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Increased Seawater Temperature Increases the Abundance and Alters the Structure of Natural Vibrio Populations Associated with the Coral Pocillopora Damicornis

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Increased Seawater Temperature Increases the Abundance and Alters the Structure of Natural Vibrio Populations Associated with the Coral Pocillopora Damicornis Increased seawater temperature increases the abundance and alters the structure of natural Vibrio populations associated with the coral Pocillopora damicornis The MIT Faculty has made this article openly available. Please share how this access benefits you. Your story matters. Citation Tout, Jessica, Nachshon Siboni, Lauren F. Messer, Melissa Garren, Roman Stocker, Nicole S. Webster, Peter J. Ralph, and Justin R. Seymour. “Increased Seawater Temperature Increases the Abundance and Alters the Structure of Natural Vibrio Populations Associated with the Coral Pocillopora Damicornis.” Frontiers in Microbiology 6 (May 18, 2015). As Published http://dx.doi.org/10.3389/fmicb.2015.00432 Publisher Frontiers Research Foundation Version Final published version Citable link http://hdl.handle.net/1721.1/98180 Terms of Use Creative Commons Attribution Detailed Terms http://creativecommons.org/licenses/by/4.0/ ORIGINAL RESEARCH published: 18 May 2015 doi: 10.3389/fmicb.2015.00432 Increased seawater temperature increases the abundance and alters the structure of natural Vibrio populations associated with the coral Pocillopora damicornis Jessica Tout1*, Nachshon Siboni1, Lauren F. Messer1, Melissa Garren2, Roman Stocker2, Nicole S. Webster3, Peter J. Ralph1 and Justin R. Seymour1 1 Plant Functional Biology and Climate Change Cluster, University of Technology, Sydney, NSW, Australia, 2 Ralph M. Parsons Laboratory, Department of Civil and Environmental Engineering, Massachusetts Institute of Technology, Cambridge, MA, USA, 3 Australian Institute of Marine Science, Townsville, QLD, Australia Edited by: Rising seawater temperature associated with global climate change is a significant Ian Hewson, threat to coral health and is linked to increasing coral disease and pathogen-related Cornell University, USA bleaching events. We performed heat stress experiments with the coral Pocillopora Reviewed by: damicornis, where temperature was increased to 31◦C, consistent with the 2–3◦C Xiu-Lan Chen, Shandong University, China predicted increase in summer sea surface maxima. 16S rRNA amplicon sequencing Roberto Bastías, revealed a large shift in the composition of the bacterial community at 31◦C, with a Pontifical Catholic University of Valparaiso, Chile notable increase in Vibrio, including known coral pathogens. To investigate the dynamics *Correspondence: of the naturally occurring Vibrio community, we performed quantitative PCR targeting ◦ Jessica Tout, (i) the whole Vibrio community and (ii) the coral pathogen Vibrio coralliilyticus.At31C, Plant Functional Biology and Climate Vibrio abundance increased by 2–3 orders of magnitude and V. coralliilyticus abundance Change Cluster, University of Technology, Sydney, P. O. Box 123 increased by four orders of magnitude. Using a Vibrio-specific amplicon sequencing Broadway, NSW 2007, Australia assay, we further demonstrated that the community composition shifted dramatically as [email protected] a consequence of heat stress, with significant increases in the relative abundance of Specialty section: known coral pathogens. Our findings provide quantitative evidence that the abundance This article was submitted to of potential coral pathogens increases within natural communities of coral-associated Aquatic Microbiology, a section of the journal microbes as a consequence of rising seawater temperature and highlight the potential Frontiers in Microbiology negative impacts of anthropogenic climate change on coral reef ecosystems. Received: 05 March 2015 Keywords: Vibrio, Vibrio coralliilyticus, Pocillopora damicornis, corals, heat stress, pathogen Accepted: 22 April 2015 Published: 18 May 2015 Citation: Tout J, Siboni N, Messer LF, Introduction Garren M, Stocker R, Webster NS, Ralph PJ and Seymour JR (2015) The health and function of coral reefs is profoundly influenced by microorganisms, which Increased seawater temperature often form species-specific associations with corals (Rohwer et al., 2002; Rosenberg et al., 2007; increases the abundance and alters Mouchka et al., 2010). These ecological relationships can be mutualistic, commensal or pathogenic the structure of natural Vibrio (Rosenberg et al., 2007), and diseases caused by pathogenic microbes have been identified as a populations associated with the coral Pocillopora damicornis. key threat to coral reefs globally (Bourne et al., 2009; Burge et al., 2014). Diseases including white Front. Microbiol. 6:432. syndrome – which causes bleaching and lysis (Kushmaro et al., 1996; Ben-Haim et al., 2003a; doi: 10.3389/fmicb.2015.00432 Rosenberg and Falkovitz, 2004), white band (Ritchie and Smith, 1998; Aronson and Precht, 2001), Frontiers in Microbiology | www.frontiersin.org 1 May 2015 | Volume 6 | Article 432 Tout et al. Increased seawater temperature and natural Coral-Vibrios whiteplague(Thompson et al., 2001), white pox (Patterson et al., 2002; Ben-Haim et al., 2003b) and involves the post-colonization 2002), black band (Frias-Lopez et al., 2002; Sato et al., 2009), and production of a potent extracellular metalloproteinase, which yellow band (Cervino et al., 2008) have all been attributed to causes coral tissue damage (Ben-Haim and Rosenberg, 2002; Ben- microorganisms and have led to mass mortalities and significant Haim et al., 2003b). Another key similarity in the infection and loss of coral cover (Bourne et al., 2009). bleaching mechanisms of V. shiloi and V. coralliilyticus is an There is evidence that the occurrence and severity of coral dis- increased infection rate under elevated seawater temperatures ease outbreaks is increasing globally (Harvell et al., 2004; Bruno (Toren et al., 1998; Ben-Haim and Rosenberg, 2002; Ben-Haim et al., 2007; Mydlarz et al., 2010), potentially due to environ- et al., 2003b). mental stressors associated with phenomena such as increases Heat stress can enhance coral disease by increasing host in seawater temperature (Mouchka et al., 2010; Ruiz-Morenol susceptibility to infection by pathogens (Bourne et al., 2009; et al., 2012). Heat stress may compromise the health of corals, Mouchka et al., 2010) or altering the behavior and virulence of leading to enhanced susceptibility to disease (Hoegh-Guldberg, pathogenic bacteria (Kushmaro et al., 1998; Banin et al., 2001; 1999; Hoegh-Guldberg and Hoegh-Guldberg, 2004; Jokiel and Ben-Haim and Rosenberg, 2002; Ben-Haim et al., 2003a,b; Koren Brown, 2004), or increase the abundance and/or virulence of and Rosenberg, 2006; Bourne et al., 2008; Kimes et al., 2011; pathogens (Vega Thurber et al., 2009; Vezzulli et al., 2010; Kimes Santos Ede et al., 2011). Notably, V. shiloi can only be iso- et al., 2011). Increases in seawater temperature have been shown lated from bleached corals during summer months (Kushmaro to change the composition and functional capacity of coral- et al., 1998) and laboratory experiments have shown that this associated microbial communities, including shifts to an elevated species causes bleaching at an accelerated rate above 29◦C, yet ◦ state of virulence, and pathogenicity (Vega Thurber et al., 2009). has negligible effect at 16 C(Kushmaro et al., 1998). Similarly, While diverse groups of microbes, including bacteria, fungi, tissue loss caused by V. coralliilyticus is most rapid at elevated ◦ and viruses have been implicated in several coral diseases, one temperatures between 27 and 29 C(Ben-Haim and Rosenberg, bacterial genus in particular has become a recurrent feature 2002; Ben-Haim et al., 2003b). Seawater temperatures above ◦ within coral disease research. Vibrio are globally distributed 27 C have also been shown to play a direct role in the up- marine Gammaproteobacteria (Pollock et al., 2010), which har- regulation of several V. coralliilyticus virulence genes, including bor a diverse virulence repertoire that enables them to be effi- factors involved in host degradation, secretion, antimicrobial cient and widespread pathogens of a wide range of marine resistance, and motility (Kimes et al., 2011). Up-regulation of species (Santos Ede et al., 2011), including shell-fish (Jeffries, motility is particularly notable as both V. shiloi and V. coralli- 1982), fish (Austin et al., 2005), algae (Ben-Haim et al., 2003b), ilyticus exhibit enhanced chemotactic capacity at elevated tem- mammals (Kaper et al., 1995; Shapiro et al., 1998; Oliver, peratures (Banin et al., 2001; Garren et al., 2014). Heat-stressed 2005), and corals (Ben-Haim et al., 2003b). White syndrome corals also increase the production and release of signaling com- in Montipora corals is caused by V. owensii (Ushijima et al., pounds including dimethylsulfoniopropionate (DMSP) at ele- 2012), white band disease II in Acropora cervicornis has been vated temperature, further enhancing the ability of pathogens attributed to V. charchariae (synonym for V. harveyi; Gil- to locate, and colonize heat-stressed corals (Garren et al., Agudelo et al., 2006; Sweet et al., 2014), and a consortium of 2014). Vibrio are responsible for yellow band disease (Cervino et al., To date, our understanding of coral-associated Vibrio dynam- 2008; Ushijima et al., 2012). Furthermore, V. shiloi and V. coral- ics under elevated seawater temperatures has been solely liilyticus are the causative agents of bleaching in the coral species derived from laboratory-based experiments using cultured iso- Oculina patagonica (Kushmaro et al., 1996, 1997, 1998; Toren lates (Kushmaro et al., 1998; Toren et al., 1998; Banin et al., 2001; et al., 1998) and the cauliflower coral Pocillopora damicor- Ben-Haim and Rosenberg, 2002; Ben-Haim et al., 2003b;
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