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Survival and rapid resuscitation permit limited productivity in desert microbial communities

Author

Listed:
  • Stefanie Imminger

    (Department of Microbiology and Ecosystem Science, University of Vienna
    Doctoral School in Microbiology and Environmental Science)

  • Dimitri V. Meier

    (Department of Microbiology and Ecosystem Science, University of Vienna
    University of Bayreuth)

  • Arno Schintlmeister

    (Department of Microbiology and Ecosystem Science, University of Vienna
    Large-Instrument Facility for Environmental and Isotope Mass Spectrometry, Centre for Microbiology and Environmental Systems Science, University of Vienna)

  • Anton Legin

    (Institute of Inorganic Chemistry, University of Vienna)

  • Jörg Schnecker

    (Department of Microbiology and Ecosystem Science, University of Vienna)

  • Andreas Richter

    (Department of Microbiology and Ecosystem Science, University of Vienna)

  • Osnat Gillor

    (Blaustein Institutes for Desert Research, Ben Gurion University of the Negev)

  • Stephanie A. Eichorst

    (Department of Microbiology and Ecosystem Science, University of Vienna)

  • Dagmar Woebken

    (Department of Microbiology and Ecosystem Science, University of Vienna)

Abstract

Microbial activity in drylands tends to be confined to rare and short periods of rain. Rapid growth should be key to the maintenance of ecosystem processes in such narrow activity windows, if desiccation and rehydration cause widespread cell death due to osmotic stress. Here, simulating rain with 2H2O followed by single-cell NanoSIMS, we show that biocrust microbial communities in the Negev Desert are characterized by limited productivity, with median replication times of 6 to 19 days and restricted number of days allowing growth. Genome-resolved metatranscriptomics reveals that nearly all microbial populations resuscitate within minutes after simulated rain, independent of taxonomy, and invest their activity into repair and energy generation. Together, our data reveal a community that makes optimal use of short activity phases by fast and universal resuscitation enabling the maintenance of key ecosystem functions. We conclude that desert biocrust communities are highly adapted to surviving rapid changes in soil moisture and solute concentrations, resulting in high persistence that balances limited productivity.

Suggested Citation

  • Stefanie Imminger & Dimitri V. Meier & Arno Schintlmeister & Anton Legin & Jörg Schnecker & Andreas Richter & Osnat Gillor & Stephanie A. Eichorst & Dagmar Woebken, 2024. "Survival and rapid resuscitation permit limited productivity in desert microbial communities," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-46920-6
    DOI: 10.1038/s41467-024-46920-6
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    References listed on IDEAS

    as
    1. Lixin Wang & Wenzhe Jiao & Natasha MacBean & Maria Cristina Rulli & Stefano Manzoni & Giulia Vico & Paolo D’Odorico, 2022. "Dryland productivity under a changing climate," Nature Climate Change, Nature, vol. 12(11), pages 981-994, November.
    2. 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.
    3. Jay T. Lennon & Frank den Hollander & Maite Wilke-Berenguer & Jochen Blath, 2021. "Principles of seed banks and the emergence of complexity from dormancy," Nature Communications, Nature, vol. 12(1), pages 1-16, December.
    4. Tami L. Swenson & Ulas Karaoz & Joel M. Swenson & Benjamin P. Bowen & Trent R. Northen, 2018. "Linking soil biology and chemistry in biological soil crust using isolate exometabolomics," Nature Communications, Nature, vol. 9(1), pages 1-10, December.
    5. Richard Baran & Eoin L. Brodie & Jazmine Mayberry-Lewis & Eric Hummel & Ulisses Nunes Da Rocha & Romy Chakraborty & Benjamin P. Bowen & Ulas Karaoz & Hinsby Cadillo-Quiroz & Ferran Garcia-Pichel & Tre, 2015. "Exometabolite niche partitioning among sympatric soil bacteria," Nature Communications, Nature, vol. 6(1), pages 1-9, November.
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