Metagenomic insights and biosynthetic potential of Candidatus Entotheonella symbiont associated with Halichondria marine sponges
ABSTRACT Korea, being surrounded by the sea, provides a rich habitat for marine sponges, which have been a prolific source of bioactive natural products. Although a diverse array of structurally novel natural products has been isolated from Korean marine sponges, their biosynthetic origins remain la...
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| Language: | English |
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American Society for Microbiology
2025-01-01
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| Series: | Microbiology Spectrum |
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| Online Access: | https://journals.asm.org/doi/10.1128/spectrum.02355-24 |
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| author | Hiyoung Kim Jiyeong Ahn Jaebum Kim Hahk-Soo Kang |
| author_facet | Hiyoung Kim Jiyeong Ahn Jaebum Kim Hahk-Soo Kang |
| author_sort | Hiyoung Kim |
| collection | DOAJ |
| description | ABSTRACT Korea, being surrounded by the sea, provides a rich habitat for marine sponges, which have been a prolific source of bioactive natural products. Although a diverse array of structurally novel natural products has been isolated from Korean marine sponges, their biosynthetic origins remain largely unknown. To explore the biosynthetic potential of Korean marine sponges, we conducted metagenomic analyses of sponges inhabiting the East Sea of Korea. This analysis revealed a symbiotic association of Candidatus Entotheonella bacteria with Halichondria sponges. Here, we report a new chemically rich Entotheonella variant, which we named Ca. Entotheonella halido. Remarkably, this symbiont makes up 69% of the microbial community in the sponge Halichondira dokdoensis. Genome-resolved metagenomics enabled us to obtain a high-quality Ca. E. halido genome, which represents the largest (12 Mb) and highest quality among previously reported Entotheonella genomes. We also identified the biosynthetic gene cluster (BGC) of the known sponge-derived Halicylindramides from the Ca. E. halido genome, enabling us to determine their biosynthetic origin. This new symbiotic association expands the host diversity and biosynthetic potential of metabolically talented bacterial genus Ca. Entotheonella symbionts.IMPORTANCEOur study reports the discovery of a new bacterial symbiont Ca. Entotheonella halido associated with the Korean marine sponge Halichondria dokdoensis. Using genome-resolved metagenomics, we recovered a high-quality Ca. E. halido MAG (Metagenome-Assembled Genome), which represents the largest and most complete Ca. Entotheonella MAG reported to date. Pangenome and BGC network analyses revealed a remarkably high BGC diversity within the Ca. Entotheonella pangenome, with almost no overlapping BGCs between different MAGs. The cryptic and genetically unique BGCs present in the Ca. Entotheonella pangenome represents a promising source of new bioactive natural products. |
| format | Article |
| id | doaj-art-8f6993d5c2404ca6b5ed1404b8588a40 |
| institution | Kabale University |
| issn | 2165-0497 |
| language | English |
| publishDate | 2025-01-01 |
| publisher | American Society for Microbiology |
| record_format | Article |
| series | Microbiology Spectrum |
| spelling | doaj-art-8f6993d5c2404ca6b5ed1404b8588a402025-01-07T14:05:19ZengAmerican Society for MicrobiologyMicrobiology Spectrum2165-04972025-01-0113110.1128/spectrum.02355-24Metagenomic insights and biosynthetic potential of Candidatus Entotheonella symbiont associated with Halichondria marine spongesHiyoung Kim0Jiyeong Ahn1Jaebum Kim2Hahk-Soo Kang3Department of Biomedical Science and Engineering, Konkuk University, Seoul, South KoreaDepartment of Biomedical Science and Engineering, Konkuk University, Seoul, South KoreaDepartment of Biomedical Science and Engineering, Konkuk University, Seoul, South KoreaDepartment of Biomedical Science and Engineering, Konkuk University, Seoul, South KoreaABSTRACT Korea, being surrounded by the sea, provides a rich habitat for marine sponges, which have been a prolific source of bioactive natural products. Although a diverse array of structurally novel natural products has been isolated from Korean marine sponges, their biosynthetic origins remain largely unknown. To explore the biosynthetic potential of Korean marine sponges, we conducted metagenomic analyses of sponges inhabiting the East Sea of Korea. This analysis revealed a symbiotic association of Candidatus Entotheonella bacteria with Halichondria sponges. Here, we report a new chemically rich Entotheonella variant, which we named Ca. Entotheonella halido. Remarkably, this symbiont makes up 69% of the microbial community in the sponge Halichondira dokdoensis. Genome-resolved metagenomics enabled us to obtain a high-quality Ca. E. halido genome, which represents the largest (12 Mb) and highest quality among previously reported Entotheonella genomes. We also identified the biosynthetic gene cluster (BGC) of the known sponge-derived Halicylindramides from the Ca. E. halido genome, enabling us to determine their biosynthetic origin. This new symbiotic association expands the host diversity and biosynthetic potential of metabolically talented bacterial genus Ca. Entotheonella symbionts.IMPORTANCEOur study reports the discovery of a new bacterial symbiont Ca. Entotheonella halido associated with the Korean marine sponge Halichondria dokdoensis. Using genome-resolved metagenomics, we recovered a high-quality Ca. E. halido MAG (Metagenome-Assembled Genome), which represents the largest and most complete Ca. Entotheonella MAG reported to date. Pangenome and BGC network analyses revealed a remarkably high BGC diversity within the Ca. Entotheonella pangenome, with almost no overlapping BGCs between different MAGs. The cryptic and genetically unique BGCs present in the Ca. Entotheonella pangenome represents a promising source of new bioactive natural products.https://journals.asm.org/doi/10.1128/spectrum.02355-24marine spongessymbiontsmetagenomicsbiosynthetic gene clusters |
| spellingShingle | Hiyoung Kim Jiyeong Ahn Jaebum Kim Hahk-Soo Kang Metagenomic insights and biosynthetic potential of Candidatus Entotheonella symbiont associated with Halichondria marine sponges Microbiology Spectrum marine sponges symbionts metagenomics biosynthetic gene clusters |
| title | Metagenomic insights and biosynthetic potential of Candidatus Entotheonella symbiont associated with Halichondria marine sponges |
| title_full | Metagenomic insights and biosynthetic potential of Candidatus Entotheonella symbiont associated with Halichondria marine sponges |
| title_fullStr | Metagenomic insights and biosynthetic potential of Candidatus Entotheonella symbiont associated with Halichondria marine sponges |
| title_full_unstemmed | Metagenomic insights and biosynthetic potential of Candidatus Entotheonella symbiont associated with Halichondria marine sponges |
| title_short | Metagenomic insights and biosynthetic potential of Candidatus Entotheonella symbiont associated with Halichondria marine sponges |
| title_sort | metagenomic insights and biosynthetic potential of candidatus entotheonella symbiont associated with halichondria marine sponges |
| topic | marine sponges symbionts metagenomics biosynthetic gene clusters |
| url | https://journals.asm.org/doi/10.1128/spectrum.02355-24 |
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