Evidence for a role of viruses in the thermal sensitivity of coral photosymbionts

Abstract

Symbiodinium, the dinoflagellate photosymbiont of corals, is posited to become more susceptible to viral infections when heat-stressed. To investigate this hypothesis, we mined transcriptome data of a thermosensitive and a thermotolerant type C1 Symbiodinium population at ambient (27 °C) and elevated (32°C) temperatures. We uncovered hundreds of transcripts from nucleocytoplasmic large double-stranded DNA viruses (NCLDVs) and the genome of a novel positive-sense single-stranded RNA virus (+ssRNAV). In the transcriptome of the thermosensitive population only, +ssRNAV transcripts had remarkable expression levels in the top 0.03% of all transcripts at 27 °C, but at 32 °C, expression levels of +ssRNAV transcripts decreased, while expression levels of anti-viral transcripts increased. In both transcriptomes, expression of NCLDV transcripts increased at 32 °C, but thermal induction of NCLDV transcripts involved in DNA manipulation was restricted to the thermosensitive population. Our findings reveal that viruses infecting Symbiodinium are affected by heat stress and may contribute to Symbiodinium thermal sensitivity.

Viruses in corals: hidden drivers of coral bleaching and disease?

“…). Transcripts of the ssRNA virus were shown to be present at high abundance in a heat-sensitive Symbiodinium culture, while they were barely detectable in a conspecific heat-tolerant culture, suggesting Symbiodinium and perhaps coral thermal tolerance is linked to the presence of this virus 19 . In order to progress the research in the field, PCR primers have been designed to assess presence and diversity of the ssRNA virus; these primers can potentially be modified for virus quantification during in situ coral bleaching events 20 .…”

Reef invertebrate viromics: diversity, host specificity and functional capacity

“…The absence of a known Phycodnaviridae host within the sponge holobionts indicates either an expansion of the host range for this viral family or that these particular sponge species filter and concentrate phototrophic microorganisms from the seawater. In corals, the Phycodnaviridae likely target the associated dinoflagellate symbionts Symbiodinium (Correa et al, 2016;Levin et al, 2017;Weynberg et al, 2017). Parvoviridae, which were traditionally thought to infect vertebrates and arthropods but have recently been reported from a range of marine invertebrates including corals (François et al, 2016), were particularly prevalent in the sponges I. basta, R. odorabile and the coral P. acuta as well as the GBR seawater.…”

“…The frequency of viruses matching Herpesviridae is more variable across coral species (Wood-Charlson et al, 2015), but this family has been observed in healthy and bleached corals using both TEM and metagenomics (Correa et al, 2016). Furthermore, Phycodnaviridae have been reported from both transcriptomic (Levin et al, 2017) and viromic (Correa et al, 2013;Weynberg et al, 2017) datasets derived from coral-isolated Symbiodinium cultures. ssDNA viruses have also been proposed as members of the core coral virome (Vega Thurber et al, 2017), with the prevalence of Circoviridae and Microviridae increasing in stressed/bleached corals (Littman et al, 2011;Soffer et al, 2014).…”

Rapid adaptive responses to climate change in corals

“…For example, shuffling of bacterial genes may result in wider metabolic potential, with coincident beneficial consequences for the coral host, for example, a broader range of products produced by dimethylsulfoniopropionate (DMSP)-metabolizing bacteria might enhance bacteria-mediated production of sulfur-based antimicrobials 97 . Despite such possible beneficial roles, however, viruses more typically have negative effects on host fitness and, in the case of corals, have been implicated in bleaching 98,99 and disease 100 .…”