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.

Fig. 1. Sampling overview and dinoRNAV detection summary from Porites lobata colonies on the reefs of Moorea, French Polynesia (South Pacific).

A Schematic cross section of sampled reef zones and representative images of focal Porites lobata coral colonies in each reef environment. Eighteen colonies per reef zone were tagged and sampled four times from August 2018 to October 2020. B Health trajectories of colonies between August 2018 and October 2020 based on image analysis. Orange icons represent colonies that remained visually healthy throughout the sampling duration, whereas blue icons indicate colonies that experienced partial mortality. Gray icons indicate colonies for which health trajectory was ambiguous based on the images available. Dark gray center dots indicate dinoRNAV detection. Light gray “N/A” dots indicates that a colony that was not sequenced due to poor RNA quality. C Number of unique dinoRNAV major capsid protein amino acid sequences (‘aminotypes’) detected in samples from all three reef zones (darker gray) or in two of the three zones (lighter gray). D Number of aminotypes detected exclusively in colonies within a given reef zone. E Boxplot and width distribution of aminotype richness per colony. Letters indicate significant differences in dinoRNAV aminotype richness based on a pairwise Wilcoxon test with Bonferroni correction (fringe vs. back, p = 0.10; fringe vs. fore, p < 0.01; back vs. fore, p = 0.99).

Fig. 2. Temperature fluctuated and the health of some Porites lobata colonies changed over time on coral reefs of Moorea, French Polynesia (South Pacific).

A Daily mean temperatures with 95% confidence interval over the sampling duration (temperature data collection ended prior to October 2020). B Representative coral health trajectories, depicting one colony that remained healthy at each sampling point over the study duration (orange box) and one colony that experienced partial mortality by October 2020 following bleaching in August 2019 (blue box, partial mortality outlined in white).

Fig. 3. Maximum likelihood tree of dinoRNAV major capsid protein (mcp) unique amino acid sequences (‘aminotypes’) from Porites lobata-Cladocopium C15 holobionts in this study as well as previously reported dinoRNAV mcp sequences and related viral sequences.

A maximum likelihood phylogeny with 500 bootstrap iterations was generated using dinoRNAV mcp aminotype sequences generated from Porites lobata-Cladocopium C15 holobionts from coral reefs of Moorea, French Polynesia (South Pacific) in this study, as well as previously reported mcp sequences from the Great Barrier Reef [30], Moorea [29], and related viral sequences such as the Beihai sobemo-like virus and the Barns Ness breadcrumb sponge weiviruslike-virus [44, 54]. This tree was outgroup rooted by the longest branch, Heterocapsa circularisquama RNA virus (HcRNAV, [52, 53]). Colors in the vertical bar (Aminotype Source, AS) indicate the origin of a given sequence. Branches with less than 50% bootstrap support were collapsed; branches with bootstrap support >70% are depicted with a black dot. Only aminotypes that were present in >10% relative abundance in at least one sample are included in the phylogeny. Gray tone heat maps indicate the number of colonies from which each aminotype was detected, separated by reef zone (rightmost columns 1–3). Circled numbers reference the three largest clades of dinoRNAV aminotypes from this study.

Fig. 4. Relative abundance of unique amino acid sequences (‘aminotypes’) detected in Porites lobata-Cladocopium C15 holobionts from coral reefs of Moorea, French Polynesia (South Pacific).

Each set of four bars represents one colony sampled over time (numerical colony ID above box); colonies are grouped by reef zone (rows) and sites (sequentially ordered across each row). Aminotypes comprising less than 5% relative abundance within a sample are depicted together in black at the top of vertical bars. All other colors represent distinct aminotypes. Triangles indicate positive dinoRNAV detection, but poor sequencing success (<1000 reads); X indicates no detection. Blank space (no symbol) indicates that a sample does not exist for a given time point.

Fig. 5. Bray-Curtis beta diversity metrics of dinoRNAV mcp aminotypes from Porites lobata-Cladocopium C15 colonies varied by reef type and sampling time on the reefs of Moorea, French Polynesia (South Pacific).

A Between-group distances (composition) varied by reef type, with the fringe and back reef differing the most. The boxplot displays Bray-Curtis distances of dinoRNAV mcp aminotypes from samples of each pairwise combination of reef types. Each dot represents the Bray-Curtis distance between a sample from one reef type and a sample of another reef type. B Within group distances (dispersion) varied across sampling timepoint. The boxplot displays mean within-group distances of dinoRNAV mcp aminotypes for each sample, separated by sampling timepoint. Each dot represents one sample; dots are colored according to reef type.

Fig. 6. Dispersion (within group distances) of dinoRNAV mcp aminotypes from Porites lobata-Cladocopium C15 colonies varied by thermal stress timepoint and colony health trajectory on the reefs of Moorea, French Polynesia (South Pacific).

Dispersion was overall higher in samples collected during reef bleaching timepoints. August 2018 and October 2020 samples were grouped as ambient temperature timepoints; March and August 2019 were grouped as “reef bleaching” related timepoints since they fell at the beginning and end of the bleaching event in Moorea. Colonies were grouped according to their health trajectory over the sampling duration (colonies that did not exhibit partial mortality- ‘healthy’ vs. colonies that did- ‘partial mortality’). Colonies with ambiguous health trajectories were excluded.