Cellular differentiation into hyphae and spores in halophilic archaea
Abstract Several groups of bacteria have complex life cycles involving cellular differentiation and multicellular structures. For example, actinobacteria of the genus Streptomyces form multicellular vegetative hyphae, aerial hyphae, and spores. However, similar life cycles have not yet been describe...
| Main Authors: | , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
Nature Portfolio
2023-04-01
|
| Series: | Nature Communications |
| Online Access: | https://doi.org/10.1038/s41467-023-37389-w |
| _version_ | 1797349835439865856 |
|---|---|
| author | Shu-Kun Tang Xiao-Yang Zhi Yao Zhang Kira S. Makarova Bing-Bing Liu Guo-Song Zheng Zhen-Peng Zhang Hua-Jun Zheng Yuri I. Wolf Yu-Rong Zhao Song-Hao Jiang Xi-Ming Chen En-Yuan Li Tao Zhang Pei-Ru Chen Yu-Zhou Feng Ming-Xian Xiang Zhi-Qian Lin Jia-Hui Shi Cheng Chang Xue Zhang Rui Li Kai Lou Yun Wang Lei Chang Min Yin Ling-Ling Yang Hui-Ying Gao Zhong-Kai Zhang Tian-Shen Tao Tong-Wei Guan Fu-Chu He Yin-Hua Lu Heng-Lin Cui Eugene V. Koonin Guo-Ping Zhao Ping Xu |
| author_facet | Shu-Kun Tang Xiao-Yang Zhi Yao Zhang Kira S. Makarova Bing-Bing Liu Guo-Song Zheng Zhen-Peng Zhang Hua-Jun Zheng Yuri I. Wolf Yu-Rong Zhao Song-Hao Jiang Xi-Ming Chen En-Yuan Li Tao Zhang Pei-Ru Chen Yu-Zhou Feng Ming-Xian Xiang Zhi-Qian Lin Jia-Hui Shi Cheng Chang Xue Zhang Rui Li Kai Lou Yun Wang Lei Chang Min Yin Ling-Ling Yang Hui-Ying Gao Zhong-Kai Zhang Tian-Shen Tao Tong-Wei Guan Fu-Chu He Yin-Hua Lu Heng-Lin Cui Eugene V. Koonin Guo-Ping Zhao Ping Xu |
| author_sort | Shu-Kun Tang |
| collection | DOAJ |
| description | Abstract Several groups of bacteria have complex life cycles involving cellular differentiation and multicellular structures. For example, actinobacteria of the genus Streptomyces form multicellular vegetative hyphae, aerial hyphae, and spores. However, similar life cycles have not yet been described for archaea. Here, we show that several haloarchaea of the family Halobacteriaceae display a life cycle resembling that of Streptomyces bacteria. Strain YIM 93972 (isolated from a salt marsh) undergoes cellular differentiation into mycelia and spores. Other closely related strains are also able to form mycelia, and comparative genomic analyses point to gene signatures (apparent gain or loss of certain genes) that are shared by members of this clade within the Halobacteriaceae. Genomic, transcriptomic and proteomic analyses of non-differentiating mutants suggest that a Cdc48-family ATPase might be involved in cellular differentiation in strain YIM 93972. Additionally, a gene encoding a putative oligopeptide transporter from YIM 93972 can restore the ability to form hyphae in a Streptomyces coelicolor mutant that carries a deletion in a homologous gene cluster (bldKA-bldKE), suggesting functional equivalence. We propose strain YIM 93972 as representative of a new species in a new genus within the family Halobacteriaceae, for which the name Actinoarchaeum halophilum gen. nov., sp. nov. is herewith proposed. Our demonstration of a complex life cycle in a group of haloarchaea adds a new dimension to our understanding of the biological diversity and environmental adaptation of archaea. |
| first_indexed | 2024-03-08T12:36:13Z |
| format | Article |
| id | doaj.art-2c52b6506bce40b197cdd804afa1f930 |
| institution | Directory Open Access Journal |
| issn | 2041-1723 |
| language | English |
| last_indexed | 2024-03-08T12:36:13Z |
| publishDate | 2023-04-01 |
| publisher | Nature Portfolio |
| record_format | Article |
| series | Nature Communications |
| spelling | doaj.art-2c52b6506bce40b197cdd804afa1f9302024-01-21T12:25:47ZengNature PortfolioNature Communications2041-17232023-04-0114111410.1038/s41467-023-37389-wCellular differentiation into hyphae and spores in halophilic archaeaShu-Kun Tang0Xiao-Yang Zhi1Yao Zhang2Kira S. Makarova3Bing-Bing Liu4Guo-Song Zheng5Zhen-Peng Zhang6Hua-Jun Zheng7Yuri I. Wolf8Yu-Rong Zhao9Song-Hao Jiang10Xi-Ming Chen11En-Yuan Li12Tao Zhang13Pei-Ru Chen14Yu-Zhou Feng15Ming-Xian Xiang16Zhi-Qian Lin17Jia-Hui Shi18Cheng Chang19Xue Zhang20Rui Li21Kai Lou22Yun Wang23Lei Chang24Min Yin25Ling-Ling Yang26Hui-Ying Gao27Zhong-Kai Zhang28Tian-Shen Tao29Tong-Wei Guan30Fu-Chu He31Yin-Hua Lu32Heng-Lin Cui33Eugene V. Koonin34Guo-Ping Zhao35Ping Xu36Yunnan Institute of Microbiology, Key Laboratory for Microbial Resources of the Ministry of Education, School of Life Sciences, Yunnan UniversityYunnan Institute of Microbiology, Key Laboratory for Microbial Resources of the Ministry of Education, School of Life Sciences, Yunnan UniversityState Key Laboratory of Proteomics, Beijing Proteome Research Center, National Center for Protein Sciences Beijing, Research Unit of Proteomics & Research and Development of New Drug，Research Unit of Proteomics Driven Cancer Precision Medicine, Chinese Academy of Medical Sciences, Institute of LifeomicsNational Center for Biotechnology Information, National Library of Medicine, National Institutes of HealthYunnan Institute of Microbiology, Key Laboratory for Microbial Resources of the Ministry of Education, School of Life Sciences, Yunnan UniversityCollege of Life Sciences, Shanghai Normal UniversityState Key Laboratory of Proteomics, Beijing Proteome Research Center, National Center for Protein Sciences Beijing, Research Unit of Proteomics & Research and Development of New Drug，Research Unit of Proteomics Driven Cancer Precision Medicine, Chinese Academy of Medical Sciences, Institute of LifeomicsShanghai-MOST Key Laboratory of Health and Disease Genomics, Chinese National Human Genome Center at Shanghai and Shanghai Institute for Biomedical and Pharmaceutical TechnologiesNational Center for Biotechnology Information, National Library of Medicine, National Institutes of HealthYunnan Institute of Microbiology, Key Laboratory for Microbial Resources of the Ministry of Education, School of Life Sciences, Yunnan UniversityState Key Laboratory of Proteomics, Beijing Proteome Research Center, National Center for Protein Sciences Beijing, Research Unit of Proteomics & Research and Development of New Drug，Research Unit of Proteomics Driven Cancer Precision Medicine, Chinese Academy of Medical Sciences, Institute of LifeomicsKey Laboratory of Desert and Desertification, Northwest Institute of Eco-Environment and Resources, Chinese Academy of SciencesYunnan Institute of Microbiology, Key Laboratory for Microbial Resources of the Ministry of Education, School of Life Sciences, Yunnan UniversityState Key Laboratory of Proteomics, Beijing Proteome Research Center, National Center for Protein Sciences Beijing, Research Unit of Proteomics & Research and Development of New Drug，Research Unit of Proteomics Driven Cancer Precision Medicine, Chinese Academy of Medical Sciences, Institute of LifeomicsState Key Laboratory of Proteomics, Beijing Proteome Research Center, National Center for Protein Sciences Beijing, Research Unit of Proteomics & Research and Development of New Drug，Research Unit of Proteomics Driven Cancer Precision Medicine, Chinese Academy of Medical Sciences, Institute of LifeomicsYunnan Institute of Microbiology, Key Laboratory for Microbial Resources of the Ministry of Education, School of Life Sciences, Yunnan UniversityYunnan Institute of Microbiology, Key Laboratory for Microbial Resources of the Ministry of Education, School of Life Sciences, Yunnan UniversityYunnan Institute of Microbiology, Key Laboratory for Microbial Resources of the Ministry of Education, School of Life Sciences, Yunnan UniversityState Key Laboratory of Proteomics, Beijing Proteome Research Center, National Center for Protein Sciences Beijing, Research Unit of Proteomics & Research and Development of New Drug，Research Unit of Proteomics Driven Cancer Precision Medicine, Chinese Academy of Medical Sciences, Institute of LifeomicsState Key Laboratory of Proteomics, Beijing Proteome Research Center, National Center for Protein Sciences Beijing, Research Unit of Proteomics & Research and Development of New Drug，Research Unit of Proteomics Driven Cancer Precision Medicine, Chinese Academy of Medical Sciences, Institute of LifeomicsHenan Key Laboratory of Industrial Microbial Resources and Fermentation Technology, College of Biological and Chemical Engineering, Nanyang Institute of TechnologyYunnan Institute of Microbiology, Key Laboratory for Microbial Resources of the Ministry of Education, School of Life Sciences, Yunnan UniversityXinjiang Institute of Microbiology, Xinjiang Academy of Agricultural ScienceXinjiang Institute of Microbiology, Xinjiang Academy of Agricultural ScienceState Key Laboratory of Proteomics, Beijing Proteome Research Center, National Center for Protein Sciences Beijing, Research Unit of Proteomics & Research and Development of New Drug，Research Unit of Proteomics Driven Cancer Precision Medicine, Chinese Academy of Medical Sciences, Institute of LifeomicsYunnan Institute of Microbiology, Key Laboratory for Microbial Resources of the Ministry of Education, School of Life Sciences, Yunnan UniversityYunnan Institute of Microbiology, Key Laboratory for Microbial Resources of the Ministry of Education, School of Life Sciences, Yunnan UniversityState Key Laboratory of Proteomics, Beijing Proteome Research Center, National Center for Protein Sciences Beijing, Research Unit of Proteomics & Research and Development of New Drug，Research Unit of Proteomics Driven Cancer Precision Medicine, Chinese Academy of Medical Sciences, Institute of LifeomicsBiotechnology and Genetic Germplasm Resources Research Institute, Yunnan Academy of Agricultural SciencesDepartment of Microbiology, Key Laboratory of Combinatorial Biosynthesis and Drug Discovery of Ministry of Education, School of Pharmaceutical Sciences, Wuhan UniversityCollege of Food and Biological Engineering, Xihua UniversityState Key Laboratory of Proteomics, Beijing Proteome Research Center, National Center for Protein Sciences Beijing, Research Unit of Proteomics & Research and Development of New Drug，Research Unit of Proteomics Driven Cancer Precision Medicine, Chinese Academy of Medical Sciences, Institute of LifeomicsCollege of Life Sciences, Shanghai Normal UniversitySchool of Food and Biological Engineering, Jiangsu UniversityNational Center for Biotechnology Information, National Library of Medicine, National Institutes of HealthKey Laboratory of Medical Molecular Virology (MOE/NHC/CAMS), School of Basic Medical Sciences and Department of Microbiology and Microbial Engineering, School of Life Sciences, Fudan UniversityState Key Laboratory of Proteomics, Beijing Proteome Research Center, National Center for Protein Sciences Beijing, Research Unit of Proteomics & Research and Development of New Drug，Research Unit of Proteomics Driven Cancer Precision Medicine, Chinese Academy of Medical Sciences, Institute of LifeomicsAbstract Several groups of bacteria have complex life cycles involving cellular differentiation and multicellular structures. For example, actinobacteria of the genus Streptomyces form multicellular vegetative hyphae, aerial hyphae, and spores. However, similar life cycles have not yet been described for archaea. Here, we show that several haloarchaea of the family Halobacteriaceae display a life cycle resembling that of Streptomyces bacteria. Strain YIM 93972 (isolated from a salt marsh) undergoes cellular differentiation into mycelia and spores. Other closely related strains are also able to form mycelia, and comparative genomic analyses point to gene signatures (apparent gain or loss of certain genes) that are shared by members of this clade within the Halobacteriaceae. Genomic, transcriptomic and proteomic analyses of non-differentiating mutants suggest that a Cdc48-family ATPase might be involved in cellular differentiation in strain YIM 93972. Additionally, a gene encoding a putative oligopeptide transporter from YIM 93972 can restore the ability to form hyphae in a Streptomyces coelicolor mutant that carries a deletion in a homologous gene cluster (bldKA-bldKE), suggesting functional equivalence. We propose strain YIM 93972 as representative of a new species in a new genus within the family Halobacteriaceae, for which the name Actinoarchaeum halophilum gen. nov., sp. nov. is herewith proposed. Our demonstration of a complex life cycle in a group of haloarchaea adds a new dimension to our understanding of the biological diversity and environmental adaptation of archaea.https://doi.org/10.1038/s41467-023-37389-w |
| spellingShingle | Shu-Kun Tang Xiao-Yang Zhi Yao Zhang Kira S. Makarova Bing-Bing Liu Guo-Song Zheng Zhen-Peng Zhang Hua-Jun Zheng Yuri I. Wolf Yu-Rong Zhao Song-Hao Jiang Xi-Ming Chen En-Yuan Li Tao Zhang Pei-Ru Chen Yu-Zhou Feng Ming-Xian Xiang Zhi-Qian Lin Jia-Hui Shi Cheng Chang Xue Zhang Rui Li Kai Lou Yun Wang Lei Chang Min Yin Ling-Ling Yang Hui-Ying Gao Zhong-Kai Zhang Tian-Shen Tao Tong-Wei Guan Fu-Chu He Yin-Hua Lu Heng-Lin Cui Eugene V. Koonin Guo-Ping Zhao Ping Xu Cellular differentiation into hyphae and spores in halophilic archaea Nature Communications |
| title | Cellular differentiation into hyphae and spores in halophilic archaea |
| title_full | Cellular differentiation into hyphae and spores in halophilic archaea |
| title_fullStr | Cellular differentiation into hyphae and spores in halophilic archaea |
| title_full_unstemmed | Cellular differentiation into hyphae and spores in halophilic archaea |
| title_short | Cellular differentiation into hyphae and spores in halophilic archaea |
| title_sort | cellular differentiation into hyphae and spores in halophilic archaea |
| url | https://doi.org/10.1038/s41467-023-37389-w |
| work_keys_str_mv | AT shukuntang cellulardifferentiationintohyphaeandsporesinhalophilicarchaea AT xiaoyangzhi cellulardifferentiationintohyphaeandsporesinhalophilicarchaea AT yaozhang cellulardifferentiationintohyphaeandsporesinhalophilicarchaea AT kirasmakarova cellulardifferentiationintohyphaeandsporesinhalophilicarchaea AT bingbingliu cellulardifferentiationintohyphaeandsporesinhalophilicarchaea AT guosongzheng cellulardifferentiationintohyphaeandsporesinhalophilicarchaea AT zhenpengzhang cellulardifferentiationintohyphaeandsporesinhalophilicarchaea AT huajunzheng cellulardifferentiationintohyphaeandsporesinhalophilicarchaea AT yuriiwolf cellulardifferentiationintohyphaeandsporesinhalophilicarchaea AT yurongzhao cellulardifferentiationintohyphaeandsporesinhalophilicarchaea AT songhaojiang cellulardifferentiationintohyphaeandsporesinhalophilicarchaea AT ximingchen cellulardifferentiationintohyphaeandsporesinhalophilicarchaea AT enyuanli cellulardifferentiationintohyphaeandsporesinhalophilicarchaea AT taozhang cellulardifferentiationintohyphaeandsporesinhalophilicarchaea AT peiruchen cellulardifferentiationintohyphaeandsporesinhalophilicarchaea AT yuzhoufeng cellulardifferentiationintohyphaeandsporesinhalophilicarchaea AT mingxianxiang cellulardifferentiationintohyphaeandsporesinhalophilicarchaea AT zhiqianlin cellulardifferentiationintohyphaeandsporesinhalophilicarchaea AT jiahuishi cellulardifferentiationintohyphaeandsporesinhalophilicarchaea AT chengchang cellulardifferentiationintohyphaeandsporesinhalophilicarchaea AT xuezhang cellulardifferentiationintohyphaeandsporesinhalophilicarchaea AT ruili cellulardifferentiationintohyphaeandsporesinhalophilicarchaea AT kailou cellulardifferentiationintohyphaeandsporesinhalophilicarchaea AT yunwang cellulardifferentiationintohyphaeandsporesinhalophilicarchaea AT leichang cellulardifferentiationintohyphaeandsporesinhalophilicarchaea AT minyin cellulardifferentiationintohyphaeandsporesinhalophilicarchaea AT linglingyang cellulardifferentiationintohyphaeandsporesinhalophilicarchaea AT huiyinggao cellulardifferentiationintohyphaeandsporesinhalophilicarchaea AT zhongkaizhang cellulardifferentiationintohyphaeandsporesinhalophilicarchaea AT tianshentao cellulardifferentiationintohyphaeandsporesinhalophilicarchaea AT tongweiguan cellulardifferentiationintohyphaeandsporesinhalophilicarchaea AT fuchuhe cellulardifferentiationintohyphaeandsporesinhalophilicarchaea AT yinhualu cellulardifferentiationintohyphaeandsporesinhalophilicarchaea AT henglincui cellulardifferentiationintohyphaeandsporesinhalophilicarchaea AT eugenevkoonin cellulardifferentiationintohyphaeandsporesinhalophilicarchaea AT guopingzhao cellulardifferentiationintohyphaeandsporesinhalophilicarchaea AT pingxu cellulardifferentiationintohyphaeandsporesinhalophilicarchaea |