org/10.3389/fmars.2015.00013. DOI: https://doi.org/10.3389/fmars.2015.00013
Rohwer, F., Seguritan, V., Azam, F., & Knowlton, N. (2002). Diversity and distribution of coral-associated bacteria. Marine Ecology Progress Series, 243, 1–10. https://doi.org/10.3354/meps243001. DOI: https://doi.org/10.3354/meps243001
Rosenberg, E., Koren, O., Reshef, L., Efrony, R., & Zilber-Rosenberg, I. (2007). The role of microorganisms in coral health, disease and evolution. Nature Reviews Microbiology, 5(5), 355–362. https://doi.org/10.1038/nrmicro1635. DOI: https://doi.org/10.1038/nrmicro1635
Rubio-Cisneros, N. T., Escalera-Briceño, A., Rubio-Cisneros, I. I., González-Rodríguez, L. S., González-Rojas, J. I., Ruiz-Ayma, G., Guzmán-Velasco, A. (2026). Tourist Environmental Awareness and Conservation Engagement in a Caribbean Marine Protected Island System: Evidence from Cozumel, Mexico. Coasts, 6, 36. https://doi.org/10.3390/coasts6030036. DOI: https://doi.org/10.3390/coasts6030036
Rubio-Portillo, E., Santos, F., Ascaso, C., Souza-Egipsy, V., & Antón, J. (2016). Structure and temporal dynamics of the bacterial communities associated to microhabitats of the coral Oculina patagonica. Environmental Microbiology, 18, 4564–4578. https://doi.org/10.1111/1462-2920.13548. DOI: https://doi.org/10.1111/1462-2920.13548
Sang, V. T., Dat, T. T. H., Vinh, L. B., Cuong, L. C. V., Oanh, P. T. T., Ha, H., Kim, Y. H., Anh, H. L. T., & Yang, S. Y. (2019). Coral and coral-associated microorganisms: A prolific source of potential bioactive natural products. Marine Drugs, 17, 468. https://doi.org/10.3390/md17080468. DOI: https://doi.org/10.3390/md17080468
Shade, A., Jones, S. E., Caporaso, J. G., Handelsman, J., Knight, R., Fierer, N., & Gilbert, J. A. (2014). Conditionally rare taxa disproportionately contribute to temporal changes in microbial diversity. mBio, 5(4), e01371-14. https://doi.org/10.1128/mbio.01371-14. DOI: https://doi.org/10.1128/mBio.01371-14
Sunagawa, S., Woodley, C. M., & Medina, M. (2010). Threatened corals provide underexplored microbial habitats. PLOS One, 5(3), e9554. https://doi.org/10.1371/journal.pone.0009554. DOI: https://doi.org/10.1371/journal.pone.0009554
Takagi, T., Aoyama, K., Motone, K., Aburaya, S., Yamashiro, H., Miura, N., & Inoue, K. (2023). Mutualistic interactions between dinoflagellates and pigmented bacteria mitigate environmental stress. Microbiology Spectrum, 11(1), e02464-22. https://doi.org/10.1128/spectrum.02464-22. DOI: https://doi.org/10.1128/spectrum.02464-22
Taylor, M. W., Tsai, P., Simister, R. L., Deines, P., Botte, E., Ericson, G., Schmitt, S., & Webster, N. S. (2013). “Sponge-specific” bacteria are widespread (but rare) in diverse marine environments. The ISME Journal, 7(2), 438–443. https://doi.org/10.1038/ismej.2012.111. DOI: https://doi.org/10.1038/ismej.2012.111
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. DOI: https://doi.org/10.3389/fcimb.2014.00176
Van-Oppen, M. J. H., & Blackall, L. L. (2019). Coral microbiome dynamics, functions and design in a changing world. Nature Reviews Microbiology, 17(9), 557–567. https://doi.org/10.1038/s41579-019-0223-4. DOI: https://doi.org/10.1038/s41579-019-0223-4
Van-Oppen, M. J. H., Doering, T., & Martins Fernandes, L. (2026). Can bacterial manipulation deliver reef-scale thermal enhancement of corals? Microorganisms, 14(1), 202. https://doi.org/10.3390/microorganisms14010202. DOI: https://doi.org/10.3390/microorganisms14010202
Vanwonterghem, I., & Webster, N. S. (2020). Coral reef microorganisms in a changing climate. iScience, 23(4), 100972. https://doi.org/10.1016/j.isci.2020.100972. DOI: https://doi.org/10.1016/j.isci.2020.100972
Vigneron, A., Cruaud, P., Alsop, E., de-Rezende, J. R., Head, I. M., & Tsesmetzis, N. (2018). Beyond the tip of the iceberg: A new view of the diversity of sulfite- and sulfate-reducing microorganisms. The ISME Journal, 12(8), 2096–2099. https://doi.org/10.1038/s41396-018-0155-4. DOI: https://doi.org/10.1038/s41396-018-0155-4
Villela, L. B., da-Silva-Lima, A. W., Moreira, A. P. B., Aiube, Y. R. A., Ribeiro, F. V., Villela, H. D. M., Majzoub, M. E., Amario, M., de-Moura, R. L., Thomas, T., Peixoto, R. S., & Salomón, P. S. (2024). Bacterial and Symbiodiniaceae communities in corals with distinct traits and geographic distribution. Scientific Reports, 14, 24319. https://doi.org/10.1038/s41598-024-70121-2. DOI: https://doi.org/10.1038/s41598-024-70121-2
Voolstra, C. R., Raina, J. B., Dörr, M., Cárdenas, A., Pogoreutz, C., Silveira, C. B., Mohamed, A. R., Bourne, D. G., Luo, H., Amin, S. A., & Peixoto, R. S. (2024). The coral microbiome in sickness, in health and in a changing world. Nature Reviews Microbiology, 22, 460–475. https://doi.org/10.1038/s41579-024-01015-3. DOI: https://doi.org/10.1038/s41579-024-01015-3
Zhang, Y., Ling, J., Yang, Q., Wen, C., Yan, Q., Sun, H., Van-Nostrand, J. D., Shi, Z., Zhou, J., & Dong, J. (2015). The functional gene composition and metabolic potential of coral-associated microbial communities. Scientific Reports, 5, 16191. https://doi.org/10.1038/srep16191. DOI: https://doi.org/10.1038/srep16191
Additional Files
Published
Issue
Section
License
Copyright (c) 2026 Revista de Biología Tropical

This work is licensed under a Creative Commons Attribution 4.0 International License.
Creative Commons Attribution 4.0 License (CC BY 4.0)
Attribution (BY) • (BY) You must attribute the work in the manner specified by the author or licensor (but not in any way that suggests that they endorse you or your use of the work).
