Increased biofilm formation due to high-temperature adaptation in marine Roseobacter

Abstract

Ocean temperatures will increase significantly over the next 100 years due to global climate change1. As temperatures increase beyond current ranges, it is unclear how adaptation will impact the distribution and ecological role of marine microorganisms2. To address this major unknown, we imposed a stressful high-temperature regime for 500 generations on a strain from the abundant marine Roseobacter clade. High-temperature-adapted isolates significantly improved their fitness but also increased biofilm formation at the air–liquid interface. Furthermore, this altered lifestyle was coupled with genomic changes linked to biofilm formation in individual isolates, and was also dominant in evolved populations. We hypothesize that the increasing biofilm formation was driven by lower oxygen availability at elevated temperature, and we observe a relative fitness increase at lower oxygen. The response is uniquely different from that of Escherichia coli adapted to high temperature3 (only 3% of mutated genes were shared in both studies). Thus, future increased temperatures could have a direct effect on organismal physiology and an indirect effect via a decrease in ocean oxygen solubility, leading to an alteration in microbial lifestyle.

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Fig. 1: Increased fitness of HTLs competed against control low temperature line 10.
Fig. 2: Changes in phenotypes due to adaptation.
Fig. 3: Mutation distribution across the genome and compared to E. coli.
Fig. 4: Genotypic associations with phenotypic variation.

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Acknowledgements

The authors thank J. Martiny and B. Gaut for helpful comments, C. Mouginot, T. Kooner and K. Linzner for laboratory assistance, and R. Belas for permission to use this strain. The authors also acknowledge the World Climate Research Programme’s Working Group on Coupled Modelling and thank the climate modelling groups listed in the Methods for creating and making available their CMIP5 model output. For CMIP, the US Department of Energy’s Program for Climate Model Diagnosis and Intercomparison leads research in partnership with the Global Organization for Earth System Science Portals. A.G.K. was supported by the National Science Foundation Graduate Research Fellowship Program (DGE-1321846) and the National Institute of Biomedical Imaging and Bioengineering, National Research Service Award EB009418 from the University of California, Irvine, Center for Complex Biological Systems. C.A.G. was supported by NASA Headquarters under the NASA Earth and Space Science Fellowship (15-EARTH15F-0335). A.C.M. was supported by the National Science Foundation (OCE-1559002 and OCE-1046297).

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A.G.K. and C.A.G. performed the experiments and analysed the data. A.G.K. and A.C.M. conceived and designed the experiments. A.G.K., C.A.G. and A.C.M. wrote the paper.

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Correspondence to Adam C. Martiny.

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Kent, A.G., Garcia, C.A. & Martiny, A.C. Increased biofilm formation due to high-temperature adaptation in marine Roseobacter. Nat Microbiol 3, 989–995 (2018). https://doi.org/10.1038/s41564-018-0213-8

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