Stable mucus-associated bacterial communities in bleached and healthy corals of Porites lobata from the Arabian Seas

Ghaida Hadaidi; Till Röthig; Lauren K. Yum; Maren Ziegler; Chatchanit Arif; Cornelia Roder; John Burt; Christian R. Voolstra

doi:10.1038/srep45362

journal article Open Access Mar 31, 2017

Stable mucus-associated bacterial communities in bleached and healthy corals of Porites lobata from the Arabian Seas

Ghaida Hadaidi Till Röthig

Lauren K. Yum Maren Ziegler Chatchanit Arif Cornelia Roder

John Burt Christian R. Voolstra

Scientific Reports Vol. 7 No. 1 · Springer Science and Business Media LLC

View at Publisher Save 10.1038/srep45362

Abstract

AbstractCoral reefs are subject to coral bleaching manifested by the loss of endosymbiotic algae from coral host tissue. Besides algae, corals associate with bacteria. In particular, bacteria residing in the surface mucus layer are thought to mediate coral health, but their role in coral bleaching is unknown. We collected mucus from bleached and healthy Porites lobata colonies in the Persian/Arabian Gulf (PAG) and the Red Sea (RS) to investigate bacterial microbiome composition using 16S rRNA gene amplicon sequencing. We found that bacterial community structure was notably similar in bleached and healthy corals, and the most abundant bacterial taxa were identical. However, fine-scale differences in bacterial community composition between the PAG and RS were present and aligned with predicted differences in sulfur- and nitrogen-cycling processes. Based on our data, we argue that bleached corals benefit from the stable composition of mucus bacteria that resemble their healthy coral counterparts and presumably provide a conserved suite of protective functions, but monitoring of post-bleaching survival is needed to further confirm this assumption. Conversely, fine-scale site-specific differences highlight flexibility of the bacterial microbiome that may underlie adjustment to local environmental conditions and contribute to the widespread success of Porites lobata.

Topics

No keywords indexed for this article. Browse by subject →

References

81

[1]

Knowlton, N. & Rohwer, F. Multispecies Microbial Mutualisms on Coral Reefs: The Host as a Habitat. Am Nat 162, S51–S62 (2003). 10.1086/378684

[2]

Rosenberg, E., Koren, O., Reshef, L., Efrony, R. & Zilber-Rosenberg, I. The role of microorganisms in coral health, disease and evolution. Nat Rev Micro 5, 355–362 (2007). 10.1038/nrmicro1635

[3]

Diversity and distribution of coral-associated bacteria

F Rohwer, V Seguritan, F Azam et al.

Marine Ecology Progress Series 10.3354/meps243001

[4]

Muscatine, L., Falkowski, P. G., Porter, J. W. & Dubinsky, Z. Fate of photosynthetic fixed carbon in light-adapted and shade-adapted colonies of the symbiotic coral Stylophora pistillata . Proc Roy Soc Ser B Biol Sci 222, 181–202 (1984).

[5]

Mouchka, M. E., Hewson, I. & Harvell, C. D. Coral-Associated Bacterial Assemblages: Current Knowledge and the Potential for Climate-Driven Impacts. Integr Comp Biol 50, 662–674 (2010). 10.1093/icb/icq061

[6]

Insights into the Coral Microbiome: Underpinning the Health and Resilience of Reef Ecosystems

David G. Bourne, Kathleen M. Morrow, Nicole S. Webster

Annual Review of Microbiology 2016 10.1146/annurev-micro-102215-095440

[7]

Koh, E. G. L. Do Scleractinian Corals Engage in Chemical Warfare Against Microbes? J Chem Ecol 23, 379–398 (1997). 10.1023/b:joec.0000006366.58633.f4

[8]

Ritchie. Regulation of microbial populations by coral surface mucus and mucus-associated bacteria. Mar Ecol Prog Ser 322, 1–14 (2006). 10.3354/meps322001

[9]

Rypien, K. L., Ward, J. R. & Azam, F. Antagonistic interactions among coral‐associated bacteria. Env Microbiol 12, 28–39 (2010). 10.1111/j.1462-2920.2009.02027.x

[10]

Metagenomic analysis of the microbial community associated with the coral Porites astreoides

Linda Wegley, Robert Edwards, Beltran Rodriguez‐Brito et al.

Environmental Microbiology 2007 10.1111/j.1462-2920.2007.01383.x

[11]

Roder, C., Bayer, T., Aranda, M., Kruse, M. & Voolstra, C. R. Microbiome structure of the fungid coral Ctenactis echinata aligns with environmental differences. Mol Ecol 24, 3501–3511 (2015). 10.1111/mec.13251

[12]

Ziegler, M. et al. Coral microbial community dynamics in response to anthropogenic impacts near a major city in the central Red Sea. Mar Pollut Bull 105, 629–640 (2016). 10.1016/j.marpolbul.2015.12.045

[13]

Roder, C. et al. Bacterial profiling of White Plague Disease in a comparative coral species framework. ISME J 8, 31–39 (2014). 10.1038/ismej.2013.127

[14]

Roder, C., Arif, C., Daniels, C., Weil, E. & Voolstra, C. R. Bacterial profiling of White Plague Disease across corals and oceans indicates a conserved and distinct disease microbiome. Molecular Ecology 23, 965–974 (2014). 10.1111/mec.12638

[15]

Bourne, D. G. & Munn, C. B. Diversity of bacteria associated with the coral Pocillopora damicornis from the Great Barrier Reef. Env Microbiol 7, 1162–1174 (2005). 10.1111/j.1462-2920.2005.00793.x

[16]

Koren, O. & Rosenberg, E. Bacteria Associated with Mucus and Tissues of the Coral Oculina patagonica in Summer and Winter. Appl Environ Microb 72, 5254–5259 (2006). 10.1128/aem.00554-06

[17]

Li, J. et al. Bacterial dynamics within the mucus, tissue and skeleton of the coral Porites lutea during different seasons. Sci Rep 4, 7320 (2014). 10.1038/srep07320

[18]

Sweet, M. J., Croquer, A. & Bythell, J. C. Bacterial assemblages differ between compartments within the coral holobiont. Coral Reefs 30, 39–52 (2011). 10.1007/s00338-010-0695-1

[19]

Brown, B. & Bythell, J. Perspectives on mucus secretion in reef corals. Mar Ecol Prog Ser 296, 291–309 (2005). 10.3354/meps296291

[20]

Glasl, B., Herndl, G. J. & Frade, P. R. The microbiome of coral surface mucus has a key role in mediating holobiont health and survival upon disturbance. ISME J 10, 2280–2292 (2016). 10.1038/ismej.2016.9

[21]

Stabili, L., Schirosi, R., Parisi, M. G., Piraino, S. & Cammarata, M. The Mucus of Actinia equina (Anthozoa, Cnidaria): An Unexplored Resource for Potential Applicative Purposes. Mar Drugs 13, 5276–5296 (2015). 10.3390/md13085276

[22]

Shnit-Orland, M. & Kushmaro, A. Coral mucus-associated bacteria: a possible first line of defense. FEMS Microb Ecol 67, 371–380 (2009). 10.1111/j.1574-6941.2008.00644.x

[23]

Coffroth, M. A. Mucous sheet formation on poritid corals: An evaluation of coral mucus as a nutrient source on reefs. Mar Biol 105, 39–49 (1990). 10.1007/bf01344269

[24]

Marshall, A. T. & Wright, O. P. Confocal laser scanning light microscopy of the extra-thecal epithelia of undecalcified scleractinian corals. Cell and Tissue Research 272, 533–543 (1993). 10.1007/bf00318560

[25]

Wild, C. et al. Coral mucus functions as an energy carrier and particle trap in the reef ecosystem. Nature 428, 66–70 (2004). 10.1038/nature02344

[26]

Maynard, J. et al. Projections of climate conditions that increase coral disease susceptibility and pathogen abundance and virulence. Nature Clim. Change 5, 688–694 (2015). 10.1038/nclimate2625

[27]

Hoegh-Guldberg, O. et al. Coral reefs under rapid climate change and ocean acidification. Science 318, 1737–1742 (2007). 10.1126/science.1152509

[28]

Hughes, T. P. et al. Phase shifts, herbivory, and the resilience of coral reefs to climate change. Curr Biol 17, 360–365 (2007). 10.1016/j.cub.2006.12.049

[29]

Carpenter, K. E. et al. One-third of reef-building corals face elevated extinction risk from climate change and local impacts. Science 321, 560–563 (2008). 10.1126/science.1159196

[30]

Kushmaro, A., Loya, Y., Fine, M. & Rosenberg, E. Bacterial infection and coral bleaching. Nature 380, 396–396 (1996). 10.1038/380396a0

[31]

Ainsworth, T. D., Fine, M., Roff, G. & Hoegh-Guldberg, O. Bacteria are not the primary cause of bleaching in the Mediterranean coral Oculina patagonica. ISME J 2, 67–73 (2007). 10.1038/ismej.2007.88

[32]

Changes in coral-associated microbial communities during a bleaching event

David Bourne, Yuki Iida, Sven Uthicke et al.

The ISME Journal 2008 10.1038/ismej.2007.112

[33]

van Hooidonk, R., Maynard, J. A. & Planes, S. Temporary refugia for coral reefs in a warming world. Nature Clim. Change 3, 508–511 (2013). 10.1038/nclimate1829

[34]

Cacciapaglia, C. & van Woesik, R. Climate-change refugia: shading reef corals by turbidity. Global Change Biology 22, 1145–1154 (2016). 10.1111/gcb.13166

[35]

Fine, M., Gildor, H. & Genin, A. A coral reef refuge in the Red Sea. Glob Chang Biol 19, 3640–3647 (2013). 10.1111/gcb.12356

[36]

Burt, J., Al-Harthi, S. & Al-Cibahy, A. Long-term impacts of coral bleaching events on the world’s warmest reefs. Mar Environ Res 72, 225–229 (2011). 10.1016/j.marenvres.2011.08.005

[37]

Roik, A., Roder, C., Röthig, T. & Voolstra, C. R. Spatial and seasonal reef calcification in corals and calcareous crusts in the central Red Sea. Coral Reefs 35, 681–693 (2016). 10.1007/s00338-015-1383-y

[38]

Roik, A. et al. Year-Long Monitoring of Physico-Chemical and Biological Variables Provide a Comparative Baseline of Coral Reef Functioning in the Central Red Sea. PLoS One 11, e0163939 (2016). 10.1371/journal.pone.0163939

[39]

Effect on the Medium Salinity on Oil Degradation by Nocardioform Bacteria

I. S. Zvyagintseva, M. N. Poglazova, M. T. Gotoeva et al.

Microbiology 2001 10.1023/a:1013179513922

[40]

Lo, J. R., Lang, J. M., Darling, A. E., Eisen, J. A. & Coil, D. A. Draft Genome Sequence of an Actinobacterium, Brachybacterium muris Strain UCD-AY4. Genome Announcements 1, e00086–00013 (2013).

[41]

Röthig, T., Ochsenkuhn, M. A., Roik, A., van der Merwe, R. & Voolstra, C. R. Long-term salinity tolerance is accompanied by major restructuring of the coral bacterial microbiome. Mol Ecol 25, 1308–1323 (2016). 10.1111/mec.13567

[42]

D. Ainsworth, T. et al. The coral core microbiome identifies rare bacterial taxa as ubiquitous endosymbionts. ISME J 9, 2261–2274 (2015). 10.1038/ismej.2015.39

[43]

Ziegler, M. et al. Biogeography and molecular diversity of coral symbionts in the genus Symbiodinium around the Arabian Peninsula. Journal of Biogeography, doi: 10.1111/jbi.12913 (2017). 10.1111/jbi.12913

[44]

Hume, B. C. C. et al. Ancestral genetic diversity associated with the rapid spread of stress-tolerant coral symbionts in response to Holocene climate change. Proc Nat Acad Sci USA 113, 4416–4421 (2016). 10.1073/pnas.1601910113

[45]

Hume, B. C. et al. Symbiodinium thermophilum sp. nov., a thermotolerant symbiotic alga prevalent in corals of the world’s hottest sea, the Persian/Arabian Gulf. Sci Rep 5, 8562 (2015). 10.1038/srep08562

[46]

Ziegler, M., Roder, C., Büchel, C. & Voolstra, C. R. Niche acclimatization in Red Sea corals is dependent on flexibility of host-symbiont association. Mar Ecol Prog Ser 533, 149–161 (2015). 10.3354/meps11365

[47]

Baker, A. C., Starger, C. J., McClanahan, T. R. & Glynn, P. W. Coral reefs: Corals’ adaptive response to climate change. Nature 430, 741–741 (2004). 10.1038/430741a

[48]

Röthig, T. et al. Distinct bacterial communities associated with the coral model Aiptasia in aposymbiotic and symbiotic states with Symbiodinium. Frontiers in Marine Science 3 (2016). 10.3389/fmars.2016.00234

[49]

Bourne, D. G. et al. Coral reef invertebrate microbiomes correlate with the presence of photosymbionts. ISME J 7, 1452–1458 (2013). 10.1038/ismej.2012.172

[50]

Littman, R. A., Willis, B. L. & Bourne, D. G. Bacterial communities of juvenile corals infected with different Symbiodinium (dinoflagellate) clades. Mar Ecol Prog Ser 389, 45–59 (2009). 10.3354/meps08180

Showing 50 of 81 references

Cited By

66

Water depth outweighs reef condition in shaping non-geniculate coralline algae-associated microbial communities in coral reefs: A case study from Thailand

Kattika Pattarach, Komwit Surachat · 2024

Heliyon

Coral microbiome composition along the northern Red Sea suggests high plasticity of bacterial and specificity of endosymbiotic dinoflagellate communities

Eslam O. Osman, David J. Suggett · 2020

Microbiome

Coral reef survival under accelerating ocean deoxygenation

David J. Hughes, Rachel Alderdice · 2020

Nature Climate Change

Metrics

66

Citations

81

References

Details

Published: Mar 31, 2017
Vol/Issue: 7(1)
License: View

Authors

Christian R. Voolstra

Cite This Article

Ghaida Hadaidi, Till Röthig, Lauren K. Yum, et al. (2017). Stable mucus-associated bacterial communities in bleached and healthy corals of Porites lobata from the Arabian Seas. Scientific Reports, 7(1). https://doi.org/10.1038/srep45362

Stable mucus-associated bacterial communities in bleached and healthy corals of Porites lobata from the Arabian Seas

You May Also Like