Cellular differentiation into hyphae and spores in halophilic archaea

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 () and Ping Xu ()
Additional contact information
Shu-Kun Tang: School of Life Sciences, Yunnan University
Xiao-Yang Zhi: School of Life Sciences, Yunnan University
Yao Zhang: 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 Lifeomics
Kira S. Makarova: National Library of Medicine, National Institutes of Health
Bing-Bing Liu: School of Life Sciences, Yunnan University
Guo-Song Zheng: Shanghai Normal University
Zhen-Peng Zhang: 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 Lifeomics
Hua-Jun Zheng: Chinese National Human Genome Center at Shanghai and Shanghai Institute for Biomedical and Pharmaceutical Technologies
Yuri I. Wolf: National Library of Medicine, National Institutes of Health
Yu-Rong Zhao: School of Life Sciences, Yunnan University
Song-Hao Jiang: 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 Lifeomics
Xi-Ming Chen: Chinese Academy of Sciences
En-Yuan Li: School of Life Sciences, Yunnan University
Tao Zhang: 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 Lifeomics
Pei-Ru Chen: 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 Lifeomics
Yu-Zhou Feng: School of Life Sciences, Yunnan University
Ming-Xian Xiang: School of Life Sciences, Yunnan University
Zhi-Qian Lin: School of Life Sciences, Yunnan University
Jia-Hui Shi: 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 Lifeomics
Cheng Chang: 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 Lifeomics
Xue Zhang: College of Biological and Chemical Engineering, Nanyang Institute of Technology
Rui Li: School of Life Sciences, Yunnan University
Kai Lou: Xinjiang Academy of Agricultural Science
Yun Wang: Xinjiang Academy of Agricultural Science
Lei Chang: 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 Lifeomics
Min Yin: School of Life Sciences, Yunnan University
Ling-Ling Yang: School of Life Sciences, Yunnan University
Hui-Ying Gao: 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 Lifeomics
Zhong-Kai Zhang: Yunnan Academy of Agricultural Sciences
Tian-Shen Tao: Wuhan University
Tong-Wei Guan: Xihua University
Fu-Chu He: 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 Lifeomics
Yin-Hua Lu: Shanghai Normal University
Heng-Lin Cui: Jiangsu University
Eugene V. Koonin: National Library of Medicine, National Institutes of Health
Guo-Ping Zhao: Fudan University
Ping Xu: 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 Lifeomics

Nature Communications, 2023, vol. 14, issue 1, 1-14

Abstract: 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.

Date: 2023
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DOI: 10.1038/s41467-023-37389-w

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