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A subset of viruses thrives following microbial resuscitation during rewetting of a seasonally dry California grassland soil

Author

Listed:
  • Alexa M. Nicolas

    (University of California Berkeley)

  • Ella T. Sieradzki

    (University of California Berkeley)

  • Jennifer Pett-Ridge

    (Physical and Life Sciences Directorate, Lawrence Livermore National Laboratory
    University of California Merced)

  • Jillian F. Banfield

    (University of California Berkeley
    University of California Berkeley
    Lawrence Berkeley National Laboratory)

  • Michiko E. Taga

    (University of California Berkeley)

  • Mary K. Firestone

    (University of California Berkeley
    Lawrence Berkeley National Laboratory)

  • Steven J. Blazewicz

    (Physical and Life Sciences Directorate, Lawrence Livermore National Laboratory)

Abstract

Viruses are abundant, ubiquitous members of soil communities that kill microbial cells, but how they respond to perturbation of soil ecosystems is essentially unknown. Here, we investigate lineage-specific virus-host dynamics in grassland soil following “wet-up”, when resident microbes are both resuscitated and lysed after a prolonged dry period. Quantitative isotope tracing, time-resolved metagenomics and viromic analyses indicate that dry soil holds a diverse but low biomass reservoir of virions, of which only a subset thrives following wet-up. Viral richness decreases by 50% within 24 h post wet-up, while viral biomass increases four-fold within one week. Though recent hypotheses suggest lysogeny predominates in soil, our evidence indicates that viruses in lytic cycles dominate the response to wet-up. We estimate that viruses drive a measurable and continuous rate of cell lysis, with up to 46% of microbial death driven by viral lysis one week following wet-up. Thus, viruses contribute to turnover of soil microbial biomass and the widely reported CO2 efflux following wet-up of seasonally dry soils.

Suggested Citation

  • Alexa M. Nicolas & Ella T. Sieradzki & Jennifer Pett-Ridge & Jillian F. Banfield & Michiko E. Taga & Mary K. Firestone & Steven J. Blazewicz, 2023. "A subset of viruses thrives following microbial resuscitation during rewetting of a seasonally dry California grassland soil," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
  • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-40835-4
    DOI: 10.1038/s41467-023-40835-4
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    References listed on IDEAS

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    1. B. Knowles & C. B. Silveira & B. A. Bailey & K. Barott & V. A. Cantu & A. G. Cobián-Güemes & F. H. Coutinho & E. A. Dinsdale & B. Felts & K. A. Furby & E. E. George & K. T. Green & G. B. Gregoracci & , 2016. "Correction: Corrigendum: Lytic to temperate switching of viral communities," Nature, Nature, vol. 539(7627), pages 123-123, November.
    2. David Burstein & Christine L. Sun & Christopher T. Brown & Itai Sharon & Karthik Anantharaman & Alexander J. Probst & Brian C. Thomas & Jillian F. Banfield, 2016. "Major bacterial lineages are essentially devoid of CRISPR-Cas viral defence systems," Nature Communications, Nature, vol. 7(1), pages 1-8, April.
    3. Peter Menzel & Kim Lee Ng & Anders Krogh, 2016. "Fast and sensitive taxonomic classification for metagenomics with Kaiju," Nature Communications, Nature, vol. 7(1), pages 1-9, September.
    4. Simon Roux & Jennifer R. Brum & Bas E. Dutilh & Shinichi Sunagawa & Melissa B. Duhaime & Alexander Loy & Bonnie T. Poulos & Natalie Solonenko & Elena Lara & Julie Poulain & Stéphane Pesant & Stefanie , 2016. "Ecogenomics and potential biogeochemical impacts of globally abundant ocean viruses," Nature, Nature, vol. 537(7622), pages 689-693, September.
    5. Estelle Couradeau & Joelle Sasse & Danielle Goudeau & Nandita Nath & Terry C. Hazen & Ben P. Bowen & Romy Chakraborty & Rex R. Malmstrom & Trent R. Northen, 2019. "Probing the active fraction of soil microbiomes using BONCAT-FACS," Nature Communications, Nature, vol. 10(1), pages 1-10, December.
    6. B. Knowles & C. B. Silveira & B. A. Bailey & K. Barott & V. A. Cantu & A. G. Cobián-Güemes & F. H. Coutinho & E. A. Dinsdale & B. Felts & K. A. Furby & E. E. George & K. T. Green & G. B. Gregoracci & , 2016. "Lytic to temperate switching of viral communities," Nature, Nature, vol. 531(7595), pages 466-470, March.
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