Taxon-specific microbial growth and mortality patterns reveal distinct temporal population responses to rewetting in a California grassland soil

Abstract

Microbial activity increases after rewetting dry soil, resulting in a pulse of carbon mineralization and nutrient availability. The biogeochemical responses to wet-up are reasonably well understood and known to be microbially mediated. Yet, the population level dynamics, and the resulting changes in microbial community patterns, are not well understood as ecological phenomena. Here, we used sequencing of 16S rRNA genes coupled with heavy water (H218O) DNA quantitative stable isotope probing to estimate population-specific rates of growth and mortality in response to a simulated wet-up event in a California annual grassland soil. Bacterial growth and mortality responded rapidly to wet-up, within 3 h, and continued throughout the 168 h incubation, with patterns of sequential growth observed at the phylum level. Of the 37 phyla detected in the prewet community, growth was found in 18 phyla while mortality was measured in 26 phyla. Rapid growth and mortality rates were measurable within 3 h of wet-up but had contrasting characteristics; growth at 3 h was dominated by select taxa within the Proteobacteria and Firmicutes, whereas mortality was taxonomically widespread. Furthermore, across the community, mortality exhibited density-independence, consistent with the indiscriminate shock resulting from dry-down and wet-up, whereas growth was density-dependent, consistent with control by competition or predation. Total aggregated growth across the community was highly correlated with total soil CO2 production. Together, these results illustrate how previously “invisible” population responses can translate quantitatively to emergent observations of ecosystem-scale biogeochemistry.

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Fig. 1: Absolute population growth rates for bacteria measured with quantitative stable isotope probing (qSIP) following wet-up of a CA annual grassland soil with H218O.
Fig. 2: Absolute population mortality rates for bacteria following wet-up of dry soil.
Fig. 3: Growth and mortality richness through time.
Fig. 4: CO2 production dynamics following wet-up.
Fig. 5: Relationship between per capita growth and mortality rates and population density following wet-up.

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Acknowledgements

SJB and this experiment were supported by a National Science Foundation Graduate Research Fellowship and a National Science Foundation Doctoral Dissertation Improvement Grant No. DEB-1011093 to UCB. Additional support for analyses and data integration was provided by the US Department of Energy, Office of Biological and Environmental Research, Genomic Science Program LLNL “Microbes Persist” Scientific Focus Area (award #SCW1632), and award #DE DE-SC0016207 at Northern Arizona University. Work conducted at LLNL was contributed under the auspices of the US Department of Energy under Contract DE-AC52-07NA27344, and at the Lawrence Berkeley National Laboratory through Contract No. DE-AC02-05CH11231.

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Blazewicz, S.J., Hungate, B.A., Koch, B.J. et al. Taxon-specific microbial growth and mortality patterns reveal distinct temporal population responses to rewetting in a California grassland soil. ISME J (2020). https://doi.org/10.1038/s41396-020-0617-3

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