Adaptive prediction of environmental changes by microorganisms (original) (raw)

Nature volume 460, pages 220–224 (2009)Cite this article

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.

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Figure 2: Conditioned response in E. coli sugar metabolism.

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Figure 3: Fitness in an alternating sugar environment.

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Figure 4: Cross-protection in the context of the diauxic shift.

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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.

Author information

Author notes

  1. Orna Dahan and Yitzhak Pilpel: These authors contributed equally to this work.

Authors and Affiliations

  1. Department of Molecular Genetics, Weizmann Institute of Science Rehovot 76100, Israel
    Amir Mitchell, Bella Groisman, Avihu Yona, Orna Dahan & Yitzhak Pilpel
  2. Department of Molecular Microbiology and Biotechnology, Tel Aviv University, Tel Aviv 69978, Israel,
    Gal H. Romano & Martin Kupiec
  3. Department of Molecular Cell Biology, Weizmann Institute of Science Rehovot 76100, Israel
    Erez Dekel
  4. Department of Systems Biology, Harvard Medical School, Boston, Massachusetts 02115, USA,
    Yitzhak Pilpel

Authors

  1. Amir Mitchell
  2. Gal H. Romano
  3. Bella Groisman
  4. Avihu Yona
  5. Erez Dekel
  6. Martin Kupiec
  7. Orna Dahan
  8. Yitzhak Pilpel

Corresponding author

Correspondence toYitzhak Pilpel.

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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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Editorial Summary

Microorganism behaviour: be prepared

Microorganisms, at first glance, look to be at the mercy of their environment and any changes that might take place within it. Reacting to events as they happen would seem to be their lot. So the finding that both bacteria and yeast, in environments where a sequence of changes follows a repeated pattern, can associate a stimulus with an appropriate response to a future environment comes as something of a surprise. In a process that resembles Pavlovian conditioning in some ways — but depends on regulatory networks and natural selection rather than cognition — Escherichia coli passing through the gut and yeast through the various stages of fermentation 'anticipate' their next experience and assemble the metabolic pathways to cope with it. E. coli later exposed repeatedly to only the first of the series of environments even 'forget' their training and lose the conditioned response.

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