Association of coral algal symbionts with a diverse viral community responsive to heat shock

Abstract

BackgroundStony corals provide the structural foundation of coral reef ecosystems and are termed holobionts given they engage in symbioses, in particular with photosynthetic dinoflagellates of the genus Symbiodinium. Besides Symbiodinium, corals also engage with bacteria affecting metabolism, immunity, and resilience of the coral holobiont, but the role of associated viruses is largely unknown. In this regard, the increase of studies using RNA sequencing (RNA-Seq) to assess gene expression provides an opportunity to elucidate viral signatures encompassed within the data via careful delineation of sequence reads and their source of origin.ResultsHere, we re-analyzed an RNA-Seq dataset from a cultured coral symbiont (Symbiodinium microadriaticum, Clade A1) across four experimental treatments (control, cold shock, heat shock, dark shock) to characterize associated viral diversity, abundance, and gene expression. Our approach comprised the filtering and removal of host sequence reads, subsequent phylogenetic assignment of sequence reads of putative viral origin, and the assembly and analysis of differentially expressed viral genes. About 15.46% (123 million) of all sequence reads were non-host-related, of which <1% could be classified as archaea, bacteria, or virus. Of these, 18.78% were annotated as virus and comprised a diverse community consistent across experimental treatments. Further, non-host related sequence reads assembled into 56,064 contigs, including 4856 contigs of putative viral origin that featured 43 differentially expressed genes during heat shock. The differentially expressed genes included viral kinases, ubiquitin, and ankyrin repeat proteins (amongst others), which are suggested to help the virus proliferate and inhibit the algal host’s antiviral response.ConclusionOur results suggest that a diverse viral community is associated with coral algal endosymbionts of the genus Symbiodinium, which prompts further research on their ecological role in coral health and resilience.Electronic supplementary materialThe online version of this article (doi:10.1186/s12866-017-1084-5) contains supplementary material, which is available to authorized users.

Initial virome characterization of the common cnidarian lab modelNematostella vectensis

“…Finally, the most common family of Exaiptasia virome, Herpesviridae, was not found in any of the remaining sea anemones. Herpesviruses have been previously associated with other cnidarian species [3,58,59] and with Symbiodinium microadriaticum found in corals [14]. Given that E. pallida is also a host to several members of Symbiodinium family [60] and the contribution of Herpesviridae decreases in aposymbiotic state when compared to a fully symbiotic Exaiptasia (8.1% and 12.9%, respectively) [16], it is possible that this viral family is associated with the presence of these symbionts and hence, not found in sea anemone species which do not harbor zooxanthellae.…”

“…Among cnidarians, much focus has been placed on deciphering the composition and significance of virome of corals (reviewed in [13]), their photosynthetic dinoflagellate symbionts from the Symbiodinium genus [14,15], and their symbiotic sea anemone proxy Exaiptasia pallida (formerly called Aiptasia pallida) [16], mainly due to the environmental significance of the coral reef ecosystems. Members of coral virome have been suggested to play a role in some coral diseases [17,18], and a general increase of viral abundance has been observed during bleaching (loss of dinoflagellate symbionts) of several coral species [19][20][21].…”

Peer Review #1 of "First insight into the viral community of the cnidarian model metaorganism Aiptasia using RNA-Seq data (v0.2)"

“…Despite the importance of microorganisms to their multicellular hosts (McFall-Ngai et al, 2013), basic knowledge about the viral community of many organisms, including the model metaorganism Aiptasia, is still lacking. The vastness of next-generation sequencing datasets provides an opportunity to begin to investigate the viral diversity (Li et al, 2015), using approaches that filter the target organism and classify remaining sequence reads (Brüwer et al, 2017). In this study, we used a previously generated Aiptasia RNA-Seq dataset to gain a first insight into the viral community associated with Aiptasia across three different symbiotic states (aposymbiotic, partially populated, fully symbiotic) with Symbiodinium.…”

“…To provide a first insight into Aiptasia viral community composition, we employed a strategy, previously employed by Brüwer et al (2017) to assess Symbiodinium-associated viruses, to reanalyze an existing RNA-Seq dataset (Baumgarten et al, 2015). The transcriptomic dataset comprised aposymbiotic Aiptasia of the strain CC7 as well as CC7 Aiptasia partially populated and fully symbiotic with endosymbiotic algae of the strain SSB01 (Clade B1, Symbiodinium minutum).…”

Reading the Book of Life – Omics as a Universal Tool Across Disciplines

“…The exact same dataset was used by Brüwer et al (2017), who in silico detected a diverse viral community associated with the dinoflagellate and observed differential viral gene expression upon heat treatment. As in this example, nextgeneration sequencing often contains "by-catch" of hostassociated microorganisms and viruses, which may be assessed separately (see also Levin et al 2017;Brüwer and Voolstra 2018; Brüwer and Voolstra within the abstracts related to this chapter).…”