Novel Gene Clusters for Secondary Metabolite Synthesis in Mesophotic Sponge‐Associated Bacteria

ABSTRACT Mesophotic coral ecosystems (MCEs) host a diverse array of sponge species, which represent a promising source of bioactive compounds. Increasing evidence suggests that sponge‐associated bacteria may be the primary producers of these compounds. However, cultivating these bacteria under labor...

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Main Authors: Nuo Chen, Liwei Liu, Jingxuan Wang, Deqiang Mao, Hongmei Lu, Tânia Keiko Shishido, Shuai Zhi, Hua Chen, Shan He
Format: Article
Language:English
Published: Wiley 2025-02-01
Series:Microbial Biotechnology
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Online Access:https://doi.org/10.1111/1751-7915.70107
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author Nuo Chen
Liwei Liu
Jingxuan Wang
Deqiang Mao
Hongmei Lu
Tânia Keiko Shishido
Shuai Zhi
Hua Chen
Shan He
author_facet Nuo Chen
Liwei Liu
Jingxuan Wang
Deqiang Mao
Hongmei Lu
Tânia Keiko Shishido
Shuai Zhi
Hua Chen
Shan He
author_sort Nuo Chen
collection DOAJ
description ABSTRACT Mesophotic coral ecosystems (MCEs) host a diverse array of sponge species, which represent a promising source of bioactive compounds. Increasing evidence suggests that sponge‐associated bacteria may be the primary producers of these compounds. However, cultivating these bacteria under laboratory conditions remains a significant challenge. To investigate the rich resource of bioactive compounds synthesised by mesophotic sponge‐associated bacteria, we retrieved 429 metagenome‐assembled genomes (MAGs) from 15 mesophotic sponges, revealing a strong correlation between bacterial diversity and sponge species. Furthermore, we identified 1637 secondary metabolite biosynthetic gene clusters (BGCs) within these MAGs. Among the identified BGCs, terpenes were the most abundant (495), followed by 369 polyketide synthases (PKSs), 293 ribosomally synthesised and post‐translationally modified peptides (RiPPs) and 135 nonribosomal peptide synthetases (NRPSs). The BGCs were classified into 1086 gene cluster families (GCFs) based on sequence similarity. Notably, only five GCFs included experimentally validated reference BGCs from the Minimum Information about a Biosynthetic Gene cluster database (MIBiG). Additionally, an unusual abundance of BGCs was detected in Entotheonella sp. (s191209.Bin93) from the Tectomicrobia phylum. In contrast, members of Proteobacteria and Acidobacteriota harboured fewer BGCs (6–7 on average), yet their high abundance in MCE sponges suggests a potentially rich reservoir of BGCs. Analysis of the BGC distribution patterns revealed that a subset of BGCs, including terpene GCFs (FAM_00447 and FAM_01046), PKS GCF (FAM_00235), and RiPPs GCF (FAM_01143), were widespread across mesophotic sponges. Furthermore, 32 GCFs were consistently present in the same MAGs across different sponges, highlighting their potential key biological roles and capacity to yield novel bioactive compounds. This study not only underscores the untapped potential of mesophotic sponge‐associated bacteria as a source of bioactive compounds but also provides valuable insights into the intricate interactions between sponges and their symbiotic microbial communities.
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spelling doaj-art-c77883af41424a008c12d45fc807f45f2025-08-20T03:07:17ZengWileyMicrobial Biotechnology1751-79152025-02-01182n/an/a10.1111/1751-7915.70107Novel Gene Clusters for Secondary Metabolite Synthesis in Mesophotic Sponge‐Associated BacteriaNuo Chen0Liwei Liu1Jingxuan Wang2Deqiang Mao3Hongmei Lu4Tânia Keiko Shishido5Shuai Zhi6Hua Chen7Shan He8Li Dak Sum Yip Yio Chin Kenneth Li Marine Biopharmaceutical Research Center, Health Science Center Ningbo University Ningbo Zhejiang ChinaLi Dak Sum Yip Yio Chin Kenneth Li Marine Biopharmaceutical Research Center, Health Science Center Ningbo University Ningbo Zhejiang ChinaLi Dak Sum Yip Yio Chin Kenneth Li Marine Biopharmaceutical Research Center, Health Science Center Ningbo University Ningbo Zhejiang ChinaLi Dak Sum Yip Yio Chin Kenneth Li Marine Biopharmaceutical Research Center, Health Science Center Ningbo University Ningbo Zhejiang ChinaLi Dak Sum Yip Yio Chin Kenneth Li Marine Biopharmaceutical Research Center, Health Science Center Ningbo University Ningbo Zhejiang ChinaInstitute of Biotechnology University of Helsinki Helsinki FinlandSchool of Public Health Ningbo University Ningbo Zhejiang ChinaMingke Biotechnology Co., Ltd. Hangzhou ChinaLi Dak Sum Yip Yio Chin Kenneth Li Marine Biopharmaceutical Research Center, Health Science Center Ningbo University Ningbo Zhejiang ChinaABSTRACT Mesophotic coral ecosystems (MCEs) host a diverse array of sponge species, which represent a promising source of bioactive compounds. Increasing evidence suggests that sponge‐associated bacteria may be the primary producers of these compounds. However, cultivating these bacteria under laboratory conditions remains a significant challenge. To investigate the rich resource of bioactive compounds synthesised by mesophotic sponge‐associated bacteria, we retrieved 429 metagenome‐assembled genomes (MAGs) from 15 mesophotic sponges, revealing a strong correlation between bacterial diversity and sponge species. Furthermore, we identified 1637 secondary metabolite biosynthetic gene clusters (BGCs) within these MAGs. Among the identified BGCs, terpenes were the most abundant (495), followed by 369 polyketide synthases (PKSs), 293 ribosomally synthesised and post‐translationally modified peptides (RiPPs) and 135 nonribosomal peptide synthetases (NRPSs). The BGCs were classified into 1086 gene cluster families (GCFs) based on sequence similarity. Notably, only five GCFs included experimentally validated reference BGCs from the Minimum Information about a Biosynthetic Gene cluster database (MIBiG). Additionally, an unusual abundance of BGCs was detected in Entotheonella sp. (s191209.Bin93) from the Tectomicrobia phylum. In contrast, members of Proteobacteria and Acidobacteriota harboured fewer BGCs (6–7 on average), yet their high abundance in MCE sponges suggests a potentially rich reservoir of BGCs. Analysis of the BGC distribution patterns revealed that a subset of BGCs, including terpene GCFs (FAM_00447 and FAM_01046), PKS GCF (FAM_00235), and RiPPs GCF (FAM_01143), were widespread across mesophotic sponges. Furthermore, 32 GCFs were consistently present in the same MAGs across different sponges, highlighting their potential key biological roles and capacity to yield novel bioactive compounds. This study not only underscores the untapped potential of mesophotic sponge‐associated bacteria as a source of bioactive compounds but also provides valuable insights into the intricate interactions between sponges and their symbiotic microbial communities.https://doi.org/10.1111/1751-7915.70107biosynthetic gene clustermesophotic coral ecosystemmetagenome‐assembled genomesecondary metabolitesponge
spellingShingle Nuo Chen
Liwei Liu
Jingxuan Wang
Deqiang Mao
Hongmei Lu
Tânia Keiko Shishido
Shuai Zhi
Hua Chen
Shan He
Novel Gene Clusters for Secondary Metabolite Synthesis in Mesophotic Sponge‐Associated Bacteria
Microbial Biotechnology
biosynthetic gene cluster
mesophotic coral ecosystem
metagenome‐assembled genome
secondary metabolite
sponge
title Novel Gene Clusters for Secondary Metabolite Synthesis in Mesophotic Sponge‐Associated Bacteria
title_full Novel Gene Clusters for Secondary Metabolite Synthesis in Mesophotic Sponge‐Associated Bacteria
title_fullStr Novel Gene Clusters for Secondary Metabolite Synthesis in Mesophotic Sponge‐Associated Bacteria
title_full_unstemmed Novel Gene Clusters for Secondary Metabolite Synthesis in Mesophotic Sponge‐Associated Bacteria
title_short Novel Gene Clusters for Secondary Metabolite Synthesis in Mesophotic Sponge‐Associated Bacteria
title_sort novel gene clusters for secondary metabolite synthesis in mesophotic sponge associated bacteria
topic biosynthetic gene cluster
mesophotic coral ecosystem
metagenome‐assembled genome
secondary metabolite
sponge
url https://doi.org/10.1111/1751-7915.70107
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