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1. Direct evidence of sex and a hypothesis about meiosis in Symbiodiniaceae

   https://doi.org/10.1038/s41598-021-98148-9  

   Figueroa, R. I. ; Howe-Kerr, L. I. ; Correa, A. M. ( December 2021 , Scientific Reports)

   null (Ed.)

   Abstract Dinoflagellates in the family Symbiodiniaceae are obligate endosymbionts of diverse marine invertebrates, including corals, and impact the capacity of their hosts to respond to climate change-driven ocean warming. Understanding the conditions under which increased genetic variation in Symbiodiniaceae arises via sexual recombination can support efforts to evolve thermal tolerance in these symbionts and ultimately mitigate coral bleaching, the breakdown of the coral-Symbiodiniaceae partnership under stress. However, direct observations of meiosis in Symbiodiniaceae have not been reported, despite various lines of indirect evidence that it occurs. We present the first cytological evidence of sex in Symbiodiniaceae based on nuclear DNA content and morphology using Image Flow Cytometry, Cell Sorting and Confocal Microscopy. We show the Symbiodiniaceae species, Cladocopium latusorum , undergoes gamete conjugation, zygote formation, and meiosis within a dominant reef-building coral in situ. On average, sex was detected in 1.5% of the cells analyzed (N = 10,000–40,000 cells observed per sample in a total of 20 samples obtained from 3 Pocillopora colonies). We hypothesize that meiosis follows a two-step process described in other dinoflagellates, in which diploid zygotes form dyads during meiosis I, and triads and tetrads as final products of meiosis II. This study sets the stage for investigating environmental triggers of Symbiodiniaceae sexuality and can accelerate the assisted evolution of a key coral symbiont in order to combat reef degradation. 

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2. Symbiotic dinoflagellates divert energy away from mutualism during coral bleaching recovery

   https://doi.org/10.1007/s13199-023-00901-3  

   Allen-Waller, Luella ; Barott, Katie L. ( March 2023 , Symbiosis)

   The future of coral reefs in a warming world depends on corals’ ability to recover from bleaching, the loss of their symbiotic dinoflagellate algae (Symbiodiniaceae) during marine heatwaves. Heat-tolerant symbiont species can remain in symbiosis during heat stress, but often provide less photosynthate to the host than heat-sensitive species under ambient conditions. Understanding how heat stress changes the dynamics of this tradeoff between stress tolerance and mutualism contribution is crucial for predicting coral success under climate change. To test how symbiont resource allocation affects coral recovery from heat stress, we exposed the coral Montipora capitata hosting either heat-sensitive Cladocopium C31 (C) or heat-tolerant Durusdinium glynnii (D) to heat stress. D regained symbiont density and photochemical efficiency faster after heat treat- ment than C, but symbiont recovery did not restore coral biomass or calcification rates to pre-bleaching levels in the initial recovery period. D populations also contributed less photosynthate to the host relative to C, even during heat stress. Further, higher-density symbiont populations of both species retained more photosynthate than lower-density populations, and corals receiving less photosynthate exhibited reduced calcification rates and lower intracellular pH. This is the first evidence that symbiont density and carbon translocation are negatively related, and the first to establish a link between Symbiodiniaceae carbon translocation and coral cellular homeostasis. Together, these results suggest the energy demand of symbiont regrowth after bleaching reduces their mutualism contribution and can thus delay host recovery. Reestablishing a beneficial endos- ymbiosis imposes additional costs as holobionts overcome stress, and may explain latent mortality among coral populations after alleviation of heat stress in the field. 

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3. Increased dominance of heat-tolerant symbionts creates resilient coral reefs in near-term ocean warming

   https://doi.org/10.1073/pnas.2202388120  

   Palacio-Castro, Ana M. ; Smith, Tyler B. ; Brandtneris, Viktor ; Snyder, Grace A. ; van Hooidonk, Ruben ; Maté, Juan L. ; Manzello, Derek ; Glynn, Peter W. ; Fong, Peggy ; Baker, Andrew C. ( February 2023 , Proceedings of the National Academy of Sciences)

   Climate change is radically altering coral reef ecosystems, mainly through increasingly frequent and severe bleaching events. Yet, some reefs have exhibited higher thermal tolerance after bleaching severely the first time. To understand changes in thermal tolerance in the eastern tropical Pacific (ETP), we compiled four decades of temperature, coral cover, coral bleaching, and mortality data, including three mass bleaching events during the 1982 to 1983, 1997 to 1998 and 2015 to 2016 El Niño heatwaves. Higher heat resistance in later bleaching events was detected in the dominant framework-building genus, Pocillopora, while other coral taxa exhibited similar susceptibility across events. Genetic analyses of Pocillopora spp . colonies and their algal symbionts (2014 to 2016) revealed that one of two Pocillopora lineages present in the region ( Pocillopora “ type 1”) increased its association with thermotolerant algal symbionts ( Durusdinium glynnii ) during the 2015 to 2016 heat stress event. This lineage experienced lower bleaching and mortality compared with Pocillopora “type 3”, which did not acquire D. glynnii . Under projected thermal stress, ETP reefs may be able to preserve high coral cover through the 2060s or later, mainly composed of Pocillopora colonies that associate with D. glynnii . However, although the low-diversity, high-cover reefs of the ETP could illustrate a potential functional state for some future reefs, this state may only be temporary unless global greenhouse gas emissions and resultant global warming are curtailed. 

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4. Farmerfish gardens help buffer stony corals against marine heat waves

   https://doi.org/10.1371/journal.pone.0282572  

   Honeycutt, Randi N. ; Holbrook, Sally J. ; Brooks, Andrew J. ; Schmitt, Russell J. ( March 2023 , PLOS ONE)

   Melzner, Frank (Ed.)

   With marine heat waves increasing in intensity and frequency due to climate change, it is important to understand how thermal disturbances will alter coral reef ecosystems since stony corals are highly susceptible to mortality from thermally-induced, mass bleaching events. In Moorea, French Polynesia, we evaluated the response and fate of coral following a major thermal stress event in 2019 that caused a substantial amount of branching coral (predominantly Pocillopora ) to bleach and die. We investigated whether Pocillopora colonies that occurred within territorial gardens protected by the farmerfish Stegastes nigricans were less susceptible to or survived bleaching better than Pocillopora on adjacent, undefended substrate. Bleaching prevalence (proportion of the sampled colonies affected) and severity (proportion of a colony’s tissue that bleached), which were quantified for >1,100 colonies shortly after they bleached, did not differ between colonies within or outside of defended gardens. By contrast, the fates of 399 focal colonies followed for one year revealed that a bleached coral within a garden was a third less likely to suffer complete colony death and about twice as likely to recover to its pre-bleaching cover of living tissue compared to Pocillopora outside of a farmerfish garden. Our findings indicate that while residing in a farmerfish garden may not reduce the bleaching susceptibility of a coral to thermal stress, it does help buffer a bleached coral against severe outcomes. This oasis effect of farmerfish gardens, where survival and recovery of thermally-damaged corals are enhanced, is another mechanism that helps explain why large Pocillopora colonies are disproportionately more abundant in farmerfish territories than elsewhere in the lagoons of Moorea, despite gardens being relatively uncommon. As such, some farmerfishes may have an increasingly important role in maintaining the resilience of branching corals as the frequency and intensity of marine heat waves continue to increase. 

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5. 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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