physiological-characterization-coral-holobiont-using-new-micro

Physiological Characterization of the Coral Holobiont Using a New Micro-Respirometry Tool

Metabolic activity, defined as the sum of organismal processes that involve energy, is of critical importance in understanding the function and evolution ...

Minderoo Foundation

The dinoflagellate-coral partnership influences the coral holobiont's tolerance to thermal stress and bleaching. However, the comparative roles of host genetic versus environmental factors in determining the composition of this symbiosis are largely unknown. Here we quantify the heritability of the initial Symbiodinium communities for two broadcast-spawning corals with different symbiont transmission modes: Acropora tenuis has environmental acquisition, whereas Montipora digitata has maternal transmission. Using high throughput sequencing of the ITS-2 region to characterize communities in parents, juveniles and eggs, we describe previously undocumented Symbiodinium diversity and dynamics in both corals. After one month of uptake in the field, Symbiodinium communities associated with A. tenuis juveniles were dominated by A3, C1, D1, A-type CCMP828, and D1a in proportional abundances conserved between experiments in two years. M. digitata eggs were predominantly characterized by C15, D1, and A3. In contrast to current paradigms, host genetic influences accounted for a surprising 29% of phenotypic variation in Symbiodinium communities in the horizontally-transmitting A. tenuis, but only 62% in the vertically-transmitting M. digitata. Our results reveal hitherto unknown flexibility in the acquisition of Symbiodinium communities and substantial heritability in both species, providing material for selection to produce partnerships that are locally adapted to changing environmental conditions.

Heritability of the Symbiodinium community in vertically- and horizontally-transmitting broadcast spawning corals.

Determining the extent to which Symbiodinium communities in corals are inherited versus environmentally acquired is fundamental to understanding coral resilience and to predicting coral responses to stressors like warming oceans that disrupt this critical endosymbiosis. We examined the fidelity with which Symbiodinium communities in the brooding coral Seriatopora hystrix are vertically transmitted and the extent to which communities are genetically regulated, by genotyping the symbiont communities within 60 larvae and their parents (9 maternal and 45 paternal colonies) using high-throughput sequencing of the ITS2 locus. Unexpectedly, Symbiodinium communities associated with brooded larvae were distinct from those within parent colonies, including the presence of types not detected in adults. Bayesian heritability (h) analysis revealed that 33% of variability in larval Symbiodinium communities was genetically controlled. Results highlight flexibility in the establishment of larval symbiont communities and demonstrate that symbiont transmission is not exclusively vertical in brooding corals. Instead, we show that Symbiodinium transmission in S. hystrix involves a mixed-mode strategy, similar to many terrestrial invertebrate symbioses. Also, variation in the abundances of common Symbiodinium types among adult corals suggests that microhabitat differences influence the structure of in hospite Symbiodinium communities. Partial genetic regulation coupled with flexibility in the environmentally acquired component of Symbiodinium communities implies that corals with vertical transmission, like S. hystrix, may be more resilient to environmental change than previously thought.

Unexpected mixed-mode transmission and moderate genetic regulation of Symbiodinium communities in a brooding coral.

Adult organisms may "prime" their offspring for environmental change through a number of genetic and non-genetic mechanisms, termed parental effects. Some coral species may shuffle the proportions of Symbiodiniaceae within their endosymbiotic communities, subsequently altering their thermal tolerance, but it is unclear if shuffled communities are transferred to offspring. We evaluated Symbiodiniaceae community composition in tagged colonies of Montipora digitata over two successive annual spawning seasons and the 2016 bleaching event on the Great Barrier Reef. ITS2 amplicon sequencing was applied to four families (four maternal colonies and 10-12 eggs per family) previously sampled and sequenced the year before to characterize shuffling potential in these M. digitata colonies and determine if shuffled abundances were preserved in gametes. Symbiont densities and photochemical efficiencies differed significantly among adults in 2016, suggesting differential responses to increased temperatures. Low-abundance ("background") sequence variants differed more among years than between maternal colonies and offspring. Results indicate that shuffling can occur in a canonically 'stable' symbiosis, and that the shuffled community is heritable. Hence, acclimatory changes like shuffling of the Symbiodiniaceae community are not limited to the lifetime of an adult coral and that shuffled communities are inherited across generations in a species with vertical symbiont transmission. Although previously hypothesized, to our knowledge, this is the first evidence that shuffled Symbiodiniaceae communities (at both the inter- and intra- genera level) can be inherited by offspring and supports the hypothesis that shuffling in microbial communities may serve as a mechanism of rapid coral acclimation to changing environmental conditions.

Transgenerational inheritance of shuffled symbiont communities in the coral Montipora digitata.

The rate of coral reef degradation from climate change is accelerating and, as a consequence, a number of interventions to increase coral resilience and accelerate recovery are under consideration.  coral colonies that survived mass bleaching in 2016 and 2017 were sourced from a bleaching-impacted and warmer northern reef on the Great Barrier Reef (GBR). These individuals were reproductively crossed with colonies collected from a recently bleached but historically cooler central GBR reef to produce pure and crossbred offspring groups (warm-warm, warm-cool and cool-warm). We tested whether corals from the warmer reef produced more thermally tolerant hybrid and purebred offspring compared with crosses produced with colonies sourced from the cooler reef and whether different symbiont taxa affect heat tolerance. Juveniles were infected with ,  and  and survival, bleaching and growth were assessed at 27.5°C and 31°C. The contribution of host genetic background and symbiont identity varied across fitness traits. Offspring with either both or one parent from the northern population exhibited a 13- to 26-fold increase in survival odds relative to all other treatments where survival probability was significantly influenced by familial cross identity at 31°C but not 27.5°C (Kaplan-Meier 0.001 versus 0.2). If in symbiosis with , a warm sire and cool dam provided the best odds of juvenile survival. Bleaching was predominantly driven by Symbiodiniaceae treatment, where juveniles hosting  bleached significantly less than the other treatments at 31°C. The greatest overall fold-benefits in growth and survival at 31°C occurred in having at least one warm dam and in symbiosis with  Juveniles associated with  grew the most at 31°C, but at 27.5°C, growth was fastest in juveniles associated with  In conclusion, selective breeding with warmer GBR corals in combination with algal symbiont manipulation can assist in increasing thermal tolerance on cooler but warming reefs. Such interventions have the potential to improve coral fitness in warming oceans.This article has an associated First Person interview with the first author of the paper.

Assessing the role of historical temperature regime and algal symbionts on the heat tolerance of coral juveniles.

Finding coral reefs resilient to climate warming is challenging given the large spatial scale of reef ecosystems. Methods are needed to predict the location of corals with heritable tolerance to high temperatures. Here, we combine Great Barrier Reef-scale remote sensing with breeding experiments that estimate larval and juvenile coral survival under exposure to high temperatures. Using reproductive corals collected from the northern and central Great Barrier Reef, we develop forecasting models to locate reefs harbouring corals capable of producing offspring with increased heat tolerance of an additional 3.4° heating weeks (~3 °C). Our findings predict hundreds of reefs (~7.5%) may be home to corals that have high and heritable heat-tolerance in habitats with high daily and annual temperature ranges and historically variable heat stress. The locations identified represent targets for protection and consideration as a source of corals for use in restoration of degraded reefs given their potential to resist climate change impacts and repopulate reefs with tolerant offspring.

Predictive models for the selection of thermally tolerant corals based on offspring survival.

Recent warm temperatures driven by climate change have caused mass coral bleaching and mortality across the world, prompting managers, policymakers, and conservation practitioners to embrace restoration as a strategy to sustain coral reefs. Despite a proliferation of new coral reef restoration efforts globally and increasing scientific recognition and research on interventions aimed at supporting reef resilience to climate impacts, few restoration programs are currently incorporating climate change and resilience in project design. As climate change will continue to degrade coral reefs for decades to come, guidance is needed to support managers and restoration practitioners to conduct restoration that promotes resilience through enhanced coral reef recovery, resistance, and adaptation. Here, we address this critical implementation gap by providing recommendations that integrate resilience principles into restoration design and practice, including for project planning and design, coral selection, site selection, and broader ecosystem context. We also discuss future opportunities to improve restoration methods to support enhanced outcomes for coral reefs in response to climate change. As coral reefs are one of the most vulnerable ecosystems to climate change, interventions that enhance reef resilience will help to ensure restoration efforts have a greater chance of success in a warming world. They are also more likely to provide essential contributions to global targets to protect natural biodiversity and the human communities that rely on reefs.

A roadmap to integrating resilience into the practice of coral reef restoration.

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 of Acropora tenuis colonies 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 progenitor Cladocopium and the more stress tolerant Durusdinium, 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.

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

Survival of symbiotic reef-building corals under global warming requires rapid acclimation or adaptation. The impact of accumulated heat stress was compared across 1643 symbiont communities before and after the 2016 mass bleaching in three coral species and free-living in the environment across ~900 kilometers of the Great Barrier Reef. Resilient reefs (less aerial bleaching than predicted from high satellite sea temperatures) showed low variation in symbioses. Before 2016, heat-tolerant environmental symbionts were common in ~98% of samples and moderately abundant (9 to 40% in samples). In corals, heat-tolerant symbionts were at low abundances (0 to 7.3%) but only in a minority (13 to 27%) of colonies. Following bleaching, environmental diversity doubled (including heat-tolerant symbionts) and increased in one coral species. Communities were dynamic () and conserved ( and ), including symbiont community turnover and redistribution. Symbiotic restructuring after bleaching occurs but is a taxon-specific ecological opportunity.

Article	Year
Heritability of the Symbiodinium community in vertically- and horizontally-transmitting broadcast spawning corals. Scientific reports\| PubMed ID: 28811517	2017
Unexpected mixed-mode transmission and moderate genetic regulation of Symbiodinium communities in a brooding coral. Heredity\| PubMed ID: 29453423	2018
Transgenerational inheritance of shuffled symbiont communities in the coral Montipora digitata. Scientific reports\| PubMed ID: 31527788	2019
Assessing the role of historical temperature regime and algal symbionts on the heat tolerance of coral juveniles. Biology open\| PubMed ID: 31915210	2020
Predictive models for the selection of thermally tolerant corals based on offspring survival. Nature communications\| PubMed ID: 35351901	2022
A roadmap to integrating resilience into the practice of coral reef restoration. Global change biology\| PubMed ID: 35451154	2022
The role of gene expression and symbiosis in reef-building coral acquired heat tolerance. Nature communications\| PubMed ID: 35922443	2022
Symbioses are restructured by repeated mass coral bleaching. Science advances\| PubMed ID: 36475796	2022

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