Cophylogeny and convergence shape holobiont evolution in sponge–microbe symbioses

Pankey, M. Sabrina; Plachetzki, David C.; Macartney, Keir J.; Gastaldi, Marianela; Slattery, Marc; Gochfeld, Deborah J.; Lesser, Michael P.

doi:10.1038/s41559-022-01712-3

Cited by 40 publications

(43 citation statements)

References 88 publications

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“…The findings of positive correlations between Endozoicomonas, host growth rate, and host disease susceptibility documented in this study complement and contextualize much of the ongoing work on the mechanisms underlying proposed coral-Endozoicomonas metabolic mutualism (39,43) and suggest that the interaction of Endozoicomonas with coral disease susceptibility deserves greater scrutiny. They also echo findings of correlations between life-history strategy and microbiome structure in other important marine invertebrates, such as that between predator defense and microbial abundance in marine sponges (44).…”

Section: Endozoicomonas May Mediate Growth-defense Tradeoffs During C...supporting

confidence: 66%

Evidence for microbially-mediated tradeoffs between growth and defense throughout coral evolution

Epstein

Brown

Akinrinade

et al. 2023

Preprint

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Evolutionary tradeoffs between life-history strategies are central to animal evolution. However, because microbes can influence aspects of host physiology, behavior, and resistance to stress or disease, changes in animal-microbial symbioses have the potential to mediate life-history tradeoffs. Scleractinian corals provide a highly biodiverse and data-rich host system to test this idea, made more relevant by increases in coral disease outbreaks as a result of anthropogenic changes to climate and reef ecosystems. Identifying factors that determine coral disease susceptibility has therefore become a focus for reef conservation efforts. Using a comparative approach, we tested if coral microbiomes correlate with disease susceptibility across 425 million years of coral evolution by combining a cross-species coral microbiome survey (the ″Global Coral Microbiome Project″) with long-term disease prevalence data at multiple sites. Interpreting these data in their phylogenetic context, we show that microbial dominance and composition predict disease susceptibility. We trace this dominance-disease association to a single putatively beneficial bacterial symbiont,Endozoicomonas, whose relative abundance in coral tissue explained 30% of variation in disease susceptibility and 60% of variation in microbiome dominance across 40 coral genera. Conversely,Endozoicomonasabundances in coral tissue strongly correlated with high growth rates. These results demonstrate that the evolution of microbial symbiosis in corals correlates with both disease prevalence and growth rate. Exploration of the mechanistic basis for these findings will be important for our understanding of how microbial symbiosis influences animal life-history tradeoffs, and in efforts to use microbes to increase coral growth or disease resistance in-situ.

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Section: Endozoicomonas May Mediate Growth-defense Tradeoffs During C...supporting

confidence: 66%

Evidence for microbially-mediated tradeoffs between growth and defense throughout coral evolution

Epstein

Brown

Akinrinade

et al. 2023

Preprint

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“…conifera and A . tubulata ; Pankey et al 2022), the morphotype used here was the tube form (Fig. 1) and will therefore be referred to here as A .…”

Section: Methodsmentioning

confidence: 99%

“…While it has recently been shown that this species represents two phenotypic morphotypes that are genetically indistinguishable (i.e., A. conifera and A. tubulata; Pankey et al 2022), the morphotype used here was the tube form (Fig. 1) and will therefore be referred to here as A. tubulata.…”

Section: Size Distribution and Reciprocal Transplant Experimentsmentioning

confidence: 99%

Production of phytodetritus by a coral reef sponge increases from shallow to mesophotic depths

Lesser

Macartney

Slattery

2023

Limnology & Oceanography

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On Caribbean coral reefs, sponges are important members of the benthic community and have an important role in consuming particulate organic matter (POM) and dissolved organic matter (DOM), with the subsequent production of detritus that is then shunted into a process now referred to as the “sponge‐loop.” An emergent species of sponge commonly found on Caribbean coral reefs, Agelas tubulata, increases in size and growth rate from shallow (< 30 m) to mesophotic depths (30–150 m) on Grand Cayman Island. A. tubulata depends largely on heterotrophy across shallow to mesophotic depths and has been shown to utilize detritus on shallow reefs. However, detritus production by A. tubulata on shallow and mesophotic coral reefs has not been previously reported. Here we show, using flow cytometry, that sponge detritus includes a previously unquantified component, phytodetritus. Sponge phytodetritus production was shown experimentally to be greater in sponges from mesophotic depths compared to sponges from shallow coral reefs. Additionally, the size range of this phytodetritus corresponds to the size range of autotrophic picoplankton, primarily prochlorophytes, known to be an important food source for filter‐feeding sponges. Given the known lability of phytodetritus, compared to other more recalcitrant components of the detrital pool, its role in the food web of mesophotic communities combined with the increased availability of live POM, may be an underappreciated component of mesophotic community carbon and nitrogen flow.

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“…LMA symbiotic state is the ancestral state among sponges, while HMA symbioses, consisting of higher specialized microbes, have evolved numerous times through the recruitment of similar assemblages. Furthermore, recent studies have found that HMA holobionts have higher endemism and metabolic dependence and encode for secondary-metabolite biosynthesis in chemical defenses [ 88 , 89 ].…”

Section: Chemical Ecology-driven Discovery Of Marine Medicinesmentioning

confidence: 99%

Impact of Marine Chemical Ecology Research on the Discovery and Development of New Pharmaceuticals

Tan

2023

Marine Drugs

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Diverse ecologically important metabolites, such as allelochemicals, infochemicals and volatile organic chemicals, are involved in marine organismal interactions. Chemically mediated interactions between intra- and interspecific organisms can have a significant impact on community organization, population structure and ecosystem functioning. Advances in analytical techniques, microscopy and genomics are providing insights on the chemistry and functional roles of the metabolites involved in such interactions. This review highlights the targeted translational value of several marine chemical ecology-driven research studies and their impact on the sustainable discovery of novel therapeutic agents. These chemical ecology-based approaches include activated defense, allelochemicals arising from organismal interactions, spatio-temporal variations of allelochemicals and phylogeny-based approaches. In addition, innovative analytical techniques used in the mapping of surface metabolites as well as in metabolite translocation within marine holobionts are summarized. Chemical information related to the maintenance of the marine symbioses and biosyntheses of specialized compounds can be harnessed for biomedical applications, particularly in microbial fermentation and compound production. Furthermore, the impact of climate change on the chemical ecology of marine organisms—especially on the production, functionality and perception of allelochemicals—and its implications on drug discovery efforts will be presented.

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Cophylogeny and convergence shape holobiont evolution in sponge–microbe symbioses

Cited by 40 publications

References 88 publications

Evidence for microbially-mediated tradeoffs between growth and defense throughout coral evolution

Evidence for microbially-mediated tradeoffs between growth and defense throughout coral evolution

Production of phytodetritus by a coral reef sponge increases from shallow to mesophotic depths

Impact of Marine Chemical Ecology Research on the Discovery and Development of New Pharmaceuticals

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