Abstract
Coral diseases impact reefs globally. Although we continue to describe diseases, little is known about the etiology or progression of even the most common cases. To examine a spectrum of coral health and determine factors of disease progression we examined Orbicella faveolata exhibiting signs of Yellow Band Disease (YBD), a widespread condition in the Caribbean. We used a novel combined approach to assess three members of the coral holobiont: the coral-host, associated Symbiodinium algae, and bacteria. We profiled three conditions: (1) healthy-appearing colonies (HH), (2) healthy-appearing tissue on diseased colonies (HD), and (3) diseased lesion (DD). Restriction fragment length polymorphism analysis revealed health state-specific diversity in Symbiodinium clade associations. 16S ribosomal RNA gene microarrays (PhyloChips) and O. faveolata complimentary DNA microarrays revealed the bacterial community structure and host transcriptional response, respectively. A distinct bacterial community structure marked each health state. Diseased samples were associated with two to three times more bacterial diversity. HD samples had the highest bacterial richness, which included components associated with HH and DD, as well as additional unique families. The host transcriptome under YBD revealed a reduced cellular expression of defense- and metabolism-related processes, while the neighboring HD condition exhibited an intermediate expression profile. Although HD tissue appeared visibly healthy, the microbial communities and gene expression profiles were distinct. HD should be regarded as an additional (intermediate) state of disease, which is important for understanding the progression of YBD.
Similar content being viewed by others
Log in or create a free account to read this content
Gain free access to this article, as well as selected content from this journal and more on nature.com
or
References
Ainsworth TD, Vega Thurber R, Gates R . (2009). The future of coral reefs: a microbial perspective. Trends Ecol Evol 25: 233–240.
Alagely A, Krediet CJ, Ritchie KB, Teplitski M . (2011). Signaling-mediated cross-talk modulates swarming and biofilm formation in a coral pathogen Serratia marcescens. ISME J 5: 1609–1620.
Anderluh G, Krizaj I, Strukelj B, Gubensek F, Macek P, Pungercar J . (1999). Equinatoxins, pore-forming proteins from the sea anemone Actinia equina, belong to a multigene family. Toxicon 37: 1391–1401.
Aranda M, Banaszak AT, Bayer T, Luyten JR, Medina M, Voolstra CR . (2011). Differential sensitivity of coral larvae to natural levels of ultraviolet radiation during the onset of larval competence. Mol Ecol 20: 2955–2972.
Barshis DJ, Ladner JT, Oliver TA, Seneca FO, Traylor-Knowles N, Palumbi SR . (2013). From the cover: genomic basis for coral resilience to climate change. Proc Natl Acad Sci USA 110: 1387–1392.
Bellantuono AJ, Granados-Cifuentes C, Miller DJ, Hoegh-Guldberg O, Rodriguez-Lanetty M . (2012). Coral thermal tolerance: tuning gene expression to resist thermal stress. PLoS One 7: e50685.
Benjamini Y, Hochberg Y . (1995). Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc Ser B 57: 289–300.
Bourne DG, Dennis PG, Uthicke S, Soo RM, Tyson GW, Webster N . (2013). Coral reef invertebrate microbiomes correlate with the presence of photosymbionts. ISME J 7: 1452–1458.
Bourne DG, Garren M, Work T, Rosenberg E, Smith G, Harvell CD . (2009). Microbial disease and the coral holobiont. Trends Microbiol 17: 554–562.
Brandt ME, McManus J . (2009). Disease incidence is related to bleaching extent in reef-building corals. Ecology 90: 2859–2861.
Brodie EL, DeSantis TZ, Joyner D, Joyner DC, Baek SM, Larsen JT et al. (2006). Application of a high-density oligonucleotide microarray approach to study bacterial population dynamics during uranium reduction and reoxidation. Appl Environ Microbiol 72: 6288–6298.
Bruckner AW, Bruckner RJ . (2006). Consequences of yellow band disease (YBD) on Montastraea annularis (species complex) populations on remote reefs off Mona Island, Puerto Rico. Dis Aquat Org 69: 67–73.
Bruno JF, Petes LE, Harvell CD, Hettinger A . (2003). Nutrient enrichment can increase the severity of coral diseases. Ecol Lett 6: 1056–1061.
Bruno JF, Selig ER, Casey KS, Page CA, Willis BL, Harvell CD et al. (2007). Thermal stress and coral cover as drivers of coral disease outbreaks. PLoS Biol 5: e124.
Budd AF, Fukami H, Smith ND, Knowlton N . (2012). Taxonomic classification of the reef coral family Mussidae (Cnidaria: Anthozoa: Scleractinia). Zoolog J Linn Soc 166: 465–529.
Cervino JM, Goreau T, Nagelkerken I, Smith G, Hayes R . (2001). Yellow band and dark spot syndromes in Caribbean corals: distribution, rate of spread, cytology, and effects on abundance and division rate of zooxanthellae. Hydrobiologia 460: 53–63.
Cervino JM, Hayes R, Polson S . (2004). Relationship of Vibrio species infection and elevated temperatures to yellow blotch/band disease in Caribbean corals. Appl Environ Microbiol 70: 6855–6864.
Cervino JM, Thompson F, Gomez-Gil B, Lorence E, Goreau T, Hayes R et al. (2008). The Vibrio core group induces yellow band disease in Caribbean and Indo-Pacific reef-building corals. J Appl Micro 105: 1658–1671.
Chimetto LA, Brocchi M, Thompson CC, Martins RCR, Ramos HR, Thompson FL . (2008). Vibrios dominate as culturable nitrogen-fixing bacteria of the Brazilian coral Mussismilia hispida. Syst Appl Microbiol 31: 312–319.
Comerford KM, Leonard MO, Karhausen J, Carey R, Colgan SP, Taylor CT . (2003). Small ubiquitin-related modifier-1 modification mediates resolution of CREB-dependent responses to hypoxia. Proc Natl Acad Sci USA 100: 986–991.
Connell JH . (1978). Diversity in tropical rain forests and coral reefs. Science 199: 1302–1310.
Costello EK, Stagaman K, Dethlefsen L, Bohannan BJM, Relman DA . (2012). The application of ecological theory toward an understanding of the human microbiome. Science 336: 1255–1262.
Cróquer A, Bastidas C, Elliott A, Sweet M . (2013). Bacterial assemblages shifts from healthy to yellow band disease states in the dominant reef coral Montastraea faveolata. Environ Microbiol Rep 5: 90–96.
Cunning J, Thurmond J, Smith G, Weil E, Ritchie KB . (2009). A survey of Vibrios associated with healthy and Yellow Band Diseased Montastraea faveolata. Proc 11th Intl Coral Reef Symp 7: 206–210.
Davies SW, Rahman M, Meyer E, Green EA, Buschiazzo E, Medina M et al. (2013). Novel polymorphic microsatellite markers for population genetics of the endangered Caribbean star coral, Montastraea faveolata. Mar Biodiv 43: 167–172.
DeSalvo MK, Estrada A, Sunagawa S, Medina M . (2012). Transcriptomic responses to darkness stress point to common coral bleaching mechanisms. Coral Reefs 31: 215–228.
DeSalvo MK, Sunagawa S, Fisher PL, Voolstra CR, Iglesias-Prieto R, Medina M . (2010). Coral host transcriptomic states are correlated with. Mol Ecol 19: 1174–1186.
DeSalvo MK, Voolstra CR, Sunagawa S, Schwarz JA, Stillman J, Coffroth M et al. (2008). Differential gene expression during thermal stress and bleaching in the Caribbean coral Montastraea faveolata. Mol Ecol 17: 3952.
Douglas AE . (1998). Nutritional interactions in insect-microbial symbioses: aphids and their symbiotic bacteria buchnera. Annu Rev Entomol 43: 17–37.
Dustan P . (1977). Vitality of reef coral populations off Key Largo, Florida: recruitment and mortality. Environ Geol 2: 51–58.
Gardner T, Côté I, Gill J, Grant A, Watkinson A . (2003). Long-term region-wide declines in Caribbean corals. Science 301: 958.
Garren M, Walsh SM, Caccone A, Knowlton N . (2006). Patterns of association between Symbiodinium and members of the Montastraea annularis species complex on spatial scales ranging from within colonies to between geographic regions. Coral Reefs 25: 503–512.
Hazen TC, Dubinsky EA, DeSantis TZ, Andersen GL, Piceno YM, Singh N et al. (2010). Deep-sea oil plume enriches indigenous oil-degrading bacteria. Science 330: 204–208.
Hughes TP, Graham NAJ, Jackson JBC, Mumby PJ, Steneck RS . (2010). Rising to the challenge of sustaining coral reef resilience. Trends Ecol Evol 25: 633–642.
Kaniewska P, Campbell PR, Kline DI, Rodriguez-Lanetty M, Miller DJ, Dove S et al. (2012). Major cellular and physiological impacts of ocean acidification on a reef building coral. PLoS One 7: e34659.
Kellogg CA, Piceno YM, Tom LM, DeSantis TZ, Zawada DG, Andersen GL . (2012). PhyloChip microarray comparison of sampling methods used for coral microbial ecology. J Microbiol Methods 88: 103–109.
Kimes NE, Van Nostrand JD, Weil E, Zhou J, Morris PJ . (2010). Microbial functional structure of Montastraea faveolata, an important Caribbean reef-building coral, differs between healthy and yellow-band diseased colonies. Environ Microbiol 12: 541–556.
Knowlton N, Jackson JBC . (2008). Shifting baselines, local impacts, and global change on coral reefs. PLoS Biol 6: e54.
Koenig JE, Bourne DG, Curtis B, Dlutek M, Stokes HW, Doolittle WF et al. (2011). Coral-mucus-associated Vibrio integrons in the Great Barrier Reef: genomic hotspots for environmental adaptation. ISME J 5: 962–972.
Krediet CJ, Ritchie KB, Paul VJ, Teplitski M . (2013). Coral-associated micro-organisms and their roles in promoting coral health and thwarting diseases. Proc Biol Sci 280: 20122328.
Lema KA, Willis BL, Bourne DG . (2012). Corals form characteristic associations with symbiotic nitrogen-fixing bacteria. Appl Environ Microbiol 78: 3136–3144.
Lesser MP, Mazel C, Gorbunov M, Falkowski P . (2004). Discovery of symbiotic nitrogen-fixing cyanobacteria in corals. Science 305: 997.
Mendes R, Kruijt M, De Bruijn I, Dekkers E, Van Der Voort M, Schneider JHM et al. (2011). Deciphering the rhizosphere microbiome for disease-suppressive bacteria. Science 332: 1097–1100.
Mouchka ME, Hewson I, Harvell CD . (2010). Coral-associated bacterial assemblages: current knowledge and the potential for climate-driven impacts. Integr Comp Biol 50: 662–674.
Muscatine L, Porter JW . (1977). Reef corals: mutualistic symbioses adapted to nutrient-poor environments. BioScience 27: 454–460.
Mydlarz LD, Couch CS, Weil E, Smith G, Harvell CD . (2009). Immune defenses of healthy, bleached and diseased Montastraea faveolata during a natural bleaching event. Dis Aquat Organ 87: 67–78.
Pandolfi JM, Bradbury RH, Sala E, Hughes TP, Bjorndal KA, Cooke RG et al. (2003). Global trajectories of the long-term decline of coral reef ecosystems. Science 301: 955–958.
Pollock FJ, Morris PJ, Willis BL, Bourne DG . (2011). The urgent need for robust coral disease diagnostics. PLoS Pathog 7: e1002183.
Portune KJ, Voolstra CR, Medina M, Szmant AM . (2010). Development and heat stress-induced transcriptomic changes during embryogenesis of the scleractinian coral Acropora palmata. Mar Genomics 3: 51–62.
Pungercar J, Anderluh G, Macek P, Gubensek F, Strukelj B . (1997). Sequence analysis of the cDNA encoding the precursor of equinatoxin V, a newly discovered hemolysin from the sea anemone Actinia equina. Biochim Biophys Acta 1341: 105–107.
R Core Team R: a Language And Environment For Statistical Computing. R Foundation for Statistical Computing: Vienna,. (2012).
Reeves L . (1994). Newly discovered: yellow band disease strikes keys reefs. Underwater USA 11: 16.
Richards Dona A, Cervino JM, Karachun V, Lorence E, Bartels E, Hughen K et al. (2008). Coral yellow band disease; current status in the caribbean, and links to new indo-pacific outbreaks. Proc 11th Intl Coral Reef Symp, 1–5.
Richardson LL . (1998). Coral diseases: what is really known? Trends Ecol Evol 13: 438–443.
Ritchie KB . (2006). Regulation of microbial populations by coral surface mucus and mucus-associated bacteria. Mar Ecol Prog Ser 322: 1–14.
Roder C, Arif C, Bayer T, Aranda M, Daniels C, Shibl A et al. (2014). Bacterial profiling of White Plague Disease in a comparative coral species framework. ISME J 8: 31–39.
Rodríguez-Román A, Hernández-Pech X, Thomé P, Enríquez S, Iglesias-Prieto R . (2006). Photosynthesis and light utilization in the Caribbean coral Montastraea faveolata recovering from a bleaching event. Limnology and Oceanography 51: 5702–2710.
Rohwer F, Breitbart M, Jara J, Azam F, Knowlton N . (2001). Diversity of bacteria associated with the Caribbean coral Montastraea franksi. Coral reefs 20: 85–91.
Rohwer F, Seguritan V, Azam F, Knowlton N . (2002). Diversity and distribution of coral-associated bacteria. Mar Ecol Prog Ser 243: 1–10.
Rowan R, Knowlton N . (1995). Intraspecific diversity and ecological zonation in coral-algal symbiosis. Proc Natl Acad Sci USA 92: 2850–2853.
Rowan R, Powers DA . (1991). Molecular genetic identification of symbiotic dinoflagellates(zooxanthellae). Mar Ecol Prog Ser 71: 65–73.
Saeed A, Sharov V, White J, Li J, Liang W, Bhagabati N et al. (2003). TM4: a free, open-source system for microarray data management and analysis. Biotechniques 34: 374–378.
Sekar R, Kaczmarsky LT, Richardson LL . (2009). Effect of freezing on PCR amplification of 16S rRNA genes from microbes associated with black band disease of corals. Appl Environ Microbiol 75: 2581–2584.
Smyth GK . (2004). Linear models and empirical Bayes methods for assessing differential expression in microarray experiments. Stat Appl Genet Mol Biol 3: 1–25.
Stat M, Morris E, Gates RD . (2008). Functional diversity in coral–dinoflagellate symbiosis. Proc Natl Acad Sci USA 105: 9256–9261.
Sunagawa S, DeSalvo MK, Voolstra CR, Reyes-Bermudez A, Medina M . (2009a). Identification and gene expression analysis of a taxonomically restricted cysteine-rich protein family in reef-building corals. PLoS One 4: e4865.
Sunagawa S, DeSantis TZ, Piceno YM, Brodie EL, DeSalvo MK, Voolstra CR et al. (2009b). Bacterial diversity and White Plague Disease-associated community changes in the Caribbean coral Montastraea faveolata. ISME J 3: 512–521.
Sunagawa S, Woodley C, Medina M . (2010). Threatened corals provide underexplored microbial habitats. PLoS One 5: e9554.
Sutherland K, Porter JW, Torres C . (2004). Disease and immunity in Caribbean and Indo-Pacific zooxanthellate corals. Mar Ecol Prog Ser 266: 273–302.
Thornhill DJ, Doubleday K, Kemp DW, Santos SR . (2010). Host hybridization alters specificity of cnidarian–dinoflagellate associations. Mar Ecol Prog Ser 420: 113–123.
Thornhill DJ, Lewis AM, Wham DC, Lajeunesse TC . (2013). Host-specialist lineages dominate the adaptive radiation of reef coral endosymbionts. Evolution 68: 352–367.
Trench RK . (1979). The cell biology of plant-animal symbiosis. Annu Rev Plant Physiol 30: 485–531.
Vega Thurber R, Willner-Hall D, Rodriguez-Mueller B, Desnues C, Edwards RA, Angly F et al. (2009). Metagenomic analysis of stressed coral holobionts. Environ Microbiol 11: 2148–2163.
Vogel BE, Hedgecock EM . (2001). Hemicentin, a conserved extracellular member of the immunoglobulin superfamily, organizes epithelial and other cell attachments into oriented line- shaped junctions. Development 128: 883–894.
Vogel BE, Muriel JM, Dong C, Xu X . (2006). Hemicentins: what have we learned from worms? Cell Res 16: 872–878.
Voolstra CR, Schnetzer J, Peshkin L, Randall CJ, Szmant AM, Medina M . (2009a). Effects of temperature on gene expression in embryos of the coral Montastraea faveolata. BMC Genomics 10: 627.
Voolstra CR, Schwarz JA, Schnetzer J, Sunagawa S, DeSalvo MK, Szmant AM et al. (2009b). The host transcriptome remains unaltered during the establishment of coral-algal symbioses. Mol Ecol 18: 1823–1833.
Wegley L, Edwards R, Rodriguez-Brito B, Liu H, Rohwer F . (2007). Metagenomic analysis of the microbial community associated with the coral Porites astreoides. Environ Microbiol 9: 2707–2719.
Weil E, Smith GW, Gil-Agudelo DL . (2006). Status and progress in coral reef disease research. Dis Aquat Organ 69: 1–7.
Wilkinson C . (2008) Status of Coral Reefs of the World: 2008. Global Coral Reef Monitoring Network and Reef and Rainforest Research Centre: Townsville, Australia, pp 1–304.
Wu C, Sercu B, Van De Werfhorst L, Wong J, DeSantis TZ, Brodie EL et al. (2010). Characterization of coastal urban watershed bacterial communities leads to alternative community-based indicators. PLoS One 5: 1–11.
Acknowledgements
We would like to thank the Instituto de Ciencias del Mar y Limnología (ICML), the Universidad Nacional Autónoma de México for providing facilities and collection permits. Additionally we would like to thank those at the ICML, as well as the Medina & Andersen Lab members who provided assistance in collecting the sample, and in experimental and analytical methods. Especially, Adan Guillermo Jordán-Garza, Julia Schnetzer and Erika M Diaz-Almeyda for helping with the sample collection. Nicholas R Polato & Elizabeth Green for genotyping coral colonies. Lauren M Tom for assistance with the analyses. Justin L Matthews for statistical input. Bishoy SK Kamel and Erika M Diaz-Almeyda for additional draft comments. This study was supported by NSF awards IOS 0644438 and IOS 0926906 from NSF to MM.
Author information
Authors and Affiliations
Corresponding authors
Ethics declarations
Competing interests
The authors declare no conflict of interest.
Additional information
Supplementary Information accompanies this paper on The ISME Journal website
Rights and permissions
About this article
Cite this article
Closek, C., Sunagawa, S., DeSalvo, M. et al. Coral transcriptome and bacterial community profiles reveal distinct Yellow Band Disease states in Orbicella faveolata. ISME J 8, 2411–2422 (2014). https://doi.org/10.1038/ismej.2014.85
Received:
Revised:
Accepted:
Published:
Issue date:
DOI: https://doi.org/10.1038/ismej.2014.85
Keywords
This article is cited by
-
Heterotrophy, microbiome, and location effects on restoration efficacy of the threatened coral Acropora palmata
Communications Earth & Environment (2023)
-
Characterization of bacterial community structure in two alcyonacean soft corals (Litophyton sp. and Sinularia sp.) from Chuuk, Micronesia
Coral Reefs (2022)
-
The microbial profile of a tissue necrosis affecting the Atlantic invasive coral Tubastraea tagusensis
Scientific Reports (2021)
-
Differential protein abundance associated with delayed regeneration of the scleractinian coral Montastraea cavernosa
Coral Reefs (2020)
-
Development of a transcriptomic database for 14 species of scleractinian corals
BMC Genomics (2019)


