Metabolomics of reef benthic interactions reveals a bioactive lipid involved in coral defence

Quinn, Robert A.; Vermeij, Mark J. A.; Hartmann, Aaron C.; d'Auriac, Ines Galtier; Benler, Sean; Haas, Andreas F.; Quistad, Steven D.; Lim, Yan Wei; Little, Mark; Sandin, Stuart A.; Smith, Jennifer E.; Dorrestein, Pieter C.; Rohwer, Forest

doi:10.1098/rspb.2016.0469

Cited by 64 publications

(79 citation statements)

References 60 publications

(92 reference statements)

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“…However, ARA are used in a myriad of physiological processes, and its derivatives such as platelet activating factors, are also known to be involved in tissue growth and coral competition (e.g. [50,51]). More detailed microbial and metabolomic studies are needed to pinpoint the source of any increased levels of ARA in the host anemones in the presence of clownfish.…”

Section: Resultsmentioning

confidence: 99%

Host identity and symbiotic association affects the taxonomic and functional diversity of the clownfish-hosting sea anemone microbiome

et al. 2020

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All eukaryotic life engages in symbioses with a diverse community of bacteria that are essential for performing basic life functions. In many cases, eukaryotic organisms form additional symbioses with other macroscopic eukaryotes. The tightly linked physical interactions that characterize many macroscopic symbioses create opportunities for microbial transfer, which likely affects the diversity and function of individual microbiomes, and may ultimately lead to microbiome convergence between distantly related taxa. Here, we sequence the microbiomes of five species of clownfish-hosting sea anemones that co-occur on coral reefs in the Maldives. We test the importance of evolutionary history, clownfish symbiont association, and habitat on the taxonomic and predicted functional diversity of the microbiome, and explore signals of microbiome convergence in anemone taxa that have evolved symbioses with clownfishes independently. Our data indicate that host identity and clownfish association shapes the majority of the taxonomic diversity of the clownfish-hosting sea anemone microbiome, and predicted functional microbial diversity analyses demonstrate a convergence among host anemone microbiomes, which reflect increased functional diversity over individuals that do not host clownfishes. Further, we identify upregulated predicted microbial functions that are likely affected by clownfish presence. Taken together our study potentially reveals an even deeper metabolic coupling between clownfishes and their host anemones, and what could be a previously unknown mutualistic benefit to anemones that are symbiotic with clownfishes.

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Section: Resultsmentioning

confidence: 99%

Host identity and symbiotic association affects the taxonomic and functional diversity of the clownfish-hosting sea anemone microbiome

et al. 2020

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“…Most notably, two genes associated with phospholipase A2 (phospholipase A2 AP‐PLA2‐I and phospholipase A2) were upregulated, as was calmodulin. These proteins work in concert to initiate the production of arachidonic acid, a precursor to a suite of inflammatory lipids (e.g., platelet‐activating factor; PAF) that are found across many taxa and were recently found to occur in corals (PAF and Lyso‐PAF; Galtier d’Auriac et al, ; Quinn et al, ). In addition, phosphatidylethanolamine‐binding protein 4, which inhibits tumour necrosis factor‐alpha‐induced apoptosis, was upregulated in Symb/Light relative to Symb/Dark treatments.…”

Section: Resultsmentioning

confidence: 99%

Acquisition of obligate mutualist symbionts during the larval stage is not beneficial for a coral host

et al. 2019

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Theory suggests that the direct transmission of beneficial endosymbionts (mutualists) from parents to offspring (vertical transmission) in animal hosts is advantageous and evolutionarily stable, yet many host species instead acquire their symbionts from the environment (horizontal acquisition). An outstanding question in marine biology is why some scleractinian corals do not provision their eggs and larvae with the endosymbiotic dinoflagellates that are necessary for a juvenile's ultimate survival. We tested whether the acquisition of photosynthetic endosymbionts (family Symbiodiniaceae) during the planktonic larval stage was advantageous, as is widely assumed, in the ecologically important and threatened Caribbean reef‐building coral Orbicella faveolata. Following larval acquisition, similar changes occurred in host energetic lipid use and gene expression regardless of whether their symbionts were photosynthesizing, suggesting the symbionts did not provide the energetic benefit characteristic of the mutualism in adults. Larvae that acquired photosymbionts isolated from conspecific adults on their natal reef exhibited a reduction in swimming, which may interfere with their ability to find suitable settlement substrate, and also a decrease in survival. Larvae exposed to two cultured algal species did not exhibit differences in survival, but decreased their swimming activity in response to one species. We conclude that acquiring photosymbionts during the larval stage confers no advantages and can in fact be disadvantageous to this coral host. The timing of symbiont acquisition appears to be a critical component of a host's life history strategy and overall reproductive fitness, and this timing itself appears to be under selective pressure.

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“…Changes in the presence or concentration of metabolites have been shown to provide new insight into the physiological processes activated in response to external stimuli, e.g. temperature, pH (Sogin et al, 2016;Hillyer et al, 2017aHillyer et al, , 2018 and the presence of competitors (Quinn et al, 2016) of reefbuilding corals. Some specific metabolites or targeted metabolite groups have also been assessed in corals during photoacclimation periods (e.g.…”

Section: Introductionmentioning

confidence: 99%

Resolving coral photoacclimation dynamics through coupled photophysiological and metabolomic profiling

Lohr

Camp

Kuzhiumparambil

et al. 2019

Journal of Experimental Biology

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Corals continuously adjust to short-term variation in light availability on shallow reefs. Long-term light alterations can also occur as a result of natural and anthropogenic stressors, as well as management interventions such as coral transplantation. Although short-term photophysiological responses are relatively well understood in corals, little information is available regarding photoacclimation dynamics over weeks of altered light availability. We coupled photophysiology and metabolomic profiling to explore changes that accompany longer-term photoacclimation in a key Great Barrier Reef coral species, Acropora muricata. High light (HL)-and low light (LL)acclimated corals were collected from the reef and reciprocally exposed to high and low light ex situ. Rapid light curves using pulseamplitude modulation (PAM) fluorometry revealed photophysiological acclimation of LL corals to HL and HL corals to LL within 21 days. A subset of colonies sampled at 7 and 21 days for untargeted LC-MS and GC-MS metabolomic profiling revealed metabolic reorganization before acclimation was detected using PAM fluorometry. Metabolomic shifts were more pronounced for LL to HL corals than for their HL to LL counterparts. Compounds driving metabolomic separation between HL-exposed and LL control colonies included amino acids, organic acids, fatty acids and sterols. Reduced glycerol and campesterol suggest decreased translocation of photosynthetic products from symbiont to host in LL to HL corals, with concurrent increases in fatty acid abundance indicating reliance on stored lipids for energy. We discuss how these data provide novel insight into environmental regulation of metabolism and implications for management strategies that drive rapid changes in light availability.

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Metabolomics of reef benthic interactions reveals a bioactive lipid involved in coral defence

Cited by 64 publications

References 60 publications

Host identity and symbiotic association affects the taxonomic and functional diversity of the clownfish-hosting sea anemone microbiome

Host identity and symbiotic association affects the taxonomic and functional diversity of the clownfish-hosting sea anemone microbiome

Acquisition of obligate mutualist symbionts during the larval stage is not beneficial for a coral host

Resolving coral photoacclimation dynamics through coupled photophysiological and metabolomic profiling

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