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Ecology of inorganic sulfur auxiliary metabolism in widespread bacteriophages

Author

Listed:
  • Kristopher Kieft

    (University of Wisconsin–Madison)

  • Zhichao Zhou

    (University of Wisconsin–Madison)

  • Rika E. Anderson

    (Carleton College)

  • Alison Buchan

    (University of Tennessee)

  • Barbara J. Campbell

    (Life Science Facility, Clemson University)

  • Steven J. Hallam

    (University of British Columbia
    University of British Columbia, Genome Sciences Centre
    University of British Columbia
    University of British Columbia)

  • Matthias Hess

    (University of California Davis)

  • Matthew B. Sullivan

    (The Ohio State University)

  • David A. Walsh

    (Concordia University)

  • Simon Roux

    (Lawrence Berkeley National Laboratory)

  • Karthik Anantharaman

    (University of Wisconsin–Madison)

Abstract

Microbial sulfur metabolism contributes to biogeochemical cycling on global scales. Sulfur metabolizing microbes are infected by phages that can encode auxiliary metabolic genes (AMGs) to alter sulfur metabolism within host cells but remain poorly characterized. Here we identified 191 phages derived from twelve environments that encoded 227 AMGs for oxidation of sulfur and thiosulfate (dsrA, dsrC/tusE, soxC, soxD and soxYZ). Evidence for retention of AMGs during niche-differentiation of diverse phage populations provided evidence that auxiliary metabolism imparts measurable fitness benefits to phages with ramifications for ecosystem biogeochemistry. Gene abundance and expression profiles of AMGs suggested significant contributions by phages to sulfur and thiosulfate oxidation in freshwater lakes and oceans, and a sensitive response to changing sulfur concentrations in hydrothermal environments. Overall, our study provides fundamental insights on the distribution, diversity, and ecology of phage auxiliary metabolism associated with sulfur and reinforces the necessity of incorporating viral contributions into biogeochemical configurations.

Suggested Citation

  • Kristopher Kieft & Zhichao Zhou & Rika E. Anderson & Alison Buchan & Barbara J. Campbell & Steven J. Hallam & Matthias Hess & Matthew B. Sullivan & David A. Walsh & Simon Roux & Karthik Anantharaman, 2021. "Ecology of inorganic sulfur auxiliary metabolism in widespread bacteriophages," Nature Communications, Nature, vol. 12(1), pages 1-16, December.
  • Handle: RePEc:nat:natcom:v:12:y:2021:i:1:d:10.1038_s41467-021-23698-5
    DOI: 10.1038/s41467-021-23698-5
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    1. M. C. Ramaboli & S. Ocvirk & M. Khan Mirzaei & B. L. Eberhart & M. Valdivia-Garcia & A. Metwaly & K. Neuhaus & G. Barker & J. Ru & L. T. Nesengani & D. Mahdi-Joest & A. S. Wilson & S. K. Joni & D. C. , 2024. "Diet changes due to urbanization in South Africa are linked to microbiome and metabolome signatures of Westernization and colorectal cancer," Nature Communications, Nature, vol. 15(1), pages 1-12, December.
    2. Meishun Yu & Menghui Zhang & Runying Zeng & Ruolin Cheng & Rui Zhang & Yanping Hou & Fangfang Kuang & Xuejin Feng & Xiyang Dong & Yinfang Li & Zongze Shao & Min Jin, 2024. "Diversity and potential host-interactions of viruses inhabiting deep-sea seamount sediments," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
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    5. Ming Yan & Akbar Adjie Pratama & Sripoorna Somasundaram & Zongjun Li & Yu Jiang & Matthew B. Sullivan & Zhongtang Yu, 2023. "Interrogating the viral dark matter of the rumen ecosystem with a global virome database," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    6. Liyun An & Xinwu Liu & Jianwei Wang & Jinbo Xu & Xiaoli Chen & Xiaonan Liu & Bingxin Hu & Yong Nie & Xiao-Lei Wu, 2024. "Global diversity and ecological functions of viruses inhabiting oil reservoirs," Nature Communications, Nature, vol. 15(1), pages 1-16, December.

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