Transcriptomic resilience, symbiont shuffling, and vulnerability to recurrent bleaching in reef‐building corals

Abstract

As climate change progresses and extreme temperature events increase in frequency, rates of disturbance may soon outpace the capacity of certain species of reef‐building coral to recover from bleaching. This may lead to dramatic shifts in community composition and ecosystem function. Understanding variation in rates of bleaching recovery among species and how that translates to resilience to recurrent bleaching is fundamental to predicting the impacts of increasing disturbances on coral reefs globally. We tracked the response of two heat sensitive species in the genus Acropora to repeated bleaching events during the austral summers of 2015 and 2017. Despite a similar bleaching response, the species Acropora gemmifera recovered faster based on transcriptome‐wide gene expression patterns and had a more dynamic algal symbiont community than Acropora hyacinthus growing on the same reef. Moreover, A. gemmifera had higher survival to repeated heat extremes, with six‐fold lower mortality than A. hyacinthus. These patterns suggest that speed of recovery from a first round of bleaching, based on multiple mechanisms, contributes strongly to sensitivity to a second round of bleaching. Furthermore, our data uncovered intragenus variation in a group of corals thought generally to be heat‐sensitive and therefore paint a more nuanced view of the future health of coral reef ecosystems against a backdrop of increasing thermal disturbances.

Resilience in reef‐building corals: The ecological and evolutionary importance of the host response to thermal stress

“…Modules also show natural fluctuations involved in homeostasis during nonstressful events and how certain temperature thresholds produce a strong but temporary reaction relating to the unfolded protein response (Ruiz-Jones & Palumbi, 2017). A similar set of modules showed that experimental heat stress and response during recurrent bleaching was similar (Thomas et al, 2019). Correlations between transplant site, origin and various photosynthetic responses have also been documented for WGCNA modules in Porites astreoides (Kenkel & Matz, 2016), which were used to examine differences in plasticity of gene response.…”

“…This difference could be due to acclimatization, but the authors could not rule out symbiont shuffling or differential mortality leading to a higher proportion of resilient corals in the second event (Hughes et al, ). Studies that follow individual corals can conclusively rule out differential mortality, such as (Fisch, Drury, Towle, Winter, & Miller, ), who documented a substantial minority of surveyed colonies which experienced less severe visual bleaching in recurrent bleaching events that could be attributed to acclimatization (but see Thomas, López, Morikawa, & Palumbi, ).…”

“…Conversely, the negative effects of repeated bleaching events have also been documented in multiple ecosystems (reviewed by Baker et al, ), frequently showing consistent or more severe impacts during the later events. Thomas et al () found higher mortality in the second of two events in American Samoa, indicating that mechanisms that allow corals to recover from a single stress may be overwhelmed in recurrent events and any acclimatization capacity gained in the interim was lost. When multiple bleaching events occur over a short time span, corals may be more likely to succumb to stress because they are energetically compromised and still coping with latent, cryptic metabolic and transcriptomic alterations even if they appear healthy.…”

Stress Memory of Recurrent Environmental Challenges in Marine Invasive Species: Ciona robusta as a Case Study

“…Transcriptional resilience was an indicator to predict stress tolerance (Franssen et al, 2011). For example, the study on the resilient patterns of recurrent bleaching on corals (genus Acropora) showed that the resilience capacity after bleaching strongly contributed to the sensitivity to future bleaching, and the species A. gemmifera with a fast recovery speed resulted in a high level of survival under repeated heat extremes (Thomas et al, 2019). Similarly, the transcriptional resilience in this study adds evidence on the adaptative response against recurrent stresses and should be functional in adaptative homeostasis simultaneously.…”

Differential gene expression during substrate probing in larvae of the Caribbean coral Porites astreoides

“…This demonstrates that although expressed coral isoforms outnumber symbiont isoforms, highly expressed symbiont isoforms were expressed significantly more than coral isoforms. Few gene expression studies report read count statistics for individual isoforms or genes; however, one recent study similarly found thousands of contigs (contiguous gene sequences) that surpassed a minimum read count threshold to compare the transcriptomic response to recurrent bleaching events between two acroporid coral species (Thomas, López, Morikawa, & Palumbi, ).…”