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1. Contrasting effects of Symbiodinium identity on coral host transcriptional profiles across latitudes

   https://doi.org/10.1111/mec.14774  

   Barfield, Sarah J. ; Aglyamova, Galina V. ; Bay, Line K. ; Matz, Mikhail V. ( July 2018 , Molecular Ecology)

   Reef‐building corals can increase their resistance to heat‐induced bleaching through adaptation and acclimatization and/or by associating with a more thermo‐tolerant strain of algal symbiont (Symbiodiniumsp.). Here, we show that these two adaptive pathways interact. We collectedAcropora milleporacorals from two contrasting thermal environments on the Great Barrier Reef: cooler, mid‐latitude Orpheus Island, where all corals hosted a heat‐sensitive clade CSymbiodinium, and warmer, low‐latitude Wilkie Island, where corals hosted either a clade C or a more thermo‐tolerant clade D. Corals were kept in a benign common garden to reveal differences in baseline gene expression, reflecting prior adaptation/long‐term acclimatization. Model‐based analysis identified gene expression differences between Wilkie and Orpheus corals that were negatively correlated with previously described transcriptome‐wide signatures of heat stress, signifying generally elevated thermotolerance of Wilkie corals. Yet, model‐free analyses of gene expression revealed that Wilkie corals hosting clade C were distinct from Wilkie corals hosting clade D, whereas Orpheus corals were more variable. Wilkie corals hosting clade C symbionts exhibited unique functional signatures, including downregulation of histone proteins and ion channels and upregulation of chaperones andRNAprocessing genes, putatively representing constitutive “frontloading” of stress response genes. Furthermore, clade CSymbiodiniumexhibited constitutive expression differences between Wilkie and Orpheus, indicative of contrasting life history strategies. Our results demonstrate that hosting alternativeSymbiodiniumtypes is associated with different pathways of local adaptation for the coral host. These interactions could play a significant role in setting the direction of genetic adaptation to global warming in the two symbiotic partners.

    

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2. Spatial and Temporal Patterns of Symbiont Colonization and Loss During Bleaching in the Model Sea Anemone Aiptasia

   https://doi.org/10.3389/fmars.2022.808696  

   Tivey, Trevor R. ; Coleman, Tyler J. ; Weis, Virginia M. ( March 2022 , Frontiers in Marine Science)

   The ability of symbionts to recolonize their hosts after a period of dysbiosis is essential to maintain a resilient partnership. Many cnidarians rely on photosynthate provided from a large algal symbiont population. Under periods of thermal stress, symbiont densities in host cnidarians decline, and the recovery of hosts is dependent on the re-establishment of symbiosis. The cellular mechanisms that govern this process of colonization are not well-defined and require further exploration. To study this process in the symbiotic sea anemone model Exaiptasia diaphana , commonly called Aiptasia, we developed a non-invasive, efficient method of imaging that uses autofluorescence to measure the abundance of symbiont cells, which were spatially distributed into distinct cell clusters within the gastrodermis of host tentacles. We estimated cell cluster sizes to measure the occurrence of singlets, doublets, and so on up to much larger cell clusters, and characterized colonization patterns by native and non-native symbionts. Native symbiont Breviolum minutum rapidly recolonized hosts and rapidly exited under elevated temperature, with increased bleaching susceptibility for larger symbiont clusters. In contrast, populations of non-native symbionts Symbiodinium microadriaticum and Durusdinium trenchii persisted at low levels under elevated temperature. To identify mechanisms driving colonization patterns, we simulated symbiont population changes through time and determined that migration was necessary to create observed patterns (i.e., egression of symbionts from larger clusters to establish new clusters). Our results support a mechanism where symbionts repopulate hosts in a predictable cluster pattern, and provide novel evidence that colonization requires both localized proliferation and continuous migration. 

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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 genotype influences holobiont response to increased temperature

   https://doi.org/10.1038/s41598-022-23244-3  

   Moffat, Jennica J. ; Coffroth, Mary Alice ; Wallingford, Piper D. ; terHorst, Casey P. ( November 2022 , Scientific Reports)

   As coral reefs face warming oceans and increased coral bleaching, a whitening of the coral due to loss of microalgal endosymbionts, the possibility of evolutionary rescue offers some hope for reef persistence. In tightly linked mutualisms, evolutionary rescue may occur through evolution of the host and/or endosymbionts. Many obligate mutualisms are composed of relatively small, fast-growing symbionts with greater potential to evolve on ecologically relevant time scales than their relatively large, slower growing hosts. Numerous jellyfish species harbor closely related endosymbiont taxa to other cnidarian species such as coral, and are commonly used as a model system for investigating cnidarian mutualisms. We examined the potential for adaptation of the upside-down jellyfishCassiopea xamachanato increased temperature via evolution of its microalgal endosymbiont,Symbiodinium microadriaticum. We quantified trait variation among five algal genotypes in response to three temperatures (26 °C, 30 °C, and 32 °C) and fitness of hosts infected with each genotype. All genotypes showed positive growth rates at each temperature, but rates of respiration and photosynthesis decreased with increased temperature. Responses varied among genotypes but were unrelated to genetic similarity. The effect of temperature on asexual reproduction and the timing of development in the host also depended on the genotype of the symbiont. Natural selection could favor different algal genotypes at different temperatures, affecting host fitness. This eco-evolutionary interaction may be a critical component of understanding species resilience in increasingly stressful environments.

    

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5. Individual variation in growth and physiology of symbionts in response to temperature

   https://doi.org/10.1002/ece3.9000  

   terHorst, Casey P. ; Coffroth, Mary Alice ( June 2022 , Ecology and Evolution)

   In many cases, understanding species’ responses to climate change requires understanding variation among individuals in response to such change. For species with strong symbiotic relationships, such as many coral reef species, genetic variation in symbiont responses to temperature may affect the response to increased ocean temperatures. To assess variation among symbiont genotypes, we examined the population dynamics and physiological responses of genotypes ofBreviolum antillogorgiumin response to increased temperature. We found broad temperature tolerance across genotypes, with all genotypes showing positive growth at 26, 30, and 32°C. Genotypes differed in the magnitude of the response of growth rate and carrying capacity to increasing temperature, suggesting that natural selection could favor different genotypes at different temperatures. However, the historical temperature at which genotypes were reared (26 or 30°C) was not a good predictor of contemporary temperature response. We found increased photosynthetic rates and decreased respiration rates with increasing contemporary temperature, and differences in physiology among genotypes, but found no significant differences in the response of these traits to temperature among genotypes. In species with such broad thermal tolerance, selection experiments on symbionts outside of the host may not yield results sufficient for evolutionary rescue from climate change.

    

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