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Soil bacteria show different tolerance ranges to an unprecedented disturbance

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Abstract

Soil microbial communities have remarkable capacities to cope with ceaseless environmental changes, but little is known about their adaptation potential when facing an unprecedented disturbance. We tested the effect of incremental dose of microwaving on soil bacteria as a model of unprecedented stress. 16S rRNA gene qPCR at both the DNA and cDNA levels was used to characterize the total (DNA) and transcriptionally active (cDNA) fractions of the bacterial community. Amplicon sequencing of 16S rRNA gene transcripts was performed to decipher tolerance ranges within the community using the concept of functional response groups (FRGs). Increasing microwaving doses resulted in 90% loss in total and transcriptionally active bacterial communities after 6.8 and 4.7 min, respectively. Four distinct FRGs with peculiar phylogenetic signatures were identified, revealing a link between taxonomy and increasing stress doses. FRG1, the most sensitive group, was dominated by Actinobacteria. FRG2 and FRG3, with intermediate tolerance, displayed prevalence of Proteobacteria, while FRG4, the most resistant group, was driven by Firmicutes. While the most sensitive FRGs showed predictable responses linked to changes in temperature and soil water content associated with microwaving, more tolerant FRG4 members exhibited a stochastic response nested within the Firmicutes phylum, potentially revealing bet-hedging strategists. The concept of FRGs based on 16S rRNA gene transcripts stood as an efficient tool for unraveling bacterial survival strategies and tolerance ranges triggered by incremental doses of an unprecedented stress, with regard to phylogeny linkages.

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Acknowledgements

The authors would like to thank Sandra Cabo-Verde for the discussions on microbial inactivation and Jan Dirk van Elsas for critical revisions of the manuscript.

Funding

This research was funded by the international project TRAINBIODIVERSE from the European Community’s Seventh Framework Program (FP7-PEOPLE-2011-ITN) under grant agreement no 289949.

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Author notes

  1. Inês Nunes

    Present address: Microbe Technology Department, Novozymes A/S, Krogshøjvej 36, 2880, Bagsværd, Denmark

  2. Stephanie Jurburg

    Present address: Wageningen University and Research, Wageningen Bioveterinary Research Institute ASG, Houtribweg 39, 8221 RA, Lelystad, Netherlands

  3. Samuel Jacquiod

    Present address: Agroécologie, UMR1347, INRA Dijon Center, Dijon, France

  4. Asker Brejnrod

    Present address: Novo Nordisk Foundation Center for Basic Metabolic Research, Section of Metabolic Genetics, Faculty of Health and Medical Sciences, University of Copenhagen, Nørre Alle 20, 2200, Copenhagen, Denmark

Authors and Affiliations

  1. Section of Microbiology, University of Copenhagen, Universitetsparken 15, 2100, Copenhagen, Denmark

    Inês Nunes, Samuel Jacquiod, Asker Brejnrod, Anders Priemé & Søren J. Sørensen

  2. Genomic Research in Ecology and Evolution in Nature (GREEN), Groningen Institute for Evolutionary Life Sciences (GELIFES), University of Groningen, Nijenborgh 7, 9747 AG, Groningen, The Netherlands

    Stephanie Jurburg & Joana Falcão Salles

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  1. Inês Nunes
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Nunes, I., Jurburg, S., Jacquiod, S. et al. Soil bacteria show different tolerance ranges to an unprecedented disturbance. Biol Fertil Soils 54, 189–202 (2018). https://doi.org/10.1007/s00374-017-1255-4

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