Metabolomic signatures of coral bleaching history

Abstract

Coral bleaching, a process where corals expel their photosynthetic symbionts, has a profound impact on the health and function of coral reefs. As global ocean temperatures continue to rise, bleaching poses the greatest threat to coral reef ecosystems. Here, untargeted metabolomics was used to analyze the biochemicals in pairs of adjacent corals from a patch reef in Kāneʻohe Bay, Hawaiʻi, where one colony in the pair bleached (in 2015) and recovered while the other did not bleach. There was a strong metabolomic signature of prior bleaching history four years after recovery found in both the host and its algal symbionts. Machine learning analysis determined that the strongest metabolite drivers of the difference in bleaching phenotype were a group of betaine lipids. Those with saturated fatty acids were significantly enriched in thermally tolerant corals and those with longer, unsaturated and diacyl forms were enriched in historically bleached corals. Host immune response molecules, Lyso-PAF and PAF, were also altered by bleaching history and were strongly correlated with symbiont community and algal-derived metabolites suggesting a role of coral immune modulation in symbiont choice and bleaching response. To validate these findings, we tested a separate in situ set of corals and were able to predict the bleaching phenotype with 100% accuracy. Furthermore, corals subjected to an experimental temperature stress had strong phenotype-specific responses in all components of the holobiont, which served to further increase the differences between historical bleaching phenotypes. Thus, we show that natural bleaching susceptibility is simultaneously manifested in the biochemistry of the coral animal and the algal symbiont and that this bleaching history results in different physiological responses to temperature stress. This work provides insight into the biochemical mechanisms involved in coral bleaching and presents a valuable new tool for resilience-based reef restoration.

Marine heatwaves depress metabolic activity and impair cellular acid–base homeostasis in reef‐building corals regardless of bleaching susceptibility

“…In the context of repeat bleaching, the slower recovery of M. capitata than P. compressa from bleaching observed throughout Kaneohe Bay in 2015 (Matsuda et al, 2020; Ritson‐Williams & Gates, 2020) likely meant that bleaching‐susceptible M. capitata was in worse energetic standing than P. compressa going into the following event in 2019 and thus was more susceptible to severe bleaching despite lower levels of heat stress in the second event. Indeed, even 4 years following the 2015 bleaching event, bleaching‐susceptible colonies of M. capitata had distinct lipid profiles from bleaching‐resistant colonies despite both phenotypes appearing visually healthy (Roach et al, 2021), supporting the hypothesis that recovery prior to the 2019 event was incomplete in this species. A slow energetic recovery has been shown to make individuals less resistant to bleaching and mortality following repeat exposure to heat stress in other coral species (Sale et al, 2019), highlighting a barrier to acclimatization and the uneven harm of repeat bleaching on different coral species.…”

Metabolomics of healthy and stony coral tissue loss disease affected Montastraea cavernosa corals

“…The betaine lipids have been previously reported in endosymbionts from various coral species (Rosset et al, 2019;Sikorskaya, 2020;Sikorskaya et al, 2021) and are reported as biomarkers of bleaching history (Roach et al, 2021) and thermal tolerance (Leblond et al, 2015;Rosset et al, 2019). It has been previously suggested that betaine lipids being the component of cell membrane are influenced by the host genotype (Sikorskaya et al, 2021).…”

Selecting Heat-Tolerant Corals for Proactive Reef Restoration

“…Requires molecular work, may be transient, some species do not harbor diverse assemblages Potentially scalable, well-studied system, predictable tradeoffs Rowan, 2004;Berkelmans and van Oppen, 2006;Sampayo et al, 2008;Cantin et al, 2009;Cunning et al, 2016 Barshis et al, 2010;Innis et al, 2018;Mayfield et al, 2018;Majerova et al, 2020*;Williams et al, 2020*;Majerova and Drury, 2021*;Roach et al, 2021 *Indicates pre-prints available online.…”