Genome-centric view of the microbiome in a new deep-sea glass sponge species Bathydorus sp.
Sponges are widely distributed in the global ocean and harbor diverse symbiotic microbes with mutualistic relationships. However, sponge symbionts in the deep sea remain poorly studied at the genome level. Here, we report a new glass sponge species of the genus Bathydorus and provide a genome-centri...
| Main Authors: | , , , , , , , |
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| Format: | Article |
| Language: | English |
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Frontiers Media S.A.
2023-02-01
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| Series: | Frontiers in Microbiology |
| Subjects: | |
| Online Access: | https://www.frontiersin.org/articles/10.3389/fmicb.2023.1078171/full |
| _version_ | 1811169462501507072 |
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| author | Tao-Shu Wei Tao-Shu Wei Zhao-Ming Gao Lin Gong Qing-Mei Li Ying-Li Zhou Hua-Guan Chen Hua-Guan Chen Li-Sheng He Yong Wang Yong Wang |
| author_facet | Tao-Shu Wei Tao-Shu Wei Zhao-Ming Gao Lin Gong Qing-Mei Li Ying-Li Zhou Hua-Guan Chen Hua-Guan Chen Li-Sheng He Yong Wang Yong Wang |
| author_sort | Tao-Shu Wei |
| collection | DOAJ |
| description | Sponges are widely distributed in the global ocean and harbor diverse symbiotic microbes with mutualistic relationships. However, sponge symbionts in the deep sea remain poorly studied at the genome level. Here, we report a new glass sponge species of the genus Bathydorus and provide a genome-centric view of its microbiome. We obtained 14 high-quality prokaryotic metagenome-assembled genomes (MAGs) affiliated with the phyla Nitrososphaerota, Pseudomonadota, Nitrospirota, Bdellovibrionota, SAR324, Bacteroidota, and Patescibacteria. In total, 13 of these MAGs probably represent new species, suggesting the high novelty of the deep-sea glass sponge microbiome. An ammonia-oxidizing Nitrososphaerota MAG B01, which accounted for up to 70% of the metagenome reads, dominated the sponge microbiomes. The B01 genome had a highly complex CRISPR array, which likely represents an advantageous evolution toward a symbiotic lifestyle and forceful ability to defend against phages. A sulfur-oxidizing Gammaproteobacteria species was the second most dominant symbiont, and a nitrite-oxidizing Nitrospirota species could also be detected, but with lower relative abundance. Bdellovibrio species represented by two MAGs, B11 and B12, were first reported as potential predatory symbionts in deep-sea glass sponges and have undergone dramatic genome reduction. Comprehensive functional analysis indicated that most of the sponge symbionts encoded CRISPR–Cas systems and eukaryotic-like proteins for symbiotic interactions with the host. Metabolic reconstruction further illustrated their essential roles in carbon, nitrogen, and sulfur cycles. In addition, diverse putative phages were identified from the sponge metagenomes. Our study expands the knowledge of microbial diversity, evolutionary adaption, and metabolic complementarity in deep-sea glass sponges. |
| first_indexed | 2024-04-10T16:42:48Z |
| format | Article |
| id | doaj.art-f8cd4d17676e4b18a23ea4f63dea9d76 |
| institution | Directory Open Access Journal |
| issn | 1664-302X |
| language | English |
| last_indexed | 2024-04-10T16:42:48Z |
| publishDate | 2023-02-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Microbiology |
| spelling | doaj.art-f8cd4d17676e4b18a23ea4f63dea9d762023-02-08T05:59:21ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2023-02-011410.3389/fmicb.2023.10781711078171Genome-centric view of the microbiome in a new deep-sea glass sponge species Bathydorus sp.Tao-Shu Wei0Tao-Shu Wei1Zhao-Ming Gao2Lin Gong3Qing-Mei Li4Ying-Li Zhou5Hua-Guan Chen6Hua-Guan Chen7Li-Sheng He8Yong Wang9Yong Wang10Institute of Deep-Sea Science and Engineering, Chinese Academy of Sciences, Sanya, Hainan, ChinaUniversity of Chinese Academy of Sciences, Beijing, ChinaInstitute of Deep-Sea Science and Engineering, Chinese Academy of Sciences, Sanya, Hainan, ChinaInstitute of Oceanology, Chinese Academy of Sciences, Qingdao, Shandong, ChinaInstitute of Deep-Sea Science and Engineering, Chinese Academy of Sciences, Sanya, Hainan, ChinaInstitute of Deep-Sea Science and Engineering, Chinese Academy of Sciences, Sanya, Hainan, ChinaInstitute of Deep-Sea Science and Engineering, Chinese Academy of Sciences, Sanya, Hainan, ChinaUniversity of Chinese Academy of Sciences, Beijing, ChinaInstitute of Deep-Sea Science and Engineering, Chinese Academy of Sciences, Sanya, Hainan, ChinaInstitute of Deep-Sea Science and Engineering, Chinese Academy of Sciences, Sanya, Hainan, ChinaInstitute for Ocean Engineering, Shenzhen International Graduate School, Tsinghua University, Shenzhen, ChinaSponges are widely distributed in the global ocean and harbor diverse symbiotic microbes with mutualistic relationships. However, sponge symbionts in the deep sea remain poorly studied at the genome level. Here, we report a new glass sponge species of the genus Bathydorus and provide a genome-centric view of its microbiome. We obtained 14 high-quality prokaryotic metagenome-assembled genomes (MAGs) affiliated with the phyla Nitrososphaerota, Pseudomonadota, Nitrospirota, Bdellovibrionota, SAR324, Bacteroidota, and Patescibacteria. In total, 13 of these MAGs probably represent new species, suggesting the high novelty of the deep-sea glass sponge microbiome. An ammonia-oxidizing Nitrososphaerota MAG B01, which accounted for up to 70% of the metagenome reads, dominated the sponge microbiomes. The B01 genome had a highly complex CRISPR array, which likely represents an advantageous evolution toward a symbiotic lifestyle and forceful ability to defend against phages. A sulfur-oxidizing Gammaproteobacteria species was the second most dominant symbiont, and a nitrite-oxidizing Nitrospirota species could also be detected, but with lower relative abundance. Bdellovibrio species represented by two MAGs, B11 and B12, were first reported as potential predatory symbionts in deep-sea glass sponges and have undergone dramatic genome reduction. Comprehensive functional analysis indicated that most of the sponge symbionts encoded CRISPR–Cas systems and eukaryotic-like proteins for symbiotic interactions with the host. Metabolic reconstruction further illustrated their essential roles in carbon, nitrogen, and sulfur cycles. In addition, diverse putative phages were identified from the sponge metagenomes. Our study expands the knowledge of microbial diversity, evolutionary adaption, and metabolic complementarity in deep-sea glass sponges.https://www.frontiersin.org/articles/10.3389/fmicb.2023.1078171/fullammonia-oxidizing archaeasymbiont Bdellovibriothe South China SeaCRISPRphage |
| spellingShingle | Tao-Shu Wei Tao-Shu Wei Zhao-Ming Gao Lin Gong Qing-Mei Li Ying-Li Zhou Hua-Guan Chen Hua-Guan Chen Li-Sheng He Yong Wang Yong Wang Genome-centric view of the microbiome in a new deep-sea glass sponge species Bathydorus sp. Frontiers in Microbiology ammonia-oxidizing archaea symbiont Bdellovibrio the South China Sea CRISPR phage |
| title | Genome-centric view of the microbiome in a new deep-sea glass sponge species Bathydorus sp. |
| title_full | Genome-centric view of the microbiome in a new deep-sea glass sponge species Bathydorus sp. |
| title_fullStr | Genome-centric view of the microbiome in a new deep-sea glass sponge species Bathydorus sp. |
| title_full_unstemmed | Genome-centric view of the microbiome in a new deep-sea glass sponge species Bathydorus sp. |
| title_short | Genome-centric view of the microbiome in a new deep-sea glass sponge species Bathydorus sp. |
| title_sort | genome centric view of the microbiome in a new deep sea glass sponge species bathydorus sp |
| topic | ammonia-oxidizing archaea symbiont Bdellovibrio the South China Sea CRISPR phage |
| url | https://www.frontiersin.org/articles/10.3389/fmicb.2023.1078171/full |
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