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Bacterial Profiling of White Plague Disease Across Corals and Oceans

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Bacterial Profiling of White Plague Disease Across Corals and Oceans Molecular Ecology (2014) 23, 965–974 doi: 10.1111/mec.12638 Bacterial profiling of White Plague Disease across corals and oceans indicates a conserved and distinct disease microbiome CORNELIA RODER,* CHATCHANIT ARIF,* CAMILLE DANIELS,* ERNESTO WEIL† and CHRISTIAN R. VOOLSTRA* *Red Sea Research Center, King Abdullah University of Science and Technology, 23955 Thuwal, Saudi Arabia, †Department of Marine Sciences, University of Puerto Rico, PO BOX 9000, Mayaguez, Puerto Rico 00680, USA Abstract Coral diseases are characterized by microbial community shifts in coral mucus and tissue, but causes and consequences of these changes are vaguely understood due to the complexity and dynamics of coral-associated bacteria. We used 16S rRNA gene microarrays to assay differences in bacterial assemblages of healthy and diseased colo- nies displaying White Plague Disease (WPD) signs from two closely related Caribbean coral species, Orbicella faveolata and Orbicella franksi. Analysis of differentially abun- dant operational taxonomic units (OTUs) revealed strong differences between healthy and diseased specimens, but not between coral species. A subsequent comparison to data from two Indo-Pacific coral species (Pavona duerdeni and Porites lutea) revealed distinct microbial community patterns associated with ocean basin, coral species and health state. Coral species were clearly separated by site, but also, the relatedness of the underlying bacterial community structures resembled the phylogenetic relationship of the coral hosts. In diseased samples, bacterial richness increased and putatively opportunistic bacteria were consistently more abundant highlighting the role of oppor- tunistic conditions in structuring microbial community patterns during disease. Our comparative analysis shows that it is possible to derive conserved bacterial footprints of diseased coral holobionts that might help in identifying key bacterial species related to the underlying etiopathology. Furthermore, our data demonstrate that simi- lar-appearing disease phenotypes produce microbial community patterns that are con- sistent over coral species and oceans, irrespective of the putative underlying pathogen. Consequently, profiling coral diseases by microbial community structure over multiple coral species might allow the development of a comparative disease framework that can inform on cause and relatedness of coral diseases. Keywords: 16S rRNA gene microarray, coral disease, microbial community, Orbicella faveolata, Orbicella franksi, Pavona duerdeni, Porites lutea, White Plague Disease (WPD), White Plague-like Disease, White Syndrome (WS) Received 11 October 2013; revision received 13 December 2013; accepted 15 December 2013 the coral holobiont (Rohwer et al. 2002). A coral’s asso- Introduction ciated microbial community contributes fundamentally Corals are animals that live in a symbiotic relationship to the holobiont’s functioning due to its role in coral with photosynthetic dinoflagellates of the genus Symbi- nutrition (Lesser et al. 2004) and host defense (Ritchie & odinium as well as a rich bacterial community among Smith 2004; Kelman et al. 2006; Ritchie 2006). Coral dis- other microorganisms that are collectively referred to as eases are considered one of the most destructive local and geographical forces that impact corals and are Correspondence: Christian R. Voolstra, Fax: +966-2-8082377; responsible for major reef ecosystem declines over the E-mail: [email protected] past decades (Sutherland et al. 2004; Weil 2004; Willis © 2013 The Authors Molecular Ecology John Wiley & Sons Ltd. This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited. 966 C. RODER ET AL. et al. 2004; Weil et al. 2006; Harvell et al. 2007; Miller to detect either of these two putative pathogens (Pantos et al. 2009). et al. 2003; Barash et al. 2005; Sunagawa et al. 2009; Coral disease is defined as any abnormal condition Cardenas et al. 2012; Roder et al. 2014) suggesting that affecting the coral holobiont (Rosenberg et al. 2007), often different pathogens must be able to produce highly simi- described as a progressive loss of coral tissue due to viral, lar disease phenotypes (Weil 2004; Reshef et al. 2008; fungal, protozoan, or bacterial infections (Sutherland Weil & Rogers 2011). In the Great Barrier Reef and Indo- et al. 2004; Bourne et al. 2009) and facilitated by environ- Pacific region, phenotypes of WPD-like etiopathology mental factors (e.g. high sea surface temperatures). It have been denominated White Syndrome (WS) (Willis usually manifests through tissue discoloration and even- et al. 2004), and strains of the coral-bleaching pathogen tually tissue loss (necrosis). While the causative agents Vibrio coralliilyticus have been identified as potential remain unknown for most diseases (Rosenberg & Kush- infectious agents in a number of coral species (Sussman maro 2011), it has been shown that compromised health et al. 2008). Accordingly, indistinguishable disease phe- in corals is accompanied by shifts in the microbial com- notypes are produced by different pathogens (Weil & munity associated with the coral holobiont (Sunagawa Rogers 2011), and disease nomenclature can be mistaken. et al. 2009; Kimes et al. 2010; Cardenas et al. 2012; For this reason, we refer to coral colonies displaying Croquer et al. 2012; Roder et al. 2014). However, it is visual characteristics of White Syndrome, White Plague unclear whether infection of a single pathogen or or White Plague-like disease as WPD, acknowledging opportunistic infections secondary to exposure to physio- that this neither includes nor excludes the presence of the logical stress trigger the restructuring of microbial com- pathogens A. coralicida, T. loyana or V. coralliilyticus.On munities in coral disease (Lesser et al. 2007). While this is the other hand, how this convergent phenotypic resem- mainly due to the complexity and dynamics of the host blance relates to similarities in shifts in the underlying microbial assemblages (Rohwer et al. 2002; Hong et al. microbial community structure is at present unknown. 2009; Littman et al. 2009), difficulty in conducting experi- In this study, we analysed microbial communities of ments underwater, an overall lack of information on the healthy and WPD-affected coral tissues of Orbicella faveo- structure and composition of the ‘natural’ bacterial com- lata and Orbicella franksi (former genus Montastraea, Budd munity of corals, and differences in applied methodolo- et al. (2012)) from the Caribbean (Puerto Rico). Subse- gies further complicate the comparison of data. Sanger quently, we compared these data to microbial communi- cloning-and-sequencing approaches are now being com- ties of two coral species, Pavona duerdeni and Porites lutea, plemented by high-throughput methodologies and com- displaying WPD characteristics (Dustan 1977; Richardson parative analyses have shown that data from different 1998) from the Indo-Pacific (Gulf of Thailand) (Roder platforms produce similar results (Sunagawa et al. 2009; et al. 2014). We employed 16S rRNA gene microarrays Bayer et al. 2013). However, unequal sample read repre- (PhyloChipsTM) assaying 59 222 operational taxonomic sentation and the use of different 16S amplicon sites hin- units (OTUs) to profile microbial communities of healthy der a direct comparison between studies. PhyloChipTM (HH) and diseased (DD) coral colonies in a standardized 16S rRNA gene microarrays provide a standardized plat- framework. We aimed to determine whether microbial form and have been successfully used to uncover micro- community patterns of healthy and diseased colonies are bial community patterns in coral disease (Sunagawa et al. not only consistent between species from the same site 2009; Kellogg et al. 2012; Roder et al. 2014). (Roder et al. 2014), but also over larger geographical dis- White Plague disease (WPD) is one of the most tances, and how these patterns change between closely destructive and widespread coral diseases in Caribbean related and more distantly related coral species. reefs (Dustan 1977; Antonius 1985; Richardson et al. 1998; Miller et al. 2009; Weil et al. 2009). It presents as a Material and methods bright white band (i.e. clean skeletal structure resulting from disappearing tissue) that initiates at the base or Study site and sample collection sides of a colony and separates the living tissue from recently settled turf algae on the exposed skeleton that Sampling took place on 5 and 6 September 2011 at quickly advances across the colony surface. Depending Weimberg reef (between N 17°53′17.40/W 66°59′52.90 on the type of WPD (I, II or III), progression rates vary and N 17°53′25.40/W 66°59′19.00) off the southwest coast and different coral species are affected (Sutherland et al. of Puerto Rico. Two coral species (Orbicella faveolata and 2004; Weil & Rogers 2011). Aurantimonas coralicida O. franksi) were sampled via SCUBA between 16 and (Denner 2003) and Thalassomonas loyana (Thompson et al. 22 m depth. From both species, tissue samples from three 2006) were proposed as causative agents of WPD or healthy colonies (displaying no visible signs of stress) WPD-like in corals from the Caribbean and the Red Sea, and three colonies with WPD phenotype were collected. respectively. However, subsequent studies were unable All corals were of similar size. All healthy samples were © 2013 The Authors Molecular
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