Adaptive prediction of environmental changes by microorganisms

Amir Mitchell, Gal H. Romano, Bella Groisman, Avihu Yona, Erez Dekel, Martin Kupiec, Orna Dahan, Yitzhak Pilpel*

*Corresponding author for this work

Research output: Contribution to journalArticlepeer-review

414 Scopus citations

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 organisms 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 networkearly 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.

Original languageAmerican English
Pages (from-to)220-224
Number of pages5
JournalNature
Volume460
Issue number7252
DOIs
StatePublished - 9 Jul 2009
Externally publishedYes

Bibliographical note

Funding Information:
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.

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