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Identification of a deep-branching thermophilic clade sheds light on early bacterial evolution

Author

Listed:
  • Hao Leng

    (Shanghai Jiao Tong University
    Shanghai Jiao Tong University)

  • Yinzhao Wang

    (Shanghai Jiao Tong University
    Shanghai Jiao Tong University)

  • Weishu Zhao

    (Shanghai Jiao Tong University
    Shanghai Jiao Tong University)

  • Stefan M. Sievert

    (Woods Hole Oceanographic Institution)

  • Xiang Xiao

    (Shanghai Jiao Tong University
    Shanghai Jiao Tong University
    Southern Marine Science and Engineering Guangdong Laboratory (Zhuhai))

Abstract

It has been proposed that early bacteria, or even the last universal common ancestor of all cells, were thermophilic. However, research on the origin and evolution of thermophily is hampered by the difficulties associated with the isolation of deep-branching thermophilic microorganisms in pure culture. Here, we isolate a deep-branching thermophilic bacterium from a deep-sea hydrothermal vent, using a two-step cultivation strategy (“Subtraction-Suboptimal”, StS) designed to isolate rare organisms. The bacterium, which we name Zhurongbacter thermophilus 3DAC, is a sulfur-reducing heterotroph that is phylogenetically related to Coprothermobacterota and other thermophilic bacterial groups, forming a clade that seems to represent a major, early-diverging bacterial lineage. The ancestor of this clade might be a thermophilic, strictly anaerobic, motile, hydrogen-dependent, and mixotrophic bacterium. Thus, our study provides insights into the early evolution of thermophilic bacteria.

Suggested Citation

  • Hao Leng & Yinzhao Wang & Weishu Zhao & Stefan M. Sievert & Xiang Xiao, 2023. "Identification of a deep-branching thermophilic clade sheds light on early bacterial evolution," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
    • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-39960-x
    DOI: 10.1038/s41467-023-39960-x
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    1. Hongjun Yu & Dominik K. Haja & Gerrit J. Schut & Chang-Hao Wu & Xing Meng & Gongpu Zhao & Huilin Li & Michael W. W. Adams, 2020. "Structure of the respiratory MBS complex reveals iron-sulfur cluster catalyzed sulfane sulfur reduction in ancient life," Nature Communications, Nature, vol. 11(1), pages 1-13, December.
    2. Joshua A. Lerman & Daniel R. Hyduke & Haythem Latif & Vasiliy A. Portnoy & Nathan E. Lewis & Jeffrey D. Orth & Alexandra C. Schrimpe-Rutledge & Richard D. Smith & Joshua N. Adkins & Karsten Zengler & , 2012. "In silico method for modelling metabolism and gene product expression at genome scale," Nature Communications, Nature, vol. 3(1), pages 1-10, January.
    3. Qiyun Zhu & Uyen Mai & Wayne Pfeiffer & Stefan Janssen & Francesco Asnicar & Jon G. Sanders & Pedro Belda-Ferre & Gabriel A. Al-Ghalith & Evguenia Kopylova & Daniel McDonald & Tomasz Kosciolek & John , 2019. "Phylogenomics of 10,575 genomes reveals evolutionary proximity between domains Bacteria and Archaea," Nature Communications, Nature, vol. 10(1), pages 1-14, December.
    4. Nicola Segata & Daniela Börnigen & Xochitl C. Morgan & Curtis Huttenhower, 2013. "PhyloPhlAn is a new method for improved phylogenetic and taxonomic placement of microbes," Nature Communications, Nature, vol. 4(1), pages 1-11, October.
    5. Anna-Louise Reysenbach & Yitai Liu & Amy B. Banta & Terry J. Beveridge & Julie D. Kirshtein & Stefan Schouten & Margaret K. Tivey & Karen L. Von Damm & Mary A. Voytek, 2006. "A ubiquitous thermoacidophilic archaeon from deep-sea hydrothermal vents," Nature, Nature, vol. 442(7101), pages 444-447, July.
    6. Christian Rinke & Patrick Schwientek & Alexander Sczyrba & Natalia N. Ivanova & Iain J. Anderson & Jan-Fang Cheng & Aaron Darling & Stephanie Malfatti & Brandon K. Swan & Esther A. Gies & Jeremy A. Do, 2013. "Insights into the phylogeny and coding potential of microbial dark matter," Nature, Nature, vol. 499(7459), pages 431-437, July.
    7. Karen E. Nelson & Rebecca A. Clayton & Steven R. Gill & Michelle L. Gwinn & Robert J. Dodson & Daniel H. Haft & Erin K. Hickey & Jeremy D. Peterson & William C. Nelson & Karen A. Ketchum & Lisa McDona, 1999. "Evidence for lateral gene transfer between Archaea and Bacteria from genome sequence of Thermotoga maritima," Nature, Nature, vol. 399(6734), pages 323-329, May.
    8. Oleg Abramov & Stephen J. Mojzsis, 2009. "Microbial habitability of the Hadean Earth during the late heavy bombardment," Nature, Nature, vol. 459(7245), pages 419-422, May.
    9. Weishu Zhao & Bozitao Zhong & Lirong Zheng & Pan Tan & Yinzhao Wang & Hao Leng & Nicolas Souza & Zhuo Liu & Liang Hong & Xiang Xiao, 2022. "Proteome-wide 3D structure prediction provides insights into the ancestral metabolism of ancient archaea and bacteria," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
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