Discovery of an Antarctic Ascidian-Associated Uncultivated Verrucomicrobia with Antimelanoma Palmerolide Biosynthetic Potential

Murray, Alison E.; Lo, Chien-Chi; Daligault, Hajnalka Erzsebet; Avalon, Nicole E.; Read, Robert W.; Davenport, Karen Walston; Higham, Mary L.; Kunde, Yuliya A.; Dichosa, Armand Earl Ko; Baker, Bill J.; Chain, Patrick Sam Guy

doi:10.1128/msphere.00759-21

Discovery of an Antarctic Ascidian-Associated Uncultivated Verrucomicrobia with Antimelanoma Palmerolide Biosynthetic Potential

Journal Article · Tue Nov 30 23:00:00 EST 2021 · mSphere

DOI:https://doi.org/10.1128/msphere.00759-21· OSTI ID:1968220

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Desert Research Inst. (DRI), Reno, NV (United States)
Los Alamos National Lab. (LANL), Los Alamos, NM (United States)
Univ. of South Florida, Tampa, FL (United States)

The Antarctic marine ecosystem harbors a wealth of biological and chemical innovation that has risen in concert over millennia since the isolation of the continent and formation of the Antarctic circumpolar current. Scientific inquiry into the novelty of marine natural products produced by Antarctic benthic invertebrates led to the discovery of a bioactive macrolide, palmerolide A, that has specific activity against melanoma and holds considerable promise as an anticancer therapeutic. While this compound was isolated from the Antarctic ascidian Synoicum adareanum, its biosynthesis has since been hypothesized to be microbially mediated, given structural similarities to microbially produced hybrid nonribosomal peptide-polyketide macrolides. Here, we describe a metagenome-enabled investigation aimed at identifying the biosynthetic gene cluster (BGC) and palmerolide A-producing organism. A 74-kbp candidate BGC encoding the multimodular enzymatic machinery (hybrid type I-trans-AT polyketide synthase-nonribosomal peptide synthetase and tailoring functional domains) was identified and found to harbor key features predicted as necessary for palmerolide A biosynthesis. Surveys of ascidian microbiome samples targeting the candidate BGC revealed a high correlation between palmerolide gene targets and a single 16S rRNA gene variant (R = 0.83 to 0.99). Through repeated rounds of metagenome sequencing followed by binning contigs into metagenome-assembled genomes, we were able to retrieve a nearly complete genome (10 contigs) of the BGC-producing organism, a novel verrucomicrobium within the Opitutaceae family that we propose here as “Candidatus Synoicihabitans palmerolidicus.” The refined genome assembly harbors five highly similar BGC copies, along with structural and functional features that shed light on the host-associated nature of this unique bacterium.

View Accepted Manuscript (DOE)

Research Organization:: Los Alamos National Laboratory (LANL), Los Alamos, NM (United States)

Sponsoring Organization:: USDOE; National Institutes of Health (NIH); National Science Foundation (NSF)

Grant/Contract Number:: 89233218CNA000001

OSTI ID:: 1968220

Report Number(s):: LA-UR-23-23081

Journal Information:: mSphere, Journal Name: mSphere Journal Issue: 6 Vol. 6; ISSN 2379-5042

Publisher:: American Society for MicrobiologyCopyright Statement

Country of Publication:: United States

Language:: English

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Supplementary information provided with Murray et al.: Discovery of an Antarctic ascidian-associated uncultivated Verrucomicrobia with antimelanoma palmerolide biosynthetic potential Murray, Alison E.; Lo, Chien-Chi; Daligault, Hajnalka E. Dryad https://doi.org/10.5061/dryad.8sf7m0cpp	dataset	January 2021

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59 BASIC BIOLOGICAL SCIENCES
Antarctic
Synoicihabitans palmerolidicus
Synoicum adareanum
Verrucomicrobia
anticancer
ascidian natural product
biological sciences
biosynthetic gene cluster
microbiome metagenome
palmerolide
secondary metabolite

Discovery of an Antarctic Ascidian-Associated Uncultivated Verrucomicrobia with Antimelanoma Palmerolide Biosynthetic Potential

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