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Ecological selection for small microbial genomes along a temperate-to-thermal soil gradient

Abstract

Small bacterial and archaeal genomes provide insights into the minimal requirements for life1 and are phylogenetically widespread2. However, the precise environmental pressures that constrain genome size in free-living microorganisms are unknown. A study including isolates has shown that thermophiles and other bacteria with high optimum growth temperatures often have small genomes3. It is unclear whether this relationship extends generally to microorganisms in nature4,5 and more specifically to microorganisms that inhabit complex and highly variable environments, such as soils3,6,7. To understand the genomic traits of thermally adapted microorganisms, here we investigated metagenomes from a 45 °C gradient of temperate-to-thermal soils that lie over the ongoing Centralia, Pennsylvania (USA) coal-seam fire. We found that hot soils harboured distinct communities with small genomes and small cell sizes relative to those in ambient soils. Hot soils notably lacked genes that encode known two-component regulatory systems, and antimicrobial production and resistance genes. Our results provide field evidence for the inverse relationship between microbial genome size and temperature in a diverse, free-living community over a wide range of temperatures that support microbial life.

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Fig. 1: Changes in average genome and cell sizes across the soil temperature gradient in Centralia.
Fig. 2: Comparison of Centralia genome sizes to other soils.
Fig. 3: Temperature distribution and diversity of Centralia MAGs compared to reference soil genomes from IMG and RefSoil.
Fig. 4: KEGG modules correlated with temperature.

Data availability

Metagenome data are available on IMG under the GOLD Study ID GS0114513. MG-RAST data are available under Project IDs mgp3731, mgp252, mgp5588, mgp14596, mgp6377, mgp6368, mgp2592, mgp2076, mgp11628, mgp13948, mgp7176 and mgp15600.

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Acknowledgements

This research was supported by Michigan State University and the National Science Foundation grant no. DEB1749544. Computational resources were provided by the Michigan State Institute for Cyber-Enabled Research. Metagenome sequencing was supported by the Joint Genome Institute Community Science Project no. 1834. The work conducted by the US Department of Energy Joint Genome Institute, a DOE Office of Science User Facility, is supported under Contract no. DE-AC02-05CH11231. We thank K. L. Grady and S. -H. Lee for technical support and S. Yeh and J. Lee (REU-ACRES NSF grant no. 1560168) for their contributions to metagenome analyses.

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Contributions

A.S. and T.C.T. conceived the study and conducted the field work. J.W.S. and T.K.D. performed analyses with A.S. J.W.S., A.S. and T.K.D. wrote the manuscript. All authors discussed results, and commented on and edited the manuscript.

Corresponding author

Correspondence to Ashley Shade.

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Supplementary information

Supplementary Information

Supplementary Results, Supplementary References, Supplementary Figures 1–3, Supplementary Table 1, Supplementary Table 3–5, Supplementary Table 7.

Reporting Summary

Supplementary Table 2

Two-sided Pearson’s correlations of Eukaryotic-specific ribosomal KEGG orthologues and plasmid pfam categories with temperature (n = 12 soils). No adjustments for multiple comparisons were made.

Supplementary Table 6

Completeness, contamination, and taxonomy of MAGs.

Supplementary Table 8

Significant two-sided Pearson’s correlations (false-discovery-rate-adjusted P value.

Supplementary Table 9

Permanent finished genomes per phylum in the integrated microbial genomes database used in Supplementary Fig. 2.

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Sorensen, J.W., Dunivin, T.K., Tobin, T.C. et al. Ecological selection for small microbial genomes along a temperate-to-thermal soil gradient. Nat Microbiol 4, 55–61 (2019). https://doi.org/10.1038/s41564-018-0276-6

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