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Adaptive prediction of environmental changes by microorganisms

Abstract

Natural habitats of some microorganisms may fluctuate erratically, whereas others, which are more predictable, offer the opportunity to prepare in advance for the next environmental change. In analogy to classical Pavlovian conditioning, microorganisms may have evolved to anticipate environmental stimuli by adapting to their temporal order of appearance. Here we present evidence for environmental change anticipation in two model microorganisms, Escherichia coli and Saccharomyces cerevisiae. We show that anticipation is an adaptive trait, because pre-exposure to the stimulus that typically appears early in the ecology improves the organism’s fitness when encountered with a second stimulus. Additionally, we observe loss of the conditioned response in E. coli strains that were repeatedly exposed in a laboratory evolution experiment only to the first stimulus. Focusing on the molecular level reveals that the natural temporal order of stimuli is embedded in the wiring of the regulatory network—early stimuli pre-induce genes that would be needed for later ones, yet later stimuli only induce genes needed to cope with them. Our work indicates that environmental anticipation is an adaptive trait that was repeatedly selected for during evolution and thus may be ubiquitous in biology.

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Figure 1: Four possible regulation strategies in response to environmental stimuli.
Figure 2: Conditioned response in E. coli sugar metabolism.
Figure 3: Fitness in an alternating sugar environment.
Figure 4: Cross-protection in the context of the diauxic shift.
Figure 5: Candidate genes underlying the asymmetrical protection between heat and oxidative stresses.

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Acknowledgements

We thank S. Trattner–Frenkel and Z. Bloom for their help and support in the yeast microarray experiments. We thank members of the Pilpel laboratory for many discussions. We thank E. Schneidman, E. Ben-Jacob, M. Springer, A. Tanay, U. Alon and D. Cavalieri for discussions and advice. We thank U. Alon for providing the promoter–GFP fused plasmids. We thank the Tauber Foundation, the Minerva Foundation, the Israel Science Foundation ‘Bikura program’, the European Research Council ‘Ideas Program’ and the Ben May Foundation for grant support. M.K. was supported from grants from the Israel Science Foundation and the Israeli Ministry of Science and Technology.

Author Contributions A.M. raised the original idea and performed all the experiments; G.R., B.G. and A.Y. participated in experiments; E.D. evolved the E. coli strain; A.M., O.D. and Y.P. designed the experiments; A.M., M.K., O.D. and Y.P. analysed the data; O.D. and Y.P. supervised the project; A.M., O.D. and Y.P. interpreted the results and wrote the manuscript.

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Correspondence to Yitzhak Pilpel.

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This file contains Supplementary Methods, Supplementary Tables 1-5, Supplementary Equation1, Supplementary Figures 1-8 with Legends, Supplementary Notes and Supplementary References. (PDF 324 kb)

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Mitchell, A., Romano, G., Groisman, B. et al. Adaptive prediction of environmental changes by microorganisms. Nature 460, 220–224 (2009). https://doi.org/10.1038/nature08112

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