Evolutionary history constrains microbial traits across environmental variation

Abstract

Organisms influence ecosystems, from element cycling to disturbance regimes, to trophic interactions and to energy partitioning. Microorganisms are part of this influence, and understanding their ecology in nature requires studying the traits of these organisms quantitatively in their natural habitats—a challenging task, but one which new approaches now make possible. Here, we show that growth rate and carbon assimilation rate of soil microorganisms are influenced more by evolutionary history than by climate, even across a broad climatic gradient spanning major temperate life zones, from mixed conifer forest to high-desert grassland. Most of the explained variation (~50% to ~90%) in growth rate and carbon assimilation rate was attributable to differences among taxonomic groups, indicating a strong influence of evolutionary history, and taxonomic groupings were more predictive for organisms responding to resource addition. With added carbon and nitrogen substrates, differences among taxonomic groups explained approximately eightfold more variance in growth rate than did differences in ecosystem type. Taxon-specific growth and carbon assimilation rates were highly intercorrelated across the four ecosystems, constrained by the taxonomic identity of the organisms, such that plasticity driven by environment was limited across ecosystems varying in temperature, precipitation and dominant vegetation. Taken together, our results suggest that, similar to multicellular life, the traits of prokaryotes in their natural habitats are constrained by evolutionary history to a greater degree than environmental variation.

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Fig. 1: Schematic of the ecosystems sampled along the C. Hart Merriam elevation gradient near Flagstaff, northern AZ.

Victor O. Leshyk, Center for Ecosystem Science and Society, Northern Arizona University

Fig. 2: Variation in microbial community composition across the ecosystems studied.
Fig. 3: Variance in potential growth rate and carbon assimilation rate attributable to taxonomy and ecosystem.
Fig. 4: Example taxa representative of variation in trait values in response to substrate addition and across ecosystems.
Fig. 5: Comparison of pairwise inter-ecosystem similarity in microbial traits (correlations of taxon-specific trait values between ecosystems) and dissimilarity in environment (Gower’s distance considering elevation, precipitation and temperature).

Data availability

The data supporting this manuscript are available in the NCBI short-read archive under accession no. PRJNA521534.

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Acknowledgements

This research was supported by grants from the Department of Energy’s Biological Systems Science Division (No. DE-SC0016207), Program in Genomic Science and the National Science Foundation (Nos. DEB-1645596 and DEB-1241094). Work at Lawrence Livermore National Laboratory (LLNL) was funded by the Department of Energy through the Genome Sciences Program under contract Nos. SCW1424 and SCW1590, and performed under the auspices of LLNL under Contract No. DE-AC52-07NA27344.

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E.M.M., E.S. and B.A.H. developed the core ideas explored in this manuscript. R.L.M., M.H. and X.-J.A.L. carried out the soil manipulation and participated in sample analysis. R.L.M. and M.H. performed the sequencing and initial bioinformatics analysis. E.M.M., B.J.K. and K.A. performed the data analysis. K.H., J.P-R., S.J.B., B.A.H. and P.D. provided guidance on data analysis and interpretation. E.M.M. drafted the manuscript and all authors contributed equally to writing, editing and revision.

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Correspondence to Ember M. Morrissey.

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Morrissey, E.M., Mau, R.L., Hayer, M. et al. Evolutionary history constrains microbial traits across environmental variation. Nat Ecol Evol 3, 1064–1069 (2019). https://doi.org/10.1038/s41559-019-0918-y

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