Abstract
White Plague Disease (WPD) is implicated in coral reef decline in the Caribbean and is characterized by microbial community shifts in coral mucus and tissue. Studies thus far have focused on assessing microbial communities or the identification of specific pathogens, yet few have addressed holobiont response across metaorganism compartments in coral disease. Here, we report on the first metatranscriptomic assessment of the coral host, algal symbiont, and microbial compartment in order to survey holobiont structure and function in healthy and diseased samples from Orbicella faveolata collected at reef sites off Puerto Rico. Our data indicate metaorganism-wide as well as compartment-specific responses to WPD. Gene expression changes in the diseased coral host involved proteins playing a role in innate immunity, cytoskeletal integrity, cell adhesion, oxidative stress, chemical defense, and retroelements. In contrast, the algal symbiont showed comparatively few expression changes, but of large magnitude, of genes related to stress, photosynthesis, and metal transport. Concordant with the coral host response, the bacterial compartment showed increased abundance of heat shock proteins, genes related to oxidative stress, DNA repair, and potential retroelement activity. Importantly, analysis of the expressed bacterial gene functions establishes the participation of multiple bacterial families in WPD pathogenesis and also suggests a possible involvement of viruses and/or phages in structuring the bacterial assemblage. In this study, we implement an experimental approach to partition the coral holobiont and resolve compartment- and taxa-specific responses in order to understand metaorganism function in coral disease.
Highlights
Coral disease is a major threat to coral reef ecosystems that has increased and contributed to the decline of reef ecosystems globally over the last 40 years (Weil and Rogers, 2011)
We found multiple stress and virulence genes to be associated with Alteromonadaceae, Rhodobacteraceae, Flavobacteriaceae, Enterobacteriaceae, and Vibrionaceae, which were consistently found in WPDaffected coral species by Roder et al (2014a) and suggested to be opportunistic bacteria (Supplementary Data 7)
All Holobiont Compartments Respond to Coral Disease By comparing active gene functions across the coral host, algal symbiont, and associated microbes of the coral holobiont, our data show that all compartments respond to White Plague Disease (WPD) infection and indicate that studying the bacterial community in isolation may bias interpretation of etiopathology
Summary
Coral disease is a major threat to coral reef ecosystems that has increased and contributed to the decline of reef ecosystems globally over the last 40 years (Weil and Rogers, 2011). WPD is described as a bacterial infection (Dustan, 1977; Richardson et al, 1998) reported to potentially afflict over 40 coral species (Weil et al, 2006) and is responsible for several local and widespread epizootic events that have caused significant reef degradation in the Caribbean (Miller et al, 2009; Weil and Croquer, 2009). In addition to ongoing studies targeting bacterial community changes during WPD progression (Sunagawa et al, 2009; Cárdenas et al, 2012; Roder et al, 2014a,b), a recent metagenomic survey of Orbicella annularis found distinct viral communities associated with healthy, WPD-affected, and bleached samples (Soffer et al, 2014). Using a combination of 16S and cDNA microarrays, Closek et al (2014) found an increase in microbial diversity in Yellow Band Disease (YBD)-infected colonies and reduced expression of defense- and metabolism-related genes in the coral host Orbicella faveolata [formerly Monstastraea faveolata (Budd et al, 2012)]
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