Coral reef symbioses under a changing climate: an integrative approach

Emma Marangon explored coral reef holobiont responses to future climate through an integrative approach. She found that parental exposure to climate stressors can influence the offspring microbiome, and host-symbiont nutrient recycling is a key player in the stability of coral reef symbioses. Her research deepens our understanding of complex symbiotic interactions, providing important insights for targeting future reef intervention strategies

Comparative genome-centric analysis reveals seasonal variation in the function of coral reef microbiomes

Microbially mediated processes contribute to coral reef resilience yet, despite extensive characterisation of microbial community variation following environmental perturbation, the effect on microbiome function is poorly understood. We undertook metagenomic sequencing of sponge, macroalgae and seawater microbiomes from a macroalgae-dominated inshore coral reef to define their functional potential and evaluate seasonal shifts in microbially mediated processes. In total, 125 high-quality metagenome-assembled genomes were reconstructed, spanning 15 bacterial and 3 archaeal phyla. Multivariate analysis of the genomes relative abundance revealed changes in the functional potential of reef microbiomes in relation to seasonal environmental fluctuations (e.g. macroalgae biomass, temperature). For example, a shift from Alphaproteobacteria to Bacteroidota-dominated seawater microbiomes occurred during summer, resulting in an increased genomic potential to degrade macroalgal-derived polysaccharides. An 85% reduction of Chloroflexota was observed in the sponge microbiome during summer, with potential consequences for nutrition, waste product removal, and detoxification in the sponge holobiont. A shift in the Firmicutes:Bacteroidota ratio was detected on macroalgae over summer with potential implications for polysaccharide degradation in macroalgal microbiomes. These results highlight that seasonal shifts in the dominant microbial taxa alter the functional repertoire of host-associated and seawater microbiomes, and highlight how environmental perturbation can affect microbially mediated processes in coral reef ecosystems.Australian Government Department of Industry, Innovation and Science; Advance Queensland PhD Scholarship Great Barrier Reef Marine Park Authority Management Award National Environmental Science Program (NESP)info:eu-repo/semantics/publishedVersio

The promotion of stress tolerant Symbiodiniaceae dominance in juveniles of two coral species under simulated future conditions of ocean warming and acidification

The symbiotic relationship between coral and its endosymbiotic algae, Symbiodiniaceae, greatly influences the hosts’ potential to withstand environmental stress. To date, the effects of climate change on this relationship has primarily focused on adult corals. Uncovering the effects of environmental stress on the establishment and development of this symbiosis in early life stages is critical for predicting how corals may respond to climate change. To determine the impacts of future climate projections on the establishment of symbionts in juvenile corals, ITS2 amplicon sequencing of single coral juveniles was applied to Goniastrea retiformis and Acropora millepora before and after exposure to three climate conditions of varying temperature and pCO2 levels (current and RCP8.5 in 2050 and 2100). Compared to ambient conditions, juvenile corals experienced shuffling in the relative abundance of Cladocopium (C1m, decrease) to Durusdinium (D1 and D1a, increase) over time. We calculated a novel risk metric incorporating functional redundancy and likelihood of impact on host physiology to identify the loss of D1a as a “low risk” to the coral compared to the loss of “higher risk” taxa like D1 and C1m. Although the increase in stress tolerant Durusdinium under future warming was encouraging for A. millepora, by 2100, G. retiformis communities displayed signs of symbiosis de-regulation, suggesting this acclimatory mechanism may have species-specific thresholds. Whilst this study cannot specifically disentangle the individual effects of temperature and pCO2, it does provide valuable insights into the impacts of both stressors combined. These results emphasize the need for understanding of long-term effects of climate change induced stress on coral juveniles, and their potential for increased acclimation to heat tolerance through changes in symbiosis

Life-stage specificity and cross-generational climate effects on the microbiome of a tropical sea urchin (Echinodermata: Echinoidea)

Microbes play a critical role in the development and health of marine invertebrates, though microbial dynamics across life stages and host generations remain poorly understood in most reef species, especially in the context of climate change. Here, we use a 4-year multigenerational experiment to explore microbe–host interactions under the Intergovernmental Panel on Climate Change (IPCC)-forecast climate scenarios in the rock-boring tropical urchin Echinometra sp. A. Adult urchins (F0) were exposed for 18 months to increased temperature and pCO2 levels predicted for years 2050 and 2100 under RCP 8.5, a period which encompassed spawning. After rearing F1 offspring for a further 2 years, spawning was induced, and F2 larvae were raised under current day and 2100 conditions. Cross-generational climate effects were also explored in the microbiome of F1 offspring through a transplant experiment. Using 16S rRNA gene sequence analysis, we determined that each life stage and generation was associated with a distinct microbiome, with higher microbial diversity observed in juveniles compared to larval stages. Although life-stage specificity was conserved under climate conditions projected for 2050 and 2100, we observed changes in the urchin microbial community structure within life stages. Furthermore, we detected a climate-mediated parental effect when juveniles were transplanted among climate treatments, with the parental climate treatment influencing the offspring microbiome. Our findings reveal a potential for cross-generational impacts of climate change on the microbiome of a tropical invertebrate species

Seawater carbonate chemistry and risk-taking behavior in prey (shrimps)

Marine prey and predators will respond to future climate through physiological and behavioral adjustments. However, our understanding of how such direct effects may shift the outcome of predator–prey interactions is still limited. Here, we investigate the effects of ocean warming and acidification on foraging behavior and biomass of a common prey (shrimps, Palaemon spp.) tested in large mesocosms harboring natural resources and habitats. Acidification did not alter foraging behavior in prey. Under warming, however, prey showed riskier behavior by foraging more actively and for longer time periods, even in the presence of a live predator. No effects of longer-term exposure to climate stressors were detected on prey biomass. Our findings suggest that ocean warming may increase the availability of some prey to predators via a behavioral pathway (i.e., increased risk-taking by prey), likely by elevating metabolic demand of prey species

Ocean warming increases availability of crustacean prey via riskier behavior

Marine prey and predators will respond to future climate through physiological and behavioral adjustments. However, our understanding of how such direct effects may shift the outcome of predator–prey interactions is still limited. Here, we investigate the effects of ocean warming and acidification on foraging behavior and biomass of a common prey (shrimps, Palaemon spp.) tested in large mesocosms harboring natural resources and habitats. Acidification did not alter foraging behavior in prey. Under warming, however, prey showed riskier behavior by foraging more actively and for longer time periods, even in the presence of a live predator. No effects of longer-term exposure to climate stressors were detected on prey biomass. Our findings suggest that ocean warming may increase the availability of some prey to predators via a behavioral pathway (i.e., increased risk-taking by prey), likely by elevating metabolic demand of prey species

Microbiome-mediated mechanisms contributing to the environmental tolerance of reef invertebrate species

Coral reefs globally are increasingly impacted by climate change. High temperature and pCO2 levels disrupt multiple physiological and biochemical pathways in marine organisms, often leading to disease and mortality in sensitive reef species. Host-associated microbes contribute critical functions that underpin host health, and environmentally induced changes in microbial communities represent a potential source for new metabolic features within holobiont systems. However, whether the acquisition of new beneficial microbial functions contributes to environmental acclimatisation of reef species is currently unknown. Using extensively studied model systems, we identify potential direct and indirect microbiome-mediated mechanisms that may contribute to environmental acclimatisation in reef invertebrate species. These mechanisms include increasing energy metabolism in the host, reduction of oxidative stress, regulation of nutrients in host cells, and increased pathogen resistance. We also propose a robust experimental strategy to test how microbial metabolic pathways may facilitate environmental acclimatisation of reef taxa. Understanding the mechanisms of microbiome-mediated acclimatisation and the timescales over which it can occur will be critical for predicting reef ecosystem dynamics under future climate scenarios and applying effective reef conservation strategies

Microbes from Mum: symbiont transmission in the tropical reef sponge Ianthella basta

Este artículo contiene 12 páginas, 5 figuras, 1 tabla.Most marine sponge species harbour distinct communities of microorganisms which contribute to various aspects of their host’s health and physiology. In addition to their key roles in nutrient transformations and chemical defence, these symbiotic microbes can shape sponge phenotype by mediating important developmental stages and influencing the environmental tolerance of the host. However, the characterisation of each microbial taxon throughout a sponge’s life cycle remains challenging, with several sponge species hosting up to 3000 distinct microbial species. Ianthella basta, an abundant broadcast spawning species in the Indo-Pacific, is an emerging model for sponge symbiosis research as it harbours only three dominant symbionts: a Thaumarchaeotum, a Gammaproteobacterium, and an Alphaproteobacterium. Here, we successfully spawned Ianthella basta, characterised its mode of reproduction, and used 16S rRNA gene amplicon sequencing, fluorescence in situ hybridisation, and transmission electron microscopy to characterise the microbial community throughout its life cycle. We confirmed I. basta as being gonochoric and showed that the three dominant symbionts, which together make up >90% of the microbiome according to 16S rRNA gene abundance, are vertically transmitted from mother to offspring by a unique method involving encapsulation in the peri-oocytic space, suggesting an obligate relationship between these microbes and their host.Peer reviewe