Section: Microbiology
Topic: Ecology, Genetics/genomics, Microbiology

The bacterial microbiome of symbiotic and menthol-bleached polyps of long-term aquarium-reared Galaxea fascicularis

10.24072/pcjournal.429 - Peer Community Journal, Volume 4 (2024), article no. e59.

Get full text PDF Peer reviewed and recommended by PCI
article image

Coral reefs support the livelihood of half a billion people but are at high risk of collapse due to the vulnerability of corals to climate change and local anthropogenic stressors. While understanding coral functioning is essential to guide conservation efforts, research is challenged by the complex nature of corals. They exist as metaorganisms (holobionts), constituted by the association between the (coral) animal host, its obligate endosymbiotic algae (Symbiodiniaceae), and other microorganisms comprising bacteria, viruses, archaea, fungi and other protists. Researchers therefore increasingly turn to model organisms to unravel holobiont complexity, dynamics, and how these determine the health and fitness of corals. The coral Galaxea fascicularis is an emerging model organism for coral symbiosis research with demonstrated suitability to aquarium rearing and reproduction, and to manipulation of the host-Symbiodiniaceae symbiosis. However, little is known about the response of the G. fascicularis microbiome to menthol bleaching—the experimental removal of the Symbiodiniaceae which represents the first step in coral-algal symbiosis manipulation. For this, we characterized the bacterial microbiome of symbiotic and menthol-bleached G. fascicularis originating from the Red Sea and South China Sea (Hong Kong) that were long-term aquarium-reared in separate facilities. We found that the coral-associated microbiomes were composed of relatively few bacterial taxa (10-78 ASVs). Symbiotic polyps (clonal replicates) from the same colony had similar microbiomes, which were distinct from those of other colonies despite co-culturing in shared aquaria. A pattern of seemingly differential response of the bacterial microbiome to menthol bleaching between the two facilities emerged, warranting further investigation into the role of rearing conditions. Nevertheless, the changes in community composition overall appeared to be stochastic suggesting a dysbiotic state. Considering the importance of bleaching treatment of captive corals for symbiosis research, our results—although preliminary—contribute fundamental knowledge for the development of the Galaxea model for coral symbiosis research.

Published online:
DOI: 10.24072/pcjournal.429
Type: Research article

Puntin, Giulia 1; Wong, Jane C. Y. 2, 3; Röthig, Till 4, 5; Baker, David M. 2, 3; Sweet, Michael 5; Ziegler, Maren 1

1 Marine Holobiomics Lab, Department of Animal Ecology & Systematics, Justus Liebig University Giessen, Heinrich-Buff-Ring 26-32 IFZ, 35392 Giessen, Germany
2 The Swire Institute of Marine Science, University of Hong Kong, Cape d’Aguilar Road, Shek O, Hong Kong SAR, China
3 School of Biological Sciences, Kadoorie Biological Science Building, University of Hong Kong, Pok Fu Lam Road, Hong Kong SAR, China
4 Branch of Bioresources, Fraunhofer Institute for Molecular Biology and Applied Ecology, Giessen, Germany
5 Aquatic Research Facility, Nature-based Solutions Research Centre, University of Derby, UK
License: CC-BY 4.0
Copyrights: The authors retain unrestricted copyrights and publishing rights
     author = {Puntin, Giulia and Wong, Jane C. Y. and R\"othig, Till and Baker, David M. and Sweet, Michael and Ziegler, Maren},
     title = {The bacterial microbiome of symbiotic and menthol-bleached polyps of long-term aquarium-reared {\protect\emph{Galaxea} fascicularis}},
     journal = {Peer Community Journal},
     eid = {e59},
     publisher = {Peer Community In},
     volume = {4},
     year = {2024},
     doi = {10.24072/pcjournal.429},
     language = {en},
     url = {}
AU  - Puntin, Giulia
AU  - Wong, Jane C. Y.
AU  - Röthig, Till
AU  - Baker, David M.
AU  - Sweet, Michael
AU  - Ziegler, Maren
TI  - The bacterial microbiome of symbiotic and menthol-bleached polyps of long-term aquarium-reared Galaxea fascicularis
JO  - Peer Community Journal
PY  - 2024
VL  - 4
PB  - Peer Community In
UR  -
DO  - 10.24072/pcjournal.429
LA  - en
ID  - 10_24072_pcjournal_429
ER  - 
%0 Journal Article
%A Puntin, Giulia
%A Wong, Jane C. Y.
%A Röthig, Till
%A Baker, David M.
%A Sweet, Michael
%A Ziegler, Maren
%T The bacterial microbiome of symbiotic and menthol-bleached polyps of long-term aquarium-reared Galaxea fascicularis
%J Peer Community Journal
%D 2024
%V 4
%I Peer Community In
%R 10.24072/pcjournal.429
%G en
%F 10_24072_pcjournal_429
Puntin, Giulia; Wong, Jane C. Y.; Röthig, Till; Baker, David M.; Sweet, Michael; Ziegler, Maren. The bacterial microbiome of symbiotic and menthol-bleached polyps of long-term aquarium-reared Galaxea fascicularis. Peer Community Journal, Volume 4 (2024), article  no. e59. doi : 10.24072/pcjournal.429.

PCI peer reviews and recommendation, and links to data, scripts, code and supplementary information: 10.24072/pci.microbiol.100048

Conflict of interest of the recommender and peer reviewers:
The recommender in charge of the evaluation of the article and the reviewers declared that they have no conflict of interest (as defined in the code of conduct of PCI) with the authors or with the content of the article.

[1] Agostini, S.; Suzuki, Y.; Higuchi, T.; Casareto, B. E.; Yoshinaga, K.; Nakano, Y.; Fujimura, H. Biological and chemical characteristics of the coral gastric cavity, Coral Reefs, Volume 31 (2012), pp. 147-156 | DOI

[2] 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. The coral core microbiome identifies rare bacterial taxa as ubiquitous endosymbionts, ISME J, Volume 9 (2015), pp. 2261-2274 | DOI

[3] Al-Horani, F. A.; Al-Moghrabi, S. M.; de Beer, D. Microsensor study of photosynthesis and calcification in the scleractinian coral, Galaxea fascicularis: active internal carbon cycle, J Exp Mar Bio Ecol, Volume 288 (2003), pp. 1-15 | DOI

[4] Al-Horani, F. A.; Ferdelman, T.; Al-Moghrabi, S. M.; de Beer, D. Spatial distribution of calcification and photosynthesis in the scleractinian coral Galaxea fascicularis, Coral Reefs, Volume 24 (2005), pp. 173-180 | DOI

[5] Al-Horani, F. A.; Tambutté, É.; Allemand, D. Dark calcification and the daily rhythm of calcification in the scleractinian coral, Galaxea fascicularis, Coral Reefs, Volume 26 (2007), pp. 531-538 | DOI

[6] Andersson, A. F.; Lindberg, M.; Jakobsson, H.; Bäckhed, F.; Nyrén, P.; Engstrand, L. Comparative Analysis of Human Gut Microbiota by Barcoded Pyrosequencing, PLoS One, Volume 3 (2008), p. e2836 | DOI

[7] Apprill, A.; Weber, L. G.; Santoro, A. E. Distinguishing between Microbial Habitats Unravels Ecological Complexity in Coral Microbiomes. mSystems 1:e00143-16, mSystems, Volume 1, 2016 | DOI

[8] Battaglia, T. btools: A suite of R function for all types of microbial diversity analyses, 2022 (

[9] Bayer, T.; Neave, M. J.; Alsheikh-Hussain, A.; Aranda, M.; Yum, L. K.; Mincer, T.; Hughen, K.; Apprill, A.; Voolstra, C. R. The Microbiome of the Red Sea Coral Stylophora pistillata Is Dominated by Tissue-Associated Endozoicomonas Bacteria, Appl Environ Microbiol, Volume 79 (2013), pp. 4759-4762 | DOI

[10] Bernasconi, R.; Stat, M.; Koenders, A.; Huggett, M. J. Global Networks of Symbiodinium-Bacteria Within the Coral Holobiont, Microb Ecol, Volume 77 (2019), pp. 794-807 | DOI

[11] Bokulich, N. A.; Kaehler, B. D.; Rideout, J. R.; Dillon, M.; Bolyen, E.; Knight, R.; Huttley, G. A.; Caporaso, J. G. Optimizing taxonomic classification of marker-gene amplicon sequences with QIIME 2's q2-feature-classifier plugin, Microbiome, Volume 6 (2018), p. 90 | DOI

[12] 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.; Cope, E. K.; Da Silva, R.; Diener, C.; Dorrestein, P. C.; Douglas, G. M.; Durall, D. M.; Duvallet, C.; Edwardson, C. F.; Ernst, M.; Estaki, M.; Fouquier, J.; Gauglitz, J. M.; Gibbons, S. M.; Gibson, D. L.; Gonzalez, A.; Gorlick, K.; Guo, J.; Hillmann, B.; Holmes, S.; Holste, H.; Huttenhower, C.; Huttley, G. A.; Janssen, S.; Jarmusch, A. K.; Jiang, L.; Kaehler, B. D.; Kang K. Bin; Keefe, C. R.; Keim, P.; Kelley, S. T.; Knights, D.; Koester, I.; Kosciolek, T.; Kreps, J.; Langille Mgi; Lee, J.; Ley, R.; Liu, Y.-X.; Loftfield, E.; Lozupone, C.; Maher, M.; Marotz, C.; Martin, B. D.; McDonald, D.; McIver, L. J.; Melnik, A. V.; Metcalf, J. L.; Morgan, S. C.; Morton, J. T.; Naimey, A. T.; Navas-Molina, J. A.; Nothias, L. F.; Orchanian, S. B.; Pearson, T.; Peoples, S. L.; Petras, D.; Preuss, M. L.; Pruesse, E.; Rasmussen, L. B.; Rivers, A.; Robeson, M. S.; Rosenthal, P.; Segata, N.; Shaffer, M.; Shiffer, A.; Sinha, R.; Song, S. J.; Spear, J. R.; Swafford, A. D.; Thompson, L. R.; Torres, P. J.; Trinh, P.; Tripathi, A.; Turnbaugh, P. J.; Ul-Hasan, S.; van der Hooft Jjj; Vargas, F.; Vázquez-Baeza, Y.; Vogtmann, E.; von Hippel, M.; Walters, W.; Wan, Y.; Wang, M.; Warren, J.; Weber, K. C.; Williamson Chd; Willis, A. D.; Xu, Z. Z.; Zaneveld, J. R.; Zhang, Y.; Zhu, Q.; Knight, R.; Caporaso, J. G. Reproducible, interactive, scalable and extensible microbiome data science using QIIME 2, Nat Biotechnol, Volume 37 (2019), pp. 852-857 | DOI

[13] Bourne, D. G.; Morrow, K. M.; Webster, N. S. Insights into the Coral Microbiome: Underpinning the Health and Resilience of Reef Ecosystems, Annu Rev Microbiol, Volume 70 (2016), pp. 317-340 | DOI

[14] Cai, L.; Tian, R. M.; Zhou, G.; Tong, H.; Wong, Y. H.; Zhang, W.; Chui Apy; Xie, J. Y.; Qiu, J. W.; Ang, P. O.; Liu, S.; Huang, H.; Qian, P. Y. Exploring coral microbiome assemblages in the South China Sea, Sci Rep, Volume 8 (2018), pp. 1-13 | DOI

[15] Cai, L.; Zhou, G.; Tong, H.; Tian, R.-M.; Zhang, W.; Ding, W.; Liu, S.; Huang, H.; Qian, P.-Y. Season structures prokaryotic partners but not algal symbionts in subtropical hard corals, Appl Microbiol Biotechnol, Volume 102 (2018), pp. 4963-4973 | DOI

[16] Callahan, B. J.; McMurdie, P. J.; Rosen, M. J.; Han, A. W.; Johnson Aja; Holmes, S. P. DADA2: High-resolution sample inference from Illumina amplicon data, Nat Methods, Volume 13 (2016), pp. 581-583 | DOI

[17] Certner, R. H.; Vollmer, S. V. Inhibiting bacterial quorum sensing arrests coral disease development and disease-associated microbes, Environ Microbiol, Volume 20 (2018), pp. 645-657 | DOI

[18] Chakravarti, L. J.; Beltran, V. H.; van Oppen Mjh Rapid thermal adaptation in photosymbionts of reef-building corals, Glob Chang Biol, Volume 23 (2017), pp. 4675-4688 | DOI

[19] Chan, W. Y.; Meyers, L.; Rudd, D.; Topa, S. H.; van Oppen, M. J. H. Heat‐evolved algal symbionts enhance bleaching tolerance of adult corals without trade‐off against growth, Global Change Biology, Volume 29 (2023) no. 24, pp. 6945-6968 | DOI

[20] Chopyk, J.; Chattopadhyay, S.; Kulkarni, P.; Claye, E.; Babik, K. R.; Reid, M. C.; Smyth, E. M.; Hittle, L. E.; Paulson, J. N.; Cruz-Cano, R.; Pop, M.; Buehler, S. S.; Clark, P. I.; Sapkota, A. R.; Mongodin, E. F. Mentholation affects the cigarette microbiota by selecting for bacteria resistant to harsh environmental conditions and selecting against potential bacterial pathogens, Microbiome, Volume 5 (2017), p. 22 | DOI

[21] Connelly, M. T.; McRae, C. J.; Liu, P.-J.; Martin, C. E.; Traylor-Knowles, N. Antibiotics Alter Pocillopora Coral-Symbiodiniaceae-Bacteria Interactions and Cause Microbial Dysbiosis During Heat Stress, Front Mar Sci, Volume 8 (2022), pp. 1-18 | DOI

[22] Conway, J. R.; Lex, A.; Gehlenborg, N. UpSetR: an R package for the visualization of intersecting sets and their properties, Bioinformatics, Volume 33 (2017), pp. 2938-2940 | DOI

[23] Costanza, R.; de Groot, R.; Sutton, P.; van der Ploeg, S.; Anderson, S. J.; Kubiszewski, I.; Farber, S.; Turner, R. K. Changes in the global value of ecosystem services, Glob Environ Chang, Volume 26 (2014), pp. 152-158 | DOI

[24] Curtis, E.; Moseley, J.; Racicot, R.; Wright, R. M. Bacterial microbiome variation across symbiotic states and clonal lines in a cnidarian model, Front Mar Sci, Volume 10 (2023), pp. 1-9 | DOI

[25] Damjanovic, K.; Blackall, L. L.; Peplow, L. M.; van Oppen Mjh Assessment of bacterial community composition within and among Acropora loripes colonies in the wild and in captivity, Coral Reefs, Volume 39 (2020), pp. 1245-1255 | DOI

[26] Dani, V.; Priouzeau, F.; Pagnotta, S.; Carette, D.; Laugier, J. P.; Sabourault, C. Thermal and menthol stress induce different cellular events during sea anemone bleaching, Symbiosis, Volume 69 (2016), pp. 175-192 | DOI

[27] Dubé, C. E.; Ziegler, M.; Mercière, A.; Boissin, E.; Planes, S.; Bourmaud Ca-F; Voolstra, C. R. Naturally occurring fire coral clones demonstrate a genetic and environmental basis of microbiome composition, Nat Commun, Volume 12 (2021), p. 6402 | DOI

[28] Dungan, A. M.; Bulach, D.; Lin, H.; van Oppen Mjh; Blackall, L. L. Development of a free radical scavenging bacterial consortium to mitigate oxidative stress in cnidarians, Microb Biotechnol, Volume 14 (2021), pp. 2025-2040 | DOI

[29] Dungan, A. M.; van Oppen Mjh; Blackall, L. L. Short-Term Exposure to Sterile Seawater Reduces Bacterial Community Diversity in the Sea Anemone, Exaiptasia diaphana, Front Mar Sci, Volume 7 (2021), pp. 1-10 | DOI

[30] Eakin, C. M.; Devotta, D.; Heron, S.; Geiger, E.; De La Cour, J.; Gomez, A.; Skirving, W.; Baird, A.; Cantin, N.; Donner, S.; Gilmour, J. The 2014-17 Global Coral Bleaching Event: The Most Severe and Widespread Coral Reef Destruction, Res Sq (2022), pp. 1-24 | DOI

[31] Eddy, T. D.; Lam Vwy; Reygondeau, G.; Cisneros-Montemayor, A. M.; Greer, K.; Palomares Mld; Bruno, J. F.; Ota, Y.; Cheung Wwl Global decline in capacity of coral reefs to provide ecosystem services, One Earth, Volume 4 (2021), pp. 1278-1285 | DOI

[32] Ferrier-Pagès, C.; Gattuso, J.; Cauwet, G.; Jaubert, J.; Allemand, D. Release of dissolved organic carbon and nitrogen by the zooxanthellate coral Galaxea fascicularis, Mar Ecol Prog Ser, Volume 172 (1998), pp. 265-274 | DOI

[33] Fraune, S.; Anton-Erxleben, F.; Augustin, R.; Franzenburg, S.; Knop, M.; Schröder, K.; Willoweit-Ohl, D.; Bosch Tcg Bacteria–bacteria interactions within the microbiota of the ancestral metazoan Hydra contribute to fungal resistance, ISME J, Volume 9 (2015), pp. 1543-1556 | DOI

[34] Gabay, Y.; Parkinson, J. E.; Wilkinson, S. P.; Weis, V. M.; Davy, S. K. Inter-partner specificity limits the acquisition of thermotolerant symbionts in a model cnidarian-dinoflagellate symbiosis, ISME J, Volume 13 (2019), pp. 2489-2499 | DOI

[35] Gabay, Y.; Weis, V. M.; Davy, S. K. Symbiont Identity Influences Patterns of Symbiosis Establishment, Host Growth, and Asexual Reproduction in a Model Cnidarian-Dinoflagellate Symbiosis, Biol Bull, Volume 234 (2018), pp. 1-10 | DOI

[36] Galand, P. E.; Ruscheweyh, H.-J.; Salazar, G.; Hochart, C.; Henry, N.; Hume Bcc; Oliveira, P. H.; Perdereau, A.; Labadie, K.; Belser, C.; Boissin, E.; Romac, S.; Poulain, J.; Bourdin, G.; Iwankow, G.; Moulin, C.; Armstrong, E. J.; Paz-García, D. A.; Ziegler, M.; Agostini, S.; Banaigs, B.; Boss, E.; Bowler, C.; de Vargas, C.; Douville, E.; Flores, M.; Forcioli, D.; Furla, P.; Gilson, E.; Lombard, F.; Pesant, S.; Reynaud, S.; Thomas, O. P.; Troublé, R.; Zoccola, D.; Voolstra, C. R.; Thurber, R. V.; Sunagawa, S.; Wincker, P.; Allemand, D.; Planes, S. Diversity of the Pacific Ocean coral reef microbiome, Nat Commun, Volume 14 (2023), p. 3039 | DOI

[37] Galliot, B. Hydra, a fruitful model system for 270 years, Int J Dev Biol, Volume 56 (2012), pp. 411-423 | DOI

[38] Goulet, T. L.; Erill, I.; Ascunce, M. S.; Finley, S. J.; Javan, G. T. Conceptualization of the Holobiont Paradigm as It Pertains to Corals, Front Physiol, Volume 11 (2020), pp. 1-8 | DOI

[39] Hartman, L. M.; van Oppen, M. J. H.; Blackall, L. L. Microbiota characterization of Exaiptasia diaphana from the Great Barrier Reef, Animal Microbiome, Volume 2 (2020) no. 1 | DOI

[40] Hernandez-Agreda, A.; Leggat, W.; Bongaerts, P.; Herrera, C.; Ainsworth, T. D. Rethinking the Coral Microbiome: Simplicity Exists within a Diverse Microbial Biosphere, MBio, Volume 9 (2018), pp. 1-14 | DOI

[41] Herrera, M.; Klein, S. G.; Schmidt-Roach, S.; Campana, S.; Cziesielski, M. J.; Chen, J. E.; Duarte, C. M.; Aranda, M. Unfamiliar partnerships limit cnidarian holobiont acclimation to warming, Glob Chang Biol, Volume 26 (2020), pp. 5539-5553 | DOI

[42] Huggett, M. J.; Apprill, A. Coral microbiome database: Integration of sequences reveals high diversity and relatedness of coral-associated microbes, Environ Microbiol Rep, Volume 11 (2019), pp. 372-385 | DOI

[43] Hughes, T. P.; Barnes, M. L.; Bellwood, D. R.; Cinner, J. E.; Cumming, G. S.; Jackson Jbc; Kleypas, J.; van de Leemput, I. A.; Lough, J. M.; Morrison, T. H.; Palumbi, S. R.; van Nes, E. H.; Scheffer, M. Coral reefs in the Anthropocene, Nature, Volume 546 (2017), pp. 82-90 | DOI

[44] Ide, K.; Nishikawa, Y.; Maruyama, T.; Tsukada, Y.; Kogawa, M.; Takeda, H.; Ito, H.; Wagatsuma, R.; Miyaoka, R.; Nakano, Y.; Kinjo, K.; Ito, M.; Hosokawa, M.; Yura, K.; Suda, S.; Takeyama, H. Targeted single-cell genomics reveals novel host adaptation strategies of the symbiotic bacteria Endozoicomonas in Acropora tenuis coral, Microbiome, Volume 10 (2022), pp. 1-16 | DOI

[45] Jaspers, C.; Fraune, S.; Arnold, A. E.; Miller, D. J.; Bosch Tcg; Voolstra, C. R. Resolving structure and function of metaorganisms through a holistic framework combining reductionist and integrative approaches, Zoology, Volume 133 (2019), pp. 81-87 | DOI

[46] Kaehler, B. D.; Bokulich, N.; McDonald, D.; Knight, R.; Caporaso, J. G.; Huttley, G. A. Species abundance information improves sequence taxonomy classification accuracy, Nat Commun, Volume 10 (2019) | DOI

[47] Kitamura, R.; Miura, N.; Ito, M.; Takagi, T.; Yamashiro, H.; Nishikawa, Y.; Nishimura, Y.; Kobayashi, K.; Kataoka, M. Specific Detection of Coral-Associated Ruegeria, a Potential Probiotic Bacterium, in Corals and Subtropical Seawater, Mar Biotechnol, Volume 23 (2021), pp. 576-589 | DOI

[48] Kooperman, N.; Ben-Dov, E.; Kramarsky-Winter, E.; Barak, Z.; Kushmaro, A. Coral mucus-associated bacterial communities from natural and aquarium environments, FEMS Microbiol Lett, Volume 276 (2007), pp. 106-113 | DOI

[49] Lawson, C. A.; Raina, J.; Kahlke, T.; Seymour, J. R.; Suggett, D. J. Defining the core microbiome of the symbiotic dinoflagellate, Symbiodinium, Environ Microbiol Rep, Volume 10 (2018), pp. 7-11 | DOI

[50] Lex, A.; Gehlenborg, N.; Strobelt, H.; Vuillemot, R.; Pfister, H. UpSet: Visualization of Intersecting Sets, IEEE Trans Vis Comput Graph, Volume 20 (2014), pp. 1983-1992 | DOI

[51] Li, J.; Chen, Q.; Zhang, S.; Huang, H.; Yang, J.; Tian, X.-P.; Long, L.-J. Highly Heterogeneous Bacterial Communities Associated with the South China Sea Reef Corals Porites lutea, Galaxea fascicularis and Acropora millepora, PLoS One, Volume 8 (2013), p. e71301 | DOI

[52] Lin, M.-F.; Takahashi, S.; Forêt, S.; Davy, S. K.; Miller, D. J. Transcriptomic analyses highlight the likely metabolic consequences of colonization of a cnidarian host by native or non-native Symbiodinium species, Biol Open, Volume 8 (2019), pp. 1-11 | DOI

[53] Littman, R. A.; Bourne, D. G.; Willis, B. L. Responses of coral-associated bacterial communities to heat stress differ with Symbiodinium type on the same coral host, Mol Ecol, Volume 19 (2010), pp. 1978-1990 | DOI

[54] Mahzoon, T.; Koraei, P.; Tavakol, O.; Gholami, M.; Barfi, A. Effect of Limonene, Camphor and Menthol on Cariogenic Oral Pathogens, Pakistan J Med Heal Sci, Volume 16 (2022), pp. 706-709 | DOI

[55] Matthews, J. L.; Raina, J.; Kahlke, T.; Seymour, J. R.; Oppen Mjh; Suggett, D. J. Symbiodiniaceae-bacteria interactions: rethinking metabolite exchange in reef-building corals as multi-partner metabolic networks, Environ Microbiol, Volume 22 (2020), pp. 1675-1687 | DOI

[56] Matthews, J. L.; Sproles, A. E.; Oakley, C. A.; Grossman, A. R.; Weis, V. M.; Davy, S. K. Menthol-induced bleaching rapidly and effectively provides experimental aposymbiotic sea anemones (Aiptasia sp.) for symbiosis investigations, J Exp Biol, Volume 219 (2015), pp. 306-310 | DOI

[57] McMurdie, P. J.; Holmes, S. phyloseq: An R package for reproducible interactive analysis and graphics of microbiome census data, PLoS One, Volume 8 (2013), p. e61217 | DOI

[58] Mikryukov, V. metagMisc: Miscellaneous functions for metagenomic analysis, 2023 (

[59] Miura, N.; Motone, K.; Takagi, T.; Aburaya, S.; Watanabe, S.; Aoki, W.; Ueda, M. Ruegeria sp. Strains Isolated from the Reef-Building Coral Galaxea fascicularis Inhibit Growth of the Temperature-Dependent Pathogen Vibrio coralliilyticus, Mar Biotechnol, Volume 21 (2019), pp. 1-8 | DOI

[60] Morrow, K. M.; Moss, A. G.; Chadwick, N. E.; Liles, M. R. Bacterial Associates of Two Caribbean Coral Species Reveal Species-Specific Distribution and Geographic Variability, Appl Environ Microbiol, Volume 78 (2012), pp. 6438-6449 | DOI

[61] Morrow, K. M.; Pankey, M. S.; Lesser, M. P. Community structure of coral microbiomes is dependent on host morphology, Microbiome, Volume 10 (2022), p. 113 | DOI

[62] Motone, K.; Takagi, T.; Aburaya, S.; Miura, N.; Aoki, W.; Ueda, M. A Zeaxanthin-Producing Bacterium Isolated from the Algal Phycosphere Protects Coral Endosymbionts from Environmental Stress, MBio, Volume 11 (2020), pp. 1-13 | DOI

[63] Murillo-Rincon, A. P.; Klimovich, A.; Pemöller, E.; Taubenheim, J.; Mortzfeld, B.; Augustin, R.; Bosch Tcg Spontaneous body contractions are modulated by the microbiome of Hydra, Sci Rep, Volume 7 (2017), p. 15937 | DOI

[64] Muscatine, L. The role of symbiotic algae in carbon and energy flux in reef corals, Ecosyst world, Volume 25 (1990), pp. 75-87 | DOI

[65] Muscatine, L.; Porter, J. W. Reef Corals: Mutualistic Symbioses Adapted to Nutrient-Poor Environments, Bioscience, Volume 27 (1977), pp. 454-460 | DOI

[66] Neave, M. J.; Apprill, A.; Ferrier-Pagès, C.; Voolstra, C. R. Diversity and function of prevalent symbiotic marine bacteria in the genus Endozoicomonas, Appl Microbiol Biotechnol, Volume 100 (2016), pp. 8315-8324 | DOI

[67] Neave, M. J.; Rachmawati, R.; Xun, L.; Michell, C. T.; Bourne, D. G.; Apprill, A.; Voolstra, C. R. Differential specificity between closely related corals and abundant Endozoicomonas endosymbionts across global scales, ISME J, Volume 11 (2017), pp. 186-200 | DOI

[68] Nitschke, M. R.; Fidalgo, C.; Simões, J.; Brandão, C.; Alves, A.; Serôdio, J.; Frommlet, J. C. Symbiolite formation: a powerful in vitro model to untangle the role of bacterial communities in the photosynthesis-induced formation of microbialites, ISME J, Volume 14 (2020), pp. 1533-1546 | DOI

[69] Niu, W.; Huang, H.; Lin, R.; Chen, C.-H.; Shen, K.-N.; Hsiao, C.-D. The complete mitogenome of the Galaxy Coral, Galaxea fascicularis (Cnidaria: Oculinidae), Mitochondrial DNA Part B, Volume 1 (2016), pp. 10-11 | DOI

[70] Peixoto, R. S.; Sweet, M.; Villela Hdm; Cardoso, P.; Thomas, T.; Voolstra, C. R.; Høj, L.; Bourne, D. G. Coral Probiotics: Premise, Promise, Prospects, Annu Rev Anim Biosci, Volume 9 (2021), pp. 265-288 | DOI

[71] Pietschke, C.; Treitz, C.; Forêt, S.; Schultze, A.; Künzel, S.; Tholey, A.; Bosch Tcg; Fraune, S. Host modification of a bacterial quorum-sensing signal induces a phenotypic switch in bacterial symbionts, Proc Natl Acad Sci, Volume 114 (2017), p. E8488-E8497 | DOI

[72] Pogoreutz, C.; Oakley, C. A.; Rädecker, N.; Cárdenas, A.; Perna, G.; Xiang, N.; Peng, L.; Davy, S. K.; Ngugi, D. K.; Voolstra, C. R. Coral holobiont cues prime Endozoicomonas for a symbiotic lifestyle, ISME J, Volume 16 (2022), pp. 1883-1895 | DOI

[73] Pogoreutz, C.; Voolstra, C. R.; Rädecker, N.; Weis, V. The coral holobiont highlights the dependence of cnidarian animal hosts on their associated microbes, Cellular dialogues in the holobiont (2020), pp. 91-118 | DOI

[74] Pollock, F. J.; McMinds, R.; Smith, S.; Bourne, D. G.; Willis, B. L.; Medina, M.; Thurber, R. V.; Zaneveld, J. R. Coral-associated bacteria demonstrate phylosymbiosis and cophylogeny, Nat Commun, Volume 9 (2018), p. 4921 | DOI

[75] Pratte, Z. A.; Richardson, L. L.; Mills, D. K. Microbiota shifts in the surface mucopolysaccharide layer of corals transferred from natural to aquaria settings, J Invertebr Pathol, Volume 125 (2015) | DOI

[76] Puntin, G. sPuntinG/Galaxea_Microbiome_PCI: Galaxea microbiome analysis 1st peer-review, Zenodo, 2024 | DOI

[77] Puntin, G. Supplementary Figures, Tables, and Materials and Methods of "The bacterial microbiome of symbiotic and menthol-bleached polyps of long-term aquarium-reared Galaxea fascicularis", Zenodo, 2024 | DOI

[78] Puntin, G.; Craggs, J.; Hayden, R.; Engelhardt, K. E.; McIlroy, S.; Sweet, M.; Baker, D. M.; Ziegler, M. The reef-building coral Galaxea fascicularis: a new model system for coral symbiosis research, Coral Reefs (2022), pp. 1-33 | DOI

[79] Puntin, G.; Sweet, M.; Fraune, S.; Medina, M.; Sharp, K.; Weis, V. M.; Ziegler, M. Harnessing the Power of Model Organisms To Unravel Microbial Functions in the Coral Holobiont, Microbiology and Molecular Biology Reviews, Volume 86 (2022) no. 4 | DOI

[80] Putnam, H. M.; Barott, K. L.; Ainsworth, T. D.; Gates, R. D. The Vulnerability and Resilience of Reef-Building Corals, Curr Biol, Volume 27 (2017), p. R528-R540 | DOI

[81] R. Core Team R: A Language and Environment for Statistical Computing, 2021 (

[82] Raina, J.-B.; Clode, P. L.; Cheong, S.; Bougoure, J.; Kilburn, M. R.; Reeder, A.; Forêt, S.; Stat, M.; Beltran, V.; Thomas-Hall, P.; Tapiolas, D.; Motti, C. M.; Gong, B.; Pernice, M.; Marjo, C. E.; Seymour, J. R.; Willis, B. L.; Bourne, D. G. Subcellular tracking reveals the location of dimethylsulfoniopropionate in microalgae and visualises its uptake by marine bacteria, Elife, Volume 6 (2017), pp. 1-17 | DOI

[83] Raina, J.-B.; Tapiolas, D.; Motti, C. A.; Foret, S.; Seemann, T.; Tebben, J.; Willis, B. L.; Bourne, D. G. Isolation of an antimicrobial compound produced by bacteria associated with reef-building corals, PeerJ, Volume 4 (2016), p. e2275 | DOI

[84] Raina, J.-B.; Tapiolas, D.; Willis, B. L.; Bourne, D. G. Coral-Associated Bacteria and Their Role in the Biogeochemical Cycling of Sulfur, Appl Environ Microbiol, Volume 75 (2009), pp. 3492-3501 | DOI

[85] Robbins, S. J.; Singleton, C. M.; Chan, C. X.; Messer, L. F.; Geers, A. U.; Ying, H.; Baker, A.; Bell, S. C.; Morrow, K. M.; Ragan, M. A.; Miller, D. J.; Forêt, S.; Ball, E.; Beeden, R.; Berumen, M.; Aranda, M.; Ravasi, T.; Bongaerts, P.; Hoegh-Guldberg, O.; Cooke, I.; Leggat, B.; Sprungala, S.; Fitzgerald, A.; Shang, C.; Lundgren, P.; Fyffe, T.; Rubino, F.; van Oppen, M.; Weynberg, K.; Robbins, S. J.; Singleton, C. M.; Xin Chan, C.; Messer, L. F.; Geers, A. U.; Ying, H.; Baker, A.; Bell, S. C.; Morrow, K. M.; Ragan, M. A.; Miller, D. J.; Foret, S.; Voolstra, C. R.; Tyson, G. W.; Bourne, D. G.; Voolstra, C. R.; Tyson, G. W.; Bourne, D. G. A genomic view of the reef-building coral Porites lutea and its microbial symbionts, Nat Microbiol, Volume 4 (2019), pp. 2090-2100 | DOI

[86] Robeson, M. S.; O’Rourke, D. R.; Kaehler, B. D.; Ziemski, M.; Dillon, M. R.; Foster, J. T.; Bokulich, N. A. RESCRIPt: Reproducible sequence taxonomy reference database management, PLOS Computational Biology, Volume 17 (2021) no. 11 | DOI

[87] Rohwer, F.; Seguritan, V.; Azam, F.; Knowlton, N. Diversity and distribution of coral-associated bacteria, Mar Ecol Prog Ser, Volume 243 (2002), pp. 1-10 | DOI

[88] Rosado, P. M.; Leite Dca; Duarte Gas; Chaloub, R. M.; Jospin, G.; Nunes da Rocha, U.; P. Saraiva, J.; Dini-Andreote, F.; Eisen, J. A.; Bourne, D. G.; Peixoto, R. S. Marine probiotics: increasing coral resistance to bleaching through microbiome manipulation, ISME J, Volume 13 (2019), pp. 921-936 | DOI

[89] Rosenberg, E.; Koren, O.; Reshef, L.; Efrony, R.; Zilber-Rosenberg, I. The role of microorganisms in coral health, disease and evolution, Nat Rev Microbiol, Volume 5 (2007), pp. 355-362 | DOI

[90] Röthig, T.; Puntin, G.; Wong Jcy; Burian, A.; McLeod, W.; Baker, D. M. Holobiont nitrogen control and its potential for eutrophication resistance in an obligate photosymbiotic jellyfish, Microbiome, Volume 9 (2021), p. 127 | DOI

[91] Röthig, T.; Costa, R. M.; Simona, F.; Baumgarten, S.; Torres, A. F.; Radhakrishnan, A.; Aranda, M.; Voolstra, C. R. Distinct Bacterial Communities Associated with the Coral Model Aiptasia in Aposymbiotic and Symbiotic States with Symbiodinium, Frontiers in Marine Science, Volume 3 (2016) | DOI

[92] Röthig, T.; Costa, R. M.; Simona, F.; Baumgarten, S.; Torres, A. F.; Radhakrishnan, A.; Aranda, M.; Voolstra, C. R. Distinct Bacterial Communities Associated with the Coral Model Aiptasia in Aposymbiotic and Symbiotic States with Symbiodinium, Frontiers in Marine Science, Volume 3 (2016) | DOI

[93] Sato, Y. An important step forward in deciphering coral symbiosis through manipulative approaches, Peer Community in Microbiology, Volume 1 (2024) | DOI

[94] Scharfenstein, H. J.; Chan, W. Y.; Buerger, P.; Humphrey, C.; van Oppen Mjh Evidence for de novo acquisition of microalgal symbionts by bleached adult corals, ISME J, Volume 16 (2022), pp. 1676-1679 | DOI

[95] Schubert, P.; Wilke, T. Coral Microcosms: Challenges and Opportunities for Global Change Biology. Corals in a Changing World, InTech (2018), pp. 143-175 | DOI

[96] Sunagawa, S.; DeSantis, T. Z.; Piceno, Y. M.; Brodie, E. L.; DeSalvo, M. K.; Voolstra, C. R.; Weil, E.; Andersen, G. L.; Medina, M. Bacterial diversity and White Plague Disease-associated community changes in the Caribbean coral Montastraea faveolata, ISME J, Volume 3 (2009), pp. 512-521 | DOI

[97] Sweet, M. J.; Croquer, A.; Bythell, J. C. Bacterial assemblages differ between compartments within the coral holobiont, Coral Reefs, Volume 30 (2011), pp. 39-52 | DOI

[98] Tandon, K.; Lu, C.-Y.; Chiang, P.-W.; Wada, N.; Yang, S.-H.; Chan, Y.-F.; Chen, P.-Y.; Chang, H.-Y.; Chiou, Y.-J.; Chou, M.-S.; Chen, W.-M.; Tang, S.-L. Comparative genomics: Dominant coral-bacterium Endozoicomonas acroporae metabolizes dimethylsulfoniopropionate (DMSP), ISME J, Volume 14 (2020), pp. 1290-1303 | DOI

[99] Tang, K.; Zhan, W.; Zhou, Y.; Xu, T.; Chen, X.; Wang, W.; Zeng, Z.; Wang, Y.; Wang, X. Antagonism between coral pathogen Vibrio coralliilyticus and other bacteria in the gastric cavity of scleractinian coral Galaxea fascicularis, Sci China Earth Sci, Volume 63 (2020), pp. 157-166 | DOI

[100] Taubenheim, J.; Willoweit-Ohl, D.; Knop, M.; Franzenburg, S.; He, J.; Bosch Tcg; Fraune, S. Bacteria- and temperature-regulated peptides modulate β-catenin signaling in Hydra, Proc Natl Acad Sci U S A, Volume 117 (2020), pp. 21459-21468 | DOI

[101] Tebben, J.; Motti, C. A.; Siboni, N.; Tapiolas, D. M.; Negri, A. P.; Schupp, P. J.; Kitamura, M.; Hatta, M.; Steinberg, P. D.; Harder, T. Chemical mediation of coral larval settlement by crustose coralline algae, Sci Rep, Volume 5 (2015) | DOI

[102] Thompson, J. R.; Rivera, H. E.; Closek, C. J.; Medina, M. Microbes in the coral holobiont: partners through evolution, development, and ecological interactions, Front Cell Infect Microbiol, Volume 4 (2015) | DOI

[103] Trombetta, D.; Castelli, F.; Sarpietro, M. G.; Venuti, V.; Cristani, M.; Daniele, C.; Saija, A.; Mazzanti, G.; Bisignano, G. Mechanisms of antibacterial action of three monoterpenes, Antimicrobial Agents and Chemotherapy, Volume 49 (2005) no. 6, pp. 2474-2478 | DOI

[104] Vega Thurber, R.; Willner-Hall, D.; Rodriguez-Mueller, B.; Desnues, C.; Edwards, R. A.; Angly, F.; Dinsdale, E.; Kelly, L.; Rohwer, F. Metagenomic analysis of stressed coral holobionts, Environ Microbiol, Volume 11 (2009), pp. 2148-2163 | DOI

[105] Wang, J. T.; Wang, Y. T.; Keshavmurthy, S.; Meng, P. J.; Chen, C. A. The coral Platygyra verweyi exhibits local adaptation to long-term thermal stress through host-specific physiological and enzymatic response, Sci Rep, Volume 9 (2019), pp. 1-11 | DOI

[106] Wang, J.-T.; Chen, Y.-Y.; Tew, K. S.; Meng, P.-J.; Chen, C. A. Physiological and biochemical performances of menthol-induced aposymbiotic corals, PLoS One, Volume 7 (2012), p. e46406 | DOI

[107] Webster, N. S.; Smith, L. D.; Heyward, A. J.; Watts Jem; Webb, R. I.; Blackall, L. L.; Negri, A. P. Metamorphosis of a Scleractinian Coral in Response to Microbial Biofilms, Appl Environ Microbiol, Volume 70 (2004), pp. 1213-1221 | DOI

[108] Weis, V. M. Cellular mechanisms of Cnidarian bleaching: stress causes the collapse of symbiosis, J Exp Biol, Volume 211 (2008), p. 3059-66 | DOI

[109] Weis, V. M.; Davy, S. K.; Hoegh-Guldberg, O.; Rodriguez-Lanetty, M.; Pringle, J. R. Cell biology in model systems as the key to understanding corals, Trends Ecol Evol, Volume 23 (2008), pp. 369-376 | DOI

[110] Wepfer, P. H.; Nakajima, Y.; Sutthacheep, M.; Radice, V. Z.; Richards, Z.; Ang, P.; Terraneo, T.; Sudek, M.; Fujimura, A.; Toonen, R. J.; Mikheyev, A. S.; Economo, E. P.; Mitarai, S. Evolutionary biogeography of the reef-building coral genus Galaxea across the Indo-Pacific ocean, Mol Phylogenet Evol, Volume 151 (2020), p. 106905 | DOI

[111] Wickham, H. ggplot2: Elegant Graphics for Data Analysis, Use R!, Springer International Publishing, Cham, 2016 | DOI

[112] Yilmaz, P.; Parfrey, L. W.; Yarza, P.; Gerken, J.; Pruesse, E.; Quast, C.; Schweer, T.; Peplies, J.; Ludwig, W.; Glöckner, F. O. The SILVA and “All-species Living Tree Project (LTP)” taxonomic frameworks, Nucleic Acids Res, Volume 42 (2013), p. D643-D648 | DOI

[113] Zaneveld, J. R.; McMinds, R.; Vega Thurber, R. Stress and stability: applying the Anna Karenina principle to animal microbiomes, Nat Microbiol, Volume 2 (2017), p. 17121 | DOI

[114] Zhou, Y.; Tang, K.; Wang, P.; Wang, W.; Wang, Y.; Wang, X. Identification of bacteria-derived urease in the coral gastric cavity, Sci China Earth Sci, Volume 63 (2020), pp. 1553-1563 | DOI

[115] Ziegler, M.; Roder, C.; Büchel, C.; Voolstra, C. Niche acclimatization in Red Sea corals is dependent on flexibility of host-symbiont association, Mar Ecol Prog Ser, Volume 533 (2015), pp. 149-161 | DOI

[116] Ziegler, M.; Roik, A.; Porter, A.; Zubier, K.; Mudarris, M. S.; Ormond, R.; Voolstra, C. R. Coral microbial community dynamics in response to anthropogenic impacts near a major city in the central Red Sea, Mar Pollut Bull, Volume 105 (2016), pp. 629-640 | DOI

[117] van Hooidonk, R.; Maynard, J.; Tamelander, J.; Gove, J.; Ahmadia, G.; Raymundo, L.; Williams, G.; Heron, S. F.; Planes, S. Local-scale projections of coral reef futures and implications of the Paris Agreement, Sci Rep, Volume 6 (2016), p. 39666 | DOI

Cited by Sources: