Characterization of an Orphan Type III Polyketide Synthase Conserved in Uncultivated “Entotheonella” Sponge Symbionts

Reiter, Silke; Cahn, John W.; Wiebach, Vincent; Ueoka, Ryoko; Piel, Jörn

doi:10.1002/cbic.201900352

Cited by 11 publications

(19 citation statements)

References 52 publications

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“…Based on this analysis, 1 was elucidated as an alpha‐pyrone decorated with a saturated C13‐chain (Figures 2B and S11). This compound has been previously reported as product of several bacterial type III PKSs, including BpsA and CepA [9,15] . Compound 2 shows a similar UV spectrum and HRMS/MS fragmentation patterns to those of 1 .…”

Section: Resultssupporting

confidence: 55%

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A Type III Polyketide Synthase Specific for Sporulating Negativicutes is Responsible for Alkylpyrone Biosynthesis

2022

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Genomic analyses indicate that anaerobic bacteria represent a neglected source of natural products. Whereas a limited number of polyketides have been reported from anaerobes, products of type III polyketide synthases (PKSs) have remained unknown. We found a highly conserved biosynthetic gene cluster (BGC) comprising genes putatively encoding a type III PKS and a methyltransferase in genomes of the Negativicutes, strictly anaerobic, diderm bacteria. By in vivo and in vitro expression of a type III PKS gene, dquA from the oak-associated Dendrosporobacter quercicolus in E. coli we show production of long-chain alkylpyrones. Intriguingly, this BGC is specific for sporulating Sporomusaceae but absent in related Negativicutes that do not sporulate, thus suggesting a physiological role.

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Section: Resultssupporting

confidence: 55%

“…By analogy to BpsA and CepA, DquA would produce 1 using the C14 starter fatty acyl‐CoA (myristoyl‐CoA), which is extended with two MCoAs, followed by lactonization to yield the pyrone ring [9,15] . In addition to myristoyl‐CoA, DquA is able to incorporate a range of other CoA‐activated fatty acids.…”

Section: Resultsmentioning

confidence: 99%

A Type III Polyketide Synthase Specific for Sporulating Negativicutes is Responsible for Alkylpyrone Biosynthesis

2022

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“…Biosynthesis of plant-like flavonoids like those recently characterized in Flavibacteria cheonhonense [65] seems unlikely, because key pathway enzyme phenylalanine ammonia lyase is missing [66,67]. However, type III PKS genes from the current study also matched CepAB genes from taxonomically distant sponge symbiont Entotheonella gemina (class Tectomicrobia) at 48% amino acid identity, suggesting phenolic lipids as a potential biosynthetic product [68].…”

Section: Secondary Metabolite Pathwaysmentioning

confidence: 47%

A genomic view of trophic and metabolic diversity in clade-specific Lamellodysidea sponge microbiomes

et al. 2020

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Background: Marine sponges and their microbiomes contribute significantly to carbon and nutrient cycling in global reefs, processing and remineralizing dissolved and particulate organic matter. Lamellodysidea herbacea sponges obtain additional energy from abundant photosynthetic Hormoscilla cyanobacterial symbionts, which also produce polybrominated diphenyl ethers (PBDEs) chemically similar to anthropogenic pollutants of environmental concern. Potential contributions of non-Hormoscilla bacteria to Lamellodysidea microbiome metabolism and the synthesis and degradation of additional secondary metabolites are currently unknown. Results: This study has determined relative abundance, taxonomic novelty, metabolic capacities, and secondary metabolite potential in 21 previously uncharacterized, uncultured Lamellodysidea-associated microbial populations by reconstructing near-complete metagenome-assembled genomes (MAGs) to complement 16S rRNA gene amplicon studies. Microbial community compositions aligned with sponge host subgroup phylogeny in 16 samples from four host clades collected from multiple sites in Guam over a 3-year period, including representatives of Alphaproteobacteria, Gammaproteobacteria, Oligoflexia, and Bacteroidetes as well as Cyanobacteria (Hormoscilla). Unexpectedly, microbiomes from one host clade also included Cyanobacteria from the prolific secondary metabolite-producer genus Prochloron, a common tunicate symbiont. Two novel Alphaproteobacteria MAGs encoded pathways diagnostic for methylotrophic metabolism as well as type III secretion systems, and have been provisionally assigned to a new order, designated Candidatus Methylospongiales. MAGs from other taxonomic groups encoded light-driven energy production pathways using not only chlorophyll, but also bacteriochlorophyll and proteorhodopsin. Diverse heterotrophic capabilities favoring aerobic versus anaerobic conditions included pathways for degrading chitin, eukaryotic extracellular matrix polymers, phosphonates, dimethylsulfoniopropionate, trimethylamine, and benzoate. Genetic evidence identified an aerobic catabolic pathway for halogenated aromatics that may enable endogenous PBDEs to be used as a carbon and energy source.

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Section: Secondary Metabolite Pathwaysmentioning

confidence: 47%

A genomic view of trophic and metabolic diversity in clade-specific Lamellodysidea sponge microbiomes

Podell

Blanton

Oliver

et al. 2020

Preprint

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Background: Marine sponges and their microbiomes contribute significantly to carbon and nutrient cycling in global reefs, processing and remineralizing dissolved and particulate organic matter. Lamellodysidea herbacea sponges obtain additional energy from abundant photosynthetic Hormoscilla cyanobacterial symbionts, which also produce polybrominated diphenyl ethers (PBDEs) chemically similar to anthropogenic pollutants of environmental concern. Potential contributions of non-Hormoscilla bacteria to Lamellodysidea microbiome metabolism and the synthesis and degradation of additional secondary metabolites are currently unknown.Results: This study has determined relative abundance, taxonomic novelty, metabolic capacities, and secondary metabolite potential in 21 previously uncharacterized, uncultured Lamellodysidea-associated microbial populations by reconstructing near-complete metagenome-assembled genomes (MAGs) to complement 16S rRNA gene amplicon studies. Microbial community compositions aligned with sponge host subgroup phylogeny in 16 samples from four host clades collected from multiple sites in Guam over a three year period, including representatives of Alphaproteobacteria, Gammaproteobacteria, Oligoflexia, and Bacteroidetes as well as Cyanobacteria (Hormoscilla). Unexpectedly, microbiomes from one host clade also included Cyanobacteria from the prolific secondary metabolite-producer genus Prochloron, a common tunicate symbiont. Two novel Alphaprotobacteria MAGs encoded pathways diagnostic for methylotrophic metabolism as well as Type III secretion systems, and have been provisionally assigned to a new order, designated Candidatus Methylospongiales. MAGs from other taxonomic groups encoded light-driven energy production pathways using not only chlorophyll, but also bacteriochlorophyll and proteorhodopsin. Diverse heterotrophic capabilities favoring aerobic versus anaerobic conditions included pathways for degrading chitin, eukaryotic extracellular matrix polymers, phosphonates, dimethylsulfoniopropionate, trimethylamine, and benzoate. Genetic evidence identified an aerobic catabolic pathway for halogenated aromatics that may enable endogenous PBDEs to be used as a carbon and energy source. Conclusions:The reconstruction of high quality MAGs from all microbial taxa comprising greater than 0.1% of the sponge microbiome enabled species-specific assignment of unique metabolic features that could not have been predicted from taxonomic data alone. This information will promote more representative models of marine invertebrate microbiome contributions to host bioenergetics, the identification of potential new sponge parasites and pathogens based on conserved metabolic and physiological markers, and a better understanding of biosynthetic and degradative pathways for secondary metabolites and halogenated compounds in sponge-associated microbiota.

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Characterization of an Orphan Type III Polyketide Synthase Conserved in Uncultivated “Entotheonella” Sponge Symbionts

Cited by 11 publications

References 52 publications

A Type III Polyketide Synthase Specific for Sporulating Negativicutes is Responsible for Alkylpyrone Biosynthesis

A Type III Polyketide Synthase Specific for Sporulating Negativicutes is Responsible for Alkylpyrone Biosynthesis

A genomic view of trophic and metabolic diversity in clade-specific Lamellodysidea sponge microbiomes

A genomic view of trophic and metabolic diversity in clade-specific Lamellodysidea sponge microbiomes

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