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1. Thermotolerant coral–algal mutualisms maintain high rates of nutrient transfer while exposed to heat stress

   https://doi.org/10.1098/rspb.2023.1403  

   Kemp, Dustin W. ; Hoadley, Kenneth D. ; Lewis, Allison M. ; Wham, Drew C. ; Smith, Robin T. ; Warner, Mark E. ; LaJeunesse, Todd C. ( September 2023 , Proceedings of the Royal Society B: Biological Sciences)

   Symbiotic mutualisms are essential to ecosystems and numerous species across the tree of life. For reef-building corals, the benefits of their association with endosymbiotic dinoflagellates differ within and across taxa, and nutrient exchange between these partners is influenced by environmental conditions. Furthermore, it is widely assumed that corals associated with symbionts in the genusDurusdiniumtolerate high thermal stress at the expense of lower nutrient exchange to support coral growth. We traced both inorganic carbon (H¹³CO₃^–) and nitrate (¹⁵NO₃^–) uptake by divergent symbiont species and quantified nutrient transfer to the host coral under normal temperatures as well as in colonies exposed to high thermal stress. Colonies representative of diverse coral taxa associated withDurusdinium trenchiiorCladocopiumspp. exhibited similar nutrient exchange under ambient conditions. By contrast, heat-exposed colonies withD. trenchiiexperienced less physiological stress than conspecifics withCladocopiumspp. while high carbon assimilation and nutrient transfer to the host was maintained. This discovery differs from the prevailing notion that these mutualisms inevitably suffer trade-offs in physiological performance. These findings emphasize that many host–symbiont combinations adapted to high-temperature equatorial environments are high-functioning mutualisms; and why their increased prevalence is likely to be important to the future productivity and stability of coral reef ecosystems.

    

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2. Cladocopium community divergence in two Acropora coral hosts across multiple spatial scales

   https://doi.org/10.1111/mec.15668  

   Davies, Sarah_W ; Moreland, Kelsey_N ; Wham, Drew_C ; Kanke, Matt_R ; Matz, Mikhail_V ( October 2020 , Molecular Ecology)

   Many broadly‐dispersing corals acquire their algal symbionts (Symbiodiniaceae) “horizontally” from their environment upon recruitment. Horizontal transmission could promote coral fitness across diverse environments provided that corals can associate with divergent algae across their range and that these symbionts exhibit reduced dispersal potential. Here we quantified community divergence ofCladocopiumalgal symbionts in two coral host species (Acropora hyacinthus, Acropora digitifera) across two spatial scales (reefs on the same island, and between islands) across the Micronesian archipelago using microsatellites. We find that both hosts associated with a variety of multilocus genotypes (MLG) within two genetically distinctCladocopiumlineages (C40, C21), confirming thatAcroporacoral hosts associate with a range ofCladocopiumsymbionts across this region. Both C40 and C21 included multiple asexual lineages bearing identical MLGs, many of which spanned host species, reef sites within islands, and even different islands. Both C40 and C21 exhibited moderate host specialization and divergence across islands. In addition, within every island, algal symbiont communities were significantly clustered by both host species and reef site, highlighting that coral‐associatedCladocopiumcommunities are structured across small spatial scales and within hosts on the same reef. This is in stark contrast to their coral hosts, which never exhibited significant genetic divergence between reefs on the same island. These results support the view that horizontal transmission could improve local fitness for broadly dispersingAcroporacoral species.

    

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3. 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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4. 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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5. Filamentous virus-like particles are present in coral dinoflagellates across genera and ocean basins

   https://doi.org/10.1038/s41396-023-01526-6  

   Howe-Kerr, Lauren I. ; Knochel, Anna M. ; Meyer, Matthew D. ; Sims, Jordan A. ; Karrick, Carly E. ; Grupstra, Carsten G. B. ; Veglia, Alex J. ; Thurber, Andrew R. ; Vega Thurber, Rebecca L. ; Correa, Adrienne M. S. ( November 2023 , The ISME Journal)

   Filamentous viruses are hypothesized to play a role in stony coral tissue loss disease (SCTLD) through infection of the endosymbiotic dinoflagellates (Family Symbiodiniaceae) of corals. To evaluate this hypothesis, it is critical to understand the global distribution of filamentous virus infections across the genetic diversity of Symbiodiniaceae hosts. Using transmission electron microscopy, we demonstrate that filamentous virus-like particles (VLPs) are present in over 60% of Symbiodiniaceae cells (genusCladocopium) within Pacific corals (Acropora hyacinthus,Porites c.f. lobata); these VLPs are more prevalent in Symbiodiniaceae of in situ colonies experiencing heat stress. Symbiodiniaceae expelled fromA. hyacinthusalso contain filamentous VLPs, and these cells are more degraded than theirin hospitecounterparts. Similar to VLPs reported from SCTLD-affected Caribbean reefs, VLPs range from ~150 to 1500 nm in length and 16–37 nm in diameter and appear to constitute various stages in a replication cycle. Finally, we demonstrate that SCTLD-affected corals containing filamentous VLPs are dominated by diverse Symbiodiniaceae lineages from the generaBreviolum, Cladocopium, andDurusdinium. Although this study cannot definitively confirm or refute the role of filamentous VLPs in SCTLD, it demonstrates that filamentous VLPs are not solely observed in SCTLD-affected corals or reef regions, nor are they solely associated with corals dominated by members of a particular Symbiodiniaceae genus. We hypothesize that filamentous viruses are a widespread, common group that infects Symbiodiniaceae. Genomic characterization of these viruses and empirical tests of the impacts of filamentous virus infection on Symbiodiniaceae and coral colonies should be prioritized.

    

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