Microbiome diversity and metabolic capacity determines the trophic ecology of the holobiont in Caribbean sponges

Lesser, Michael P.; Pankey, M. Sabrina; Slattery, Marc; Macartney, Keir J.; Gochfeld, Deborah J.

doi:10.1038/s43705-022-00196-3

Cited by 17 publications

(12 citation statements)

References 86 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…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

View full text Add to dashboard Cite

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.

show abstract

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

View full text Add to dashboard Cite

show abstract

“…Sponges are sessile, filter‐feeding animals that typically harbour species‐specific, temporally stable and diverse symbiotic microbiomes (Easson & Thacker, 2014; Erwin et al., 2015; Lesser et al., 2022; Pita et al., 2013; Schmitt et al., 2012; Taylor et al., 2007; Thomas et al., 2016). Symbiont communities co‐diversify with host lineages, which often rely on symbionts for both nutrition and chemical protection against predation (Lesser & Slattery, 2013; Pankey et al., 2022; Pawlik, 2011; Slaby et al., 2017; Taylor et al., 2007).…”

Section: Introductionmentioning

confidence: 99%

“…Symbiont communities co‐diversify with host lineages, which often rely on symbionts for both nutrition and chemical protection against predation (Lesser & Slattery, 2013; Pankey et al., 2022; Pawlik, 2011; Slaby et al., 2017; Taylor et al., 2007). Together, sponges and their symbionts serve valuable ecological and biogeochemical roles in coral reef ecosystems through benthic–pelagic coupling and nutrient cycling (Freeman et al., 2020; Lesser, 2006; Lesser et al., 2018, 2022; Webster & Taylor, 2012; Wulff, 2012).…”

Section: Introductionmentioning

confidence: 99%

“…In addition, Agelas spp. Produce numerous secondary metabolites that provide defence against predators, competitors, and pathogens (Abraham et al., 2022; Assmann et al., 2000; Slattery & Lesser, 2014), the production of which is likely encoded by genes from their microbial symbionts (Lesser et al., 2022; Pankey et al., 2022; Rua et al., 2018; Thomas et al., 2010). Whereas the taxonomy of Agelas has been traditionally approached by integrating morphotypes and spicules, a comprehensive molecular analysis of Agelas is needed to resolve species boundaries within this morphologically diverse genus (Parra‐Velandia, 2011; Parra‐Velandia et al., 2014).…”

Section: Introductionmentioning

confidence: 99%

See 1 more Smart Citation

Phylosymbiosis and metabolomics resolve phenotypically plastic and cryptic sponge species in the genus Agelas across the Caribbean basin

Pankey,

Gochfeld,

Gastaldi

et al. 2024

Molecular Ecology

View full text Add to dashboard Cite

Fundamental to holobiont biology is recognising how variation in microbial composition and function relates to host phenotypic variation. Sponges often exhibit considerable phenotypic plasticity and also harbour dense microbial communities that function to protect and nourish hosts. One of the most prominent sponge genera on Caribbean coral reefs is Agelas. Using a comprehensive set of morphological (growth form, spicule), chemical and molecular data on 13 recognised species of Agelas in the Caribbean basin, we were able to define only five species (=clades) and found that many morphospecies designations were incongruent with phylogenomic and population genetic analyses. Microbial communities were also strongly differentiated between phylogenetic species, showing little evidence of cryptic divergence and relatively low correlation with morphospecies assignment. Metagenomic analyses also showed strong correspondence to phylogenetic species, and to a lesser extent, geographical and morphological characters. Surprisingly, the variation in secondary metabolites produced by sponge holobionts was explained by geography and morphospecies assignment, in addition to phylogenetic species, and covaried significantly with a subset of microbial symbionts. Spicule characteristics were highly plastic, under greater impact from geographical location than phylogeny. Our results suggest that while phenotypic plasticity is rampant in Agelas, morphological differences within phylogenetic species affect functionally important ecological traits, including the composition of the symbiotic microbial communities and metabolomic profiles.

show abstract

“…Sponges, both high and low microbial abundance symbiotic states, known as HMA and LMA phenotypes, respectively, in the sponge biology literature (Hentschel et al 2006), also consume DOM with the rates of uptake and assimilation greater in high microbial abundance sponges compared to low microbial abundance sponges (Hoer et al 2018; McMurray et al 2018). Rates of pumping, choanocyte chamber densities and POM uptake and assimilation, however, are commonly higher in low microbial abundance sponges when assessed directly or when using stable isotopic analyses (Weisz et al 2008; Maldonado et al 2012; Poppell et al 2014; McMurray et al 2018; Rix et al 2020; Macartney et al 2021 a , b , 2022; Lesser et al 2022) with some low microbial abundance sponge species apparently not utilizing DOM at all (de Goeij et al 2017; Hoer et al 2018; McMurray et al 2018). In high microbial abundance sponges the majority of DOM uptake is driven by their microbiomes as host DOM uptake is equivalent between high microbial abundance and low microbial abundance sponges (Rix et al 2020).…”

mentioning

confidence: 99%

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

Lesser

Macartney

Slattery

2023

Limnology & Oceanography

Self Cite

View full text Add to dashboard Cite

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.

show abstract

Microbiome diversity and metabolic capacity determines the trophic ecology of the holobiont in Caribbean sponges

Cited by 17 publications

References 86 publications

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

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

Phylosymbiosis and metabolomics resolve phenotypically plastic and cryptic sponge species in the genus Agelas across the Caribbean basin

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

Contact Info

Product

Resources

About