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1. Symbiont shuffling induces differential DNA methylation responses to thermal stress in the coral Montastraea cavernosa

   https://doi.org/10.1111/mec.16246  

   Rodriguez‐Casariego, Javier A. ; Cunning, Ross ; Baker, Andrew C. ; Eirin‐Lopez, Jose M. ( November 2021 , Molecular Ecology)

   Algal symbiont shuffling in favour of more thermotolerant species has been shown to enhance coral resistance to heat‐stress. Yet, the mechanistic underpinnings and long‐term implications of these changes are poorly understood. This work studied the modifications in coral DNA methylation, an epigenetic mechanism involved in coral acclimatization, in response to symbiont manipulation and subsequent heat stress exposure. Symbiont composition was manipulated in the great star coralMontastraea cavernosathrough controlled thermal bleaching and recovery, producing paired ramets of three genets dominated by either their native symbionts (genusCladocopium) or the thermotolerant species (Durusdinium trenchi). Single‐base genome‐wide analyses showed significant modifications in DNA methylation concentrated in intergenic regions, introns and transposable elements. Remarkably, DNA methylation changes in response to heat stress were dependent on the dominant symbiont, with twice as many differentially methylated regions found in heat‐stressed corals hosting different symbionts (Cladocopiumvs.D.trenchii) compared to all other comparisons. Interestingly, while differential gene body methylation was not correlated with gene expression, an enrichment in differentially methylated regions was evident in repetitive genome regions. Overall, these results suggest that changes in algal symbionts favouring heat tolerant associations are accompanied by changes in DNA methylation in the coral host. The implications of these results for coral adaptation, along with future avenues of research based on current knowledge gaps, are discussed in the present work.

    

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2. The role of gene expression and symbiosis in reef-building coral acquired heat tolerance

   https://doi.org/10.1038/s41467-022-32217-z  

   Strader, Marie E. ; Quigley, Kate M. ( August 2022 , Nature Communications)

   Predicting how reef-building corals will respond to accelerating ocean warming caused by climate change requires knowledge of how acclimation and symbiosis modulate heat tolerance in coral early life-history stages. We assayed transcriptional responses to heat in larvae and juveniles of 11 reproductive crosses ofAcropora tenuiscolonies along the Great Barrier Reef. Larvae produced from the warmest reef had the highest heat tolerance, although gene expression responses to heat were largely conserved by cross identity. Juvenile transcriptional responses were driven strongly by symbiosis – when in symbiosis with heat-evolved Symbiodiniaceae, hosts displayed intermediate expression between its progenitorCladocopiumand the more stress tolerantDurusdinium, indicating the acquisition of tolerance is a conserved evolutionary process in symbionts. Heat-evolved Symbiodiniaceae facilitated juvenile survival under heat stress, although host transcriptional responses to heat were positively correlated among those hosting different genera of Symbiodiniaceae. These findings reveal the relative contribution of parental environmental history as well as symbiosis establishment in coral molecular responses to heat in early life-history stages.

    

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3. Biogeographic variability in the physiological response of the cold‐water coral Lophelia pertusa to ocean acidification

   https://doi.org/10.1111/maec.12373  

   Georgian, Samuel E. ; Dupont, Sam ; Kurman, Melissa ; Butler, Adam ; Strömberg, Susanna M. ; Larsson, Ann I. ; Cordes, Erik E. ( September 2016 , Marine Ecology)

   While ocean acidification is a global issue, the severity of ecosystem effects is likely to vary considerably at regional scales. The lack of understanding of how biogeographically separated populations will respond to acidification hampers our ability to predict the future of vital ecosystems. Cold‐water corals are important drivers of biodiversity in ocean basins across the world and are considered one of the most vulnerable ecosystems to ocean acidification. We tested the short‐term physiological response of the cold‐water coralLophelia pertusato three pH treatments (pH = 7.9, 7.75 and 7.6) for Gulf of Mexico (USA) and Tisler Reef (Norway) populations, and found that reductions in seawater pH elicited contrasting responses. Gulf of Mexico corals exhibited reductions in net calcification, respiration and prey capture rates with decreasing pH. In contrast, Tisler Reef corals showed only slight reductions in net calcification rates under decreased pH conditions while significantly elevating respiration and capture rates. These differences are likely the result of environmental differences (depth, pH, food supply) between the two regions, invoking the potential for local adaptation or acclimatization to alter their response to global change. However, it is also possible that variations in the methodology used in the experiments contributed to the observed differences. Regardless, these results provide insights into the resilience ofL. pertusato ocean acidification as well as the potential influence of regional differences on the viability of species in future oceans.

    

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4. Thermotolerant coral symbionts modulate heat stress‐responsive genes in their hosts

   https://doi.org/10.1111/mec.15526  

   Cunning, Ross ; Baker, Andrew C. ( July 2020 , Molecular Ecology)

   Some corals may become more resistant to bleaching by shuffling their Symbiodiniaceae communities toward thermally tolerant species, and manipulations to boost the abundance of these symbionts in corals may increase resilience in warming oceans. However, the thermotolerant symbiontDurusdinium trenchiimay reduce growth and fecundity in Caribbean corals, and these tradeoffs need to be better understood as this symbiont spreads through the region. We sought to understand howD. trenchiimodulates coral gene expression by manipulating symbiont communities inMontastraea cavernosato produce replicate ramets containingD. trenchiitogether with paired ramets of these same genets (n = 3) containingCladocopiumC3 symbionts. We then examined differences in global gene expression between corals hostingDurusdiniumandCladocopiumunder control temperatures, and in response to short‐term heat stress. We identified numerous transcriptional differences associated with symbiont identity, which explained 2%–14% of the transcriptional variance. Corals withD. trenchiiupregulated genes related to translation, ribosomal structure and biogenesis, and downregulated genes related to extracellular structures, and carbohydrate and lipid transport and metabolism, relative to corals withCladocopium. Unexpectedly, these changes were similar to those observed inCladocopium‐dominated corals in response to heat stress, suggesting that thermotolerantD. trenchiimay cause corals to increase expression of heat stress‐responsive genes, explaining both the increased heat tolerance and the associated energetic tradeoffs in corals containingD. trenchii. These findings provide insight into the ecological changes occurring on contemporary coral reefs in response to climate change, and the diverse ways in which different symbionts modulate emergent phenotypes of their hosts.

    

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5. Cophylogeny and specificity between cryptic coral species ( Pocillopora spp.) at Mo′orea and their symbionts (Symbiodiniaceae)

   https://doi.org/10.1111/mec.16654  

   Johnston, Erika C. ; Cunning, Ross ; Burgess, Scott C. ( August 2022 , Molecular Ecology)

   The congruence between phylogenies of tightly associated groups of organisms (cophylogeny) reflects evolutionary links between ecologically important interactions. However, despite being a classic example of an obligate symbiosis, tests of cophylogeny between scleractinian corals and their photosynthetic algal symbionts have been hampered in the past because both corals and algae contain genetically unresolved and morphologically cryptic species. Here, we studied co‐occurring, crypticPocilloporaspecies from Mo′orea, French Polynesia, that differ in their relative abundance across depth. We constructed new phylogenies of the hostPocillopora(using complete mitochondrial genomes, genomic loci, and thousands of single nucleotide polymorphisms) and their Symbiodiniaceae symbionts (using ITS2 and psbA^ncrmarkers) and tested for cophylogeny. The analysis supported the presence of fivePocilloporaspecies on the fore reef at Mo′orea that mostly hosted eitherCladocopium latusorumorC. pacificum.OnlyPocilloporaspecies hostingC. latusorumalso hosted taxa fromSymbiodiniumandDurusdinium. In general, theCladocopiumphylogeny mirrored thePocilloporaphylogeny. WithinCladocopiumspecies, lineages also differed in their associations withPocilloporahaplotypes, except those showing evidence of nuclear introgression, and with depth in the two most commonPocilloporaspecies. We also found evidence for a newPocilloporaspecies (haplotype 10), that has so far only been sampled from French Polynesia, that warrants formal identification. The linked phylogenies of thesePocilloporaandCladocopiumspecies and lineages suggest that symbiont speciation is driven by niche diversification in the host, but there is still evidence for symbiont flexibility in some cases.

    

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