Metatranscriptome analysis of the reef-building coral Orbicella faveolata indicates holobiont response to coral disease

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 holobiont-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.

Unraveling the microbial processes of black band disease in corals through integrated genomics

“…Recent advances in high-throughput sequencing technologies and bioinformatic methodologies have enabled an improved understanding of coral diseases by profiling genomes and transcriptomes of host, symbionts and potential pathogens596061. The integrated genomic approach applied in this study documented the differences in microbial function between comparatively benign CP lesions and virulent BBD lesions, providing in-depth insights into the microbial mechanisms responsible for the development and progression of BBD in corals.…”

Disentangling causation: complex roles of coral‐associated microorganisms in disease

“…In some cases, causation has been inferred based on retrieval of sequences affiliated with previously characterized pathogens. Recently metagenomic, metatranscriptomic and metaproteomic approaches have also been providing unprecedented information on microbial gene content, actively expressed genes and translated proteins within coral disease lesions, further contributing information on roles of microorganisms in the disease processes (e.g., Santos Ede et al ., ; Burge et al ., ; Correa et al ., ; Daniels et al ., ; Garcia et al ., ; Sato et al ., ; Wood‐Charlson et al ., ). While all approaches have their merits, care should be taken in interpretation of the results, especially the interaction and causation which can only be confirmed through directly linking the agent with the disease lesion at both the gross and cellular levels (Work et al ., ; Work and Meteyer, ).…”

Microbiome engineering: enhancing climate resilience in corals

“…This approach has been implemented in more recent studies, such as an examination of active microbial players in coral disease (eg Daniels et al . ) and identification of key proteins of healthy and diseased corals, which provided insights into how the transition occurs between these two states (Garcia et al . ).…”

“…Metatranscriptomics and metaproteomics reveal which microbial genes are active at a given time point. This approach has been implemented in more recent studies, such as an examination of active microbial players in coral disease (eg Daniels et al 2015) and identification of key proteins of healthy and diseased corals, which provided insights into how the transition occurs between these two states (Garcia et al 2016). These "meta'omics" techniques, in addition to traditional culturing methods, may offer further elucidation of active and important microbial partners during climatebased stress events (eg coral bleaching), which can then be targeted for ME.…”