Report on Intergenerational Metabolomic Signatures of Bleaching Resistance in Corals

Abstract

Coral bleaching poses a significant threat to tropical reef ecosystems, necessitating the identification of attributes linked to coral resistance and resilience to thermal stress across generations. This study employs metabolomics to investigate biochemical signatures associated with heat-induced bleaching in Montipora capitata (rice coral). Through selective breeding of bleaching-resistant and susceptible parents, metabolomic signatures reflecting parental bleaching phenotypes were detected in sperm, eggs, embryos, larvae, and juvenile corals. These thermal tolerance signatures originate from both the coral host and algal symbionts, spanning diverse molecular families. Notably, the saturation state of DGCC betaine lipids, previously linked to thermal tolerance in dinoflagellate symbionts, emerged as a strong marker of intergenerational heat tolerance. Even progeny harboring thermally susceptible Cladocopium algae exhibited increased saturation of these lipids if their parents resisted bleaching. This evidence of biochemical inheritance as a mechanism for intergenerational acclimatization has vital implications for reef conservation and restoration amid climate change.

Introduction

Corals and their intracellular algal symbionts (family Symbiodiniaceae) form an ancient and ecologically crucial symbiosis, collectively known as the coral holobiont. Metabolites exchanged within this consortium underpin energy and nutrient cycling, with algal photosynthates supplying up to 95% of the coral’s energetic needs. However, environmental stressors such as ocean warming disrupt this metabolic exchange, leading to coral bleaching—the loss of algal symbionts—which threatens coral survival and reef ecosystem stability.

Bleaching involves complex genetic and biochemical changes in both coral hosts and algal symbionts. Prior studies have demonstrated transcriptional, microbial, and metabolomic impacts of heat stress. Untargeted metabolomics enables simultaneous assessment of metabolites from all holobiont members, providing insights into coral health and early stress signals.

Given the increasing frequency and severity of bleaching events, understanding mechanisms of thermal tolerance and their transmission across generations is critical. Montipora capitata vertically transmits its symbionts and passes thermal tolerance traits to offspring, but the extent to which biochemical signatures are inherited remains unclear.

This study uses untargeted metabolomic profiling across life stages of M. capitata with known thermal tolerance phenotypes to elucidate intergenerational biochemical inheritance mechanisms that support coral resilience under climate change.

Results

Metabolomic Variation Through the Coral Life Cycle

1. Samples of adult corals, sperm, eggs, embryos, larvae, and juveniles were collected from 47 parent colonies with distinct bleaching histories.
2. Untargeted metabolomics identified 7,532 metabolite features, with unique and shared metabolites across life stages.
3. Metabolome profiles significantly differed among life stages, with sperm metabolomes distinctly aposymbiotic.
4. Larval metabolomes changed progressively during development, reflecting dynamic biochemical processes.
5. Egg metabolomes showed closer similarity to their parent colonies compared to unrelated corals, indicating parental biochemical influence.

Intergenerational Thermal Tolerance Signatures in the Coral Metabolome

• Historical parental bleaching phenotype significantly explained metabolomic variation across all life stages.
• Post-fertilization stages (embryos, larvae, juveniles) exhibited strong parental bleaching phenotype signatures with 100% classification accuracy.
• Both host and symbiont metabolomes contributed to these intergenerational thermal tolerance signatures.

Molecular Families Driving Thermal Tolerance Signatures

• Metabolomic analysis revealed higher abundance of sesquiterpenoids, bile acids, triterpenoids, tetraterpenoids, steroid esters, amino acids, peptides, and glycerophospholipids in thermally resistant corals.
• These molecular families reflect biochemical adaptations linked to bleaching resistance.

Lipid Biochemistry Reflecting Thermal Tolerance is Vertically Transferred

• DGCC betaine lipids, particularly lyso-betaine lipids with saturated fatty acid tails, were strong classifiers of bleaching history across life stages.
• Thermally resistant corals showed higher abundance and saturation of DGCC lipids, including monoacyl forms, which increased during larval development.
• Host-derived phosphocholine lipids, such as platelet activating factor (PAF), also correlated with thermal tolerance.
• These findings suggest lipid biochemical properties from both host and symbiont are inherited and contribute to thermal resilience.

Association of the Metabolome with Symbiodiniaceae Genotypes

• Symbiont communities (genus Cladocopium, Durusdinium, or mixed) significantly influenced metabolome profiles.
• DGCC lipid biochemistry differed markedly between symbiont genera, particularly in lipid saturation states.
• Even corals hosting thermally susceptible Cladocopium exhibited DGCC lipid profiles associated with thermal tolerance if their parents were bleaching resistant.

Discussion

This study demonstrates that biochemical modifications linked to coral thermal stress responses are transmitted intergenerationally from parents to offspring. The persistence of these metabolomic signatures through all life stages, including both host and symbiont components, underscores their role as stable phenotypic markers of thermal tolerance.

DGCC betaine lipids, particularly saturated lyso-lipids, emerge as promising biomarkers and potential functional agents in maintaining coral-algal symbiosis under heat stress. The coordinated lipid biochemical patterns in both symbiont and host highlight a holistic mechanism of thermal resilience.

Parental biochemical imprinting likely occurs via multiple mechanisms including genetic and epigenetic inheritance, biochemical provisioning, and vertical symbiont transmission. The vertical transmission of symbionts in M. capitata supports the maintenance of lipidome profiles linked to thermal tolerance.

These findings have significant implications for coral reef conservation and restoration, aligning with Sustainable Development Goal 14 (Life Below Water) by enhancing coral resilience to climate change. Understanding and leveraging biochemical inheritance mechanisms can inform selective breeding and assisted evolution strategies to safeguard coral reef ecosystems.

Methods

Experimental Framework and Sampling

• Reproductively capable M. capitata colonies with known bleaching histories were collected and maintained under ambient conditions.
• Gametes were collected during spawning, separated into sperm and eggs, and used for selective breeding to produce offspring pools based on parental bleaching phenotype.
• Embryos, larvae, and juveniles were reared and sampled at multiple developmental stages for metabolomic analysis.

Metabolomic Analysis

• Untargeted metabolomics was performed using liquid chromatography-tandem mass spectrometry (LC-MS/MS).
• Metabolite features were identified and annotated using spectral databases and molecular networking.
• Metabolites were mapped to host or symbiont origin based on comparative abundance in bleached coral and purified symbiont samples.

Symbiont Genotyping

• Symbiodiniaceae communities were characterized using ITS2 marker gene sequencing and analyzed with Symportal.

Statistical and Machine Learning Analyses

• Alpha- and beta-diversity metrics were calculated to assess metabolomic variation.
• PERMANOVA and random forest classification were used to evaluate the influence of parental bleaching phenotype and genotype on metabolomes.
• Significant metabolites and molecular families were identified through variable importance and non-parametric tests.

Data Availability and Ethical Compliance

• All mass spectrometry and sequencing data are publicly accessible through GNPS MassIVE and NCBI repositories.
• Coral collections were conducted under appropriate permits ensuring ethical compliance.

Implications for Sustainable Development Goals (SDGs)

• SDG 14: Life Below Water – Enhancing coral thermal tolerance supports the conservation and sustainable use of marine ecosystems, crucial for biodiversity and livelihoods.
• SDG 13: Climate Action – Understanding intergenerational acclimatization mechanisms aids in mitigating climate change impacts on coral reefs.
• SDG 15: Life on Land – Coral reefs contribute to coastal protection and ecosystem services, linking marine and terrestrial sustainability.
• SDG 9: Industry, Innovation and Infrastructure – Application of advanced metabolomics and molecular techniques exemplifies innovation in environmental research.

This research underscores the importance of integrating biochemical inheritance knowledge into coral reef restoration strategies to foster resilient ecosystems in a warming world, thereby contributing to global sustainable development efforts.

1. Sustainable Development Goals (SDGs) Addressed or Connected

1. SDG 13: Climate Action
   • The article focuses on coral bleaching caused by thermal stress due to warming oceans, a direct consequence of climate change.
   • It discusses mechanisms of coral resilience and adaptation to climate-induced stress.
2. SDG 14: Life Below Water
   • The study centers on coral reef ecosystems, their health, and persistence.
   • It addresses coral bleaching, which threatens marine biodiversity and ecosystem services.
   • It highlights reef conservation and restoration efforts.
3. SDG 15: Life on Land
   • Indirectly relevant through ecosystem conservation and biodiversity maintenance.

2. Specific Targets Under Identified SDGs

1. SDG 13: Climate Action
   • Target 13.1: Strengthen resilience and adaptive capacity to climate-related hazards and natural disasters in all countries.
   • Target 13.3: Improve education, awareness-raising and human and institutional capacity on climate change mitigation, adaptation, impact reduction, and early warning.
2. SDG 14: Life Below Water
   • Target 14.2: Sustainably manage and protect marine and coastal ecosystems to avoid significant adverse impacts, and take action for their restoration to achieve healthy and productive oceans.
   • Target 14.5: By 2020, conserve at least 10 per cent of coastal and marine areas, consistent with national and international law and based on the best available scientific information.

3. Indicators Mentioned or Implied to Measure Progress

1. Coral Bleaching and Thermal Tolerance Indicators
   • Metabolomic signatures of coral bleaching resistance and susceptibility, including biochemical markers such as DGCC betaine lipids saturation state.
   • Presence and abundance of specific metabolites (e.g., lyso-betaine lipids, phosphocholine lipids) as biomarkers for thermal tolerance.
   • Genetic and symbiont community composition (e.g., Symbiodiniaceae genera like Cladocopium and Durusdinium) linked to bleaching susceptibility.
   • Metabolomic profiling across life stages (adults, gametes, embryos, larvae, juveniles) to assess intergenerational transmission of thermal tolerance.
2. Ecological and Biological Indicators
   • Frequency and severity of coral bleaching events over time.
   • Survivorship and growth rates of juvenile corals in restoration efforts.
   • Changes in metabolite diversity (richness, Shannon entropy) as indicators of coral health status.

4. Table of SDGs, Targets, and Indicators

Source: nature.com