Viruses of a key coral symbiont exhibit temperature-driven productivity across a reefscape

Abstract

Viruses can affect coral health by infecting their symbiotic dinoflagellate partners (Symbiodiniaceae). Yet, viral dynamics in coral colonies exposed to environmental stress have not been studied at the reef scale, particularly within individual viral lineages. We sequenced the viral major capsid protein (mcp) gene of positive-sense single-stranded RNA viruses known to infect symbiotic dinoflagellates (‘dinoRNAVs’) to analyze their dynamics in the reef-building coral, Porites lobata. We repeatedly sampled 54 colonies harboring Cladocopium C15 dinoflagellates, across three environmentally distinct reef zones (fringing reef, back reef, and forereef) around the island of Moorea, French Polynesia over a 3-year period and spanning a reef-wide thermal stress event. By the end of the sampling period, 28% (5/18) of corals in the fringing reef experienced partial mortality versus 78% (14/18) of corals in the forereef. Over 90% (50/54) of colonies had detectable dinoRNAV infections. Reef zone influenced the composition and richness of viral mcp amino acid types (‘aminotypes’), with the fringing reef containing the highest aminotype richness. The reef-wide thermal stress event significantly increased aminotype dispersion, and this pattern was strongest in the colonies that experienced partial mortality. These findings demonstrate that dinoRNAV infections respond to environmental fluctuations experienced in situ on reefs. Further, viral productivity will likely increase as ocean temperatures continue to rise, potentially impacting the foundational symbiosis underpinning coral reef ecosystems.

Stony coral tissue loss disease induces transcriptional signatures of in situ degradation of dysfunctional Symbiodiniaceae

“…As a hotspot for coral diseases, the Caribbean is particularly at risk of severe biodiversity loss, exhibiting a 50–80% decline in living coral tissue since the 1970s 4 , 5 . Although the etiologic agents of many of these diseases remain elusive, one prevailing hypothesis postulates that a growing number of diseases result from environmentally induced microbiome imbalances and a subsequent increase in opportunistic or polymicrobial infections 6 , 7 . As climate change pressures continue to escalate, emerging and endemic outbreaks in the Caribbean are likely to decimate reef-building coral populations, resulting in reef ecosystem collapse.…”

Microbiome ecological memory and responses to repeated marine heatwaves clarify variation in coral bleaching and mortality

“…A variety of factors not measured in this study may explain different microbiome–host outcomes, including coral host genotype background (Rosales et al., 2019; Williams et al., 2022), benthic community dynamics, variation in Symbiodiniaceae lineages and composition (Howe‐Kerr et al., 2023; Jones & Berkelmans, 2010; Kriefall et al., 2022; LaJeunesse et al., 2018), virome dynamics (Howe‐Kerr et al., 2023; Levin et al., 2017; Messyasz et al., 2020; Vega Thurber et al., 2017), and bacterial strain‐level functional variation. For example, multiple strains of the proposed mutualist Endozoicomonadaceae have been observed in Pocillopora spp.…”

“…Along with the dominant bacterial taxa, it is well known that changes in dinoflagellate symbiont profiles can result in variable colony responses to thermal stress (Howe‐Kerr et al., 2023; Jones & Berkelmans, 2010; Kriefall et al., 2022; LaJeunesse et al., 2018). In Mo'orean Acropora hyacinthus colonies, reef zones structure symbiont and holobiont communities (Kriefall et al., 2022; Leinbach et al., 2023), which might have an impact on host thermal tolerance at our forereef sites.…”

“…Along with the dominant bacterial taxa, it is well known that changes in dinoflagellate symbiont profiles can result in variable colony responses to thermal stress (Howe-Kerr et al, 2023;Jones & Berkelmans, 2010;Kriefall et al, 2022;LaJeunesse et al, 2018).…”

“…A variety of factors not measured in this study may explain different microbiome-host outcomes, including coral host genotype background (Rosales et al, 2019;Williams et al, 2022) (Howe- Kerr et al, 2023;Levin et al, 2017;Messyasz et al, 2020;Vega Thurber et al, 2017), and bacterial strain-level functional variation. For example, multiple strains of the proposed mutualist Endozoicomonadaceae have been observed in Pocillopora spp.…”