Abstract
The coral microbiome has attracted increased attention because of its potential roles in host protection against deadly diseases. However, little is known about the role of coral-associated bacteria against the temperature-dependent opportunistic pathogen Vibrio coralliilyticus. In this study, we tested whether bacteria associated with the reef-building coral Galaxea fascicularis could inhibit the growth of V. coralliilyticus. Twenty-nine cultivable bacteria were successfully isolated from a healthy colony of G. fascicularis kept in an aquarium. Among the bacterial isolates, three Ruegeria sp. strains inhibited the growth of V. coralliilyticus P1 as a reference strain and Vibrio sp. isolated in this study. Ruegeria sp. strains were also detected from other G. fascicularis colonies in the aquarium and in previous field studies by 16S rRNA amplicon sequencing, suggesting that Ruegeria sp. strains are common among G. fascicularis colonies. These results illuminate the potential role of Ruegeria sp. in protecting corals against pathogenic Vibrio species.
References
Apprill A, Hughen K, Mincer T (2013) Major similarities in the bacterial communities associated with lesioned and healthy fungiidae corals. Environ Microbiol 15:2063–2072
Aswani S, Mumby PJ, Baker AC, Christie P, McCook LJ, Steneck RS, Richmond RH (2015) Scientific frontiers in the management of coral reefs. Front Mar Sci 2:50
Ben-Haim Y, Zicherman-Keren M, Rosenberg E (2003) Temperature-regulated bleaching and lysis of the coral Pocillopora damicornis by the novel pathogen Vibrio coralliilyticus. Appl Environ Microbiol 69:4236–4242
Berger M, Neumann A, Schulz S, Simon M, Brinkhoff T (2011) Tropodithietic acid production in Phaeobacter gallaeciensis is regulated by N-acyl homoserine lactone-mediated quorum sensing J Bacteriol 193:6576–6585
Bolger AM, Lohse M, Usadel B (2014) Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30:2114–2120
Bourne DG, Morrow KM, Webster NS (2016) Insights into the coral microbiome: underpinning the health and resilience of reef ecosystems. Annu Rev Microbiol 70:317–340
Bruno JF, Selig ER, Casey KS, Page CA, Willis BL, Harvell CD, Sweatman H, Melendy AM (2007) Thermal stress and coral cover as drivers of coral disease outbreaks. PLoS Biol 5:e124
Cai L et al (2018) Season structures prokaryotic partners but not algal symbionts in subtropical hard corals. Appl Microbiol Biotechnol 102:4963–4973
Caporaso JG et al (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7:335–336
Casey JM, Connolly SR, Ainsworth TD (2015) Coral transplantation triggers shift in microbiome and promotion of coral disease associated potential pathogens. Sci Rep 5:11903
Cervino JM, Hayes RL, Polson SW, Polson SC, Goreau TJ, Martinez RJ, Smith GW (2004) Relationship of Vibrio species infection and elevated temperatures to yellow blotch/band disease in Caribbean corals. Appl Environ Microbiol 70:6855–6864
Christie-Oleza JA, Armengaud J (2010) In-depth analysis of exoproteomes from marine bacteria by shotgun liquid chromatography-tandem mass spectrometry: the Ruegeria pomeroyi DSS-3 case-study. Mar Drugs 8:2223–2239
Christie-Oleza JA, Pina-Villalonga JM, Bosch R, Nogales B, Armengaud J (2012) Comparative proteogenomics of twelve Roseobacter exoproteomes reveals different adaptive strategies among these marine bacteria. Mol Cell Proteomics 11:M111 013110
Donner SD, Rickbeil GJM, Heron SF (2017) A new, high-resolution global mass coral bleaching database. PloS One 12:e0175490
Edgar RC (2010) Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26:2460–2461
Garren M, Son K, Tout J, Seymour JR, Stocker R (2016) Temperature-induced behavioral switches in a bacterial coral pathogen. ISME J 10:1363–1372
Glasl B, Herndl GJ, Frade PR (2016) The microbiome of coral surface mucus has a key role in mediating holobiont health and survival upon disturbance. ISME J 10:2280–2292
Hanshew AS, Mason CJ, Raffa KF, Currie CR (2013) Minimization of chloroplast contamination in 16S rRNA gene pyrosequencing of insect herbivore bacterial communities. J Microbiol Methods 95:149–155
Hughes TP et al (2017) Global warming and recurrent mass bleaching of corals. Nature 543:373–377
Kimes NE et al (2012) Temperature regulation of virulence factors in the pathogen Vibrio coralliilyticus. ISME J 6:835–846
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
Laurans Y, Pascal N, Binet T, Brander L, Clua E, David G, Rojat D, Seidl A (2013) Economic valuation of ecosystem services from coral reefs in the South Pacific: taking stock of recent experience. J Environ Manag 116:135–144
Li J, Chen Q, Zhang S, Huang H, Yang J, Tian XP, Long LJ (2013) Highly heterogeneous bacterial communities associated with the South China Sea reef corals Porites lutea, Galaxea fascicularis and Acropora millepora. PloS One 8:e71301
Luo H, Moran MA (2014) Evolutionary ecology of the marine Roseobacter clade. Microbiol Mol Biol Rev 78:573–587
Mera H, Bourne DG (2017) Disentangling causation: complex roles of coral-associated microorganisms in disease. Environ Microbiol 20:431–449
Miller TR, Belas R (2004) Dimethylsulfoniopropionate metabolism by Pfiesteria-associated Roseobacter spp. Appl Environ Microbiol 70:3383–3391
Miller TR, Hnilicka K, Dziedzic A, Desplats P, Belas R (2004) Chemotaxis of Silicibacter sp. strain TM1040 toward dinoflagellate products. Appl Environ Microbiol 70:4692–4701
Miranda LN, Hutchison K, Grossman AR, Brawley SH (2013) Diversity and abundance of the bacterial community of the red macroalga Porphyra umbilicalis: did bacterial farmers produce macroalgae? PLoS One 8:e58269
Mitova M, Tommonaro G, Hentschel U, Muller WE, De Rosa S (2004) Exocellular cyclic dipeptides from a Ruegeria strain associated with cell cultures of Suberites domuncula. Mar Biotechnol (NY) 6:95–103
Moberg F, Folke C (1999) Ecological goods and services of coral reef ecosystems. Ecol Econ 29:215–233
Mohamed NM, Cicirelli EM, Kan J, Chen F, Fuqua C, Hill RT (2008) Diversity and quorum-sensing signal production of Proteobacteria associated with marine sponges. Environ Microbiol 10:75–86
Moran MA et al (2007) Ecological genomics of marine Roseobacters. Appl Environ Microbiol 73:4559–4569
Motone K et al (2018) Protection of coral larvae from thermally induced oxidative stress by redox nanoparticles. Mar Biotechnol (NY) 20:542–548
Munn CB (2015) The role of vibrios in diseases of corals. Microbiol Spectr 3. https://doi.org/10.1128/microbiolspec.VE-0006-2014
Paillard C, Le Roux F, Borrego JJ (2004) Bacterial disease in marine bivalves, a review of recent studies: trends and evolution. Aquat Living Resour 17:477–498
Raina JB, Tapiolas D, Motti CA, Foret S, Seemann T, Tebben J, Willis BL, Bourne DG (2016) Isolation of an antimicrobial compound produced by bacteria associated with reef-building corals. PeerJ 4:e2275
Reshef L, Koren O, Loya Y, Zilber-Rosenberg I, Rosenberg E (2006) The coral probiotic hypothesis. Environ Microbiol 8:2068–2073
Rivers AR, Burns AS, Chan LK, Moran MA (2016) Experimental identification of small non-coding RNAs in the model marine bacterium Ruegeria pomeroyi DSS-3. Front Microbiol 7:380
Rosenberg E, Koren O, Reshef L, Efrony R, Zilber-Rosenberg I (2007) The role of microorganisms in coral health, disease and evolution. Nat Rev Microbiol 5:355–362
Rosenberg E, Kushmaro A, Kramarsky-Winter E, Banin E, Yossi L (2009) The role of microorganisms in coral bleaching. ISME J 3:139–146
Rygaard AM, Thogersen MS, Nielsen KF, Gram L, Bentzon-Tilia M (2017) Effects of gelling agent and extracellular signaling molecules on the culturability of marine bacteria. Appl Environ Microbiol 83. https://doi.org/10.1128/aem.00243-17
Santos Ede O et al (2011) Genomic and proteomic analyses of the coral pathogen Vibrio coralliilyticus reveal a diverse virulence repertoire. ISME J 5:1471–1483
Schneider CA, Rasband WS, Eliceiri KW (2012) NIH image to ImageJ: 25 years of image analysis. Nat Methods 9:671–675
Sekar R, Kaczmarsky LT, Richardson LL (2008) Microbial community composition of black band disease on the coral host Siderastrea siderea from three regions of the wider Caribbean. Mar Ecol Prog Ser 362:85–98
Shapiro OH, Kramarsky-Winter E, Gavish AR, Stocker R, Vardi A (2016) A coral-on-a-chip microfluidic platform enabling live-imaging microscopy of reef-building corals. Nat Commun 7:10860
Shnit-Orland M, Kushmaro A (2009) Coral mucus-associated bacteria: a possible first line of defense. FEMS Microbiol Ecol 67:371–380
Sonnenschein EC, Nielsen KF, D'Alvise P, Porsby CH, Melchiorsen J, Heilmann J, Kalatzis PG, López-Pérez M, Bunk B, Spröer C, Middelboe M, Gram L (2017) Global occurrence and heterogeneity of the Roseobacter-clade species Ruegeria mobilis. ISME J 11:588
Stuhr M, Blank-Landeshammer B, Reymond CE, Kollipara L, Sickmann A, Kucera M, Westphal H (2018) Disentangling thermal stress responses in a reef-calcifier and its photosymbionts by shotgun proteomics. Sci Rep 8:3524
Sunagawa S et al (2009) Bacterial diversity and white plague disease-associated community changes in the Caribbean coral Montastraea faveolata. ISME J 3:512–521
Sussman M, Willis BL, Victor S, Bourne DG (2008) Coral pathogens identified for White Syndrome (WS) epizootics in the Indo-Pacific. PLoS One 3:e2393
Sussman M, Mieog JC, Doyle J, Victor S, Willis BL, Bourne DG (2009) Vibrio zinc-metalloprotease causes photoinactivation of coral endosymbionts and coral tissue lesions. PLoS One 4:e4511
Tout J, Siboni N, Messer LF, Garren M, Stocker R, Webster NS, Ralph PJ, Seymour JR (2015) Increased seawater temperature increases the abundance and alters the structure of natural Vibrio populations associated with the coral Pocillopora damicornis. Front Microbiol 6:432
Ushijima B et al (2014a) Vibrio coralliilyticus strain OCN008 is an etiological agent of acute Montipora white syndrome. Appl Environ Microbiol 80:2102–2109
Ushijima B, Videau P, Poscablo D, Vine V, Salcedo M, Aeby G, Callahan SM (2014b) Complete genome sequence of Vibrio coralliilyticus strain OCN014, isolated from a diseased coral at Palmyra Atoll. Genome Announc 2. https://doi.org/10.1128/genomeA.01318-14
Wada N, Pollock FJ, Willis BL, Ainsworth T, Mano N, Bourne DG (2016) In situ visualization of bacterial populations in coral tissues: pitfalls and solutions. PeerJ 4:e2424
Weynberg KD, Voolstra CR, Neave MJ, Buerger P, van Oppen MJ (2015) From cholera to corals: viruses as drivers of virulence in a major coral bacterial pathogen. Sci Rep 5:17889
Zhang Z, Schwartz S, Wagner L, Miller W (2000) A greedy algorithm for aligning DNA sequences. J Comput Biol 7:203–214
Acknowledgments
We thank Dr. Chuya Shinzato of the University of Tokyo for his fruitful discussions. This study was partially supported by JSPS Research Fellowships for Young Scientists (K.M., 17J07458, and S.A., 16J08791) and Postdoctoral Researchers (T.T., 17J05024), as well as Grant-in-aid for Young Scientists (KAKENHI) (T.T., 18K14479). This study was also partially supported by JST-CREST (N.M., W.A., M.U., JPMJCR16G2).
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Miura, N., Motone, K., Takagi, T. et al. Ruegeria sp. Strains Isolated from the Reef-Building Coral Galaxea fascicularis Inhibit Growth of the Temperature-Dependent Pathogen Vibrio coralliilyticus. Mar Biotechnol 21, 1–8 (2019). https://doi.org/10.1007/s10126-018-9853-1
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10126-018-9853-1