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

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Nature Microbiology


Small bacterial and archaeal genomes provide insights into the minimal requirements for life(1) and are phylogenetically widespread(2). 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 genomes(3). It is unclear whether this relationship extends generally to microorganisms in nature(4,5) and more specifically to microorganisms that inhabit complex and highly variable environments, such as soils(3,6,7). 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. (1.) Hutchison, C. A. et al. Design and synthesis of a minimal bacterial genome. Science 351, aad6253 (2016). (2.) Hug, L. A. et al. A new view of the tree of life. Nat. Microbiol. 1, 16048 (2016). (3.) Sabath, N., Ferrada, E., Barve, A. & Wagner, A. Growth temperature and genome size in bacteria are negatively correlated, suggesting genomic streamlining during thermal adaptation. Genome Biol. Evol. 5, 966–977 (2013). (4.) Huete-Stauffer, T. M., Arandia-Gorostidi, N., Alonso-Sáez, L. & Morán, X. A. G. Experimental warming decreases the average size and nucleic acid content of marine bacterial communities. Front. Microbiol. 7, 730 (2016). (5.) Swan, B. K. et al. Prevalent genome streamlining and latitudinal divergence of planktonic bacteria in the surface ocean. Proc. Natl Acad. Sci. USA 110, 11463–11468 (2013). (6.) Brewer, T. E., Handley, K. M., Carini, P., Gilbert, J. A. & Fierer, N. Genome reduction in an abundant and ubiquitous soil bacterium ‘Candidatus Udaeobacter copiosus’. Nat. Microbiol. 2, 16198 (2016). (7.) Giovannoni, S. J., Thrash, J. C. & Temperton, B. Implications of streamlining theory for microbial ecology. ISME J. 8, 1553–1565 (2014).


This version of the article has been accepted for publication, after peer review (when applicable) and is subject to Springer Nature’s AM terms of use, but is not the Version of Record and does not reflect post-acceptance improvements, or any corrections. The Version of Record is available online at: http://dx.doi.org/10.1038/s41564-018-0276-6.