Cited by 590Gene Regulatory Network AnalysisEvolution and Genetic DynamicsBacterial Genetics and Biotechnology

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Adaptive prediction of environmental changes by microorganisms

Mitchell, Amir, Romano, Gal H., Groisman, Bella, Yona, Avihu, Dekel, Erez, Kupiec, Martin, Dahan, Orna, Pilpel, Yitzhak·2009·Nature

DOI 10.1038/nature08112

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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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Additional file 5 of Natural variation in yeast reveals multiple paths for acquiring higher stress resistance
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Additional file 2 of Natural variation in yeast reveals multiple paths for acquiring higher stress resistance
Scholes, A. N., Stuecker, T. N., Hood, S. E., Locke, C. J., Stacy, C. L., Zhang, Q., & Lewis, J. A. (2024) · Figshare · doi:10.6084/m9.figshare.26182341
Additional file 10 of Natural variation in yeast reveals multiple paths for acquiring higher stress resistance
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Additional file 1 of Natural variation in yeast reveals multiple paths for acquiring higher stress resistance
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Additional file 7 of Natural variation in yeast reveals multiple paths for acquiring higher stress resistance
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Additional file 8 of Natural variation in yeast reveals multiple paths for acquiring higher stress resistance
Scholes, A. N., Stuecker, T. N., Hood, S. E., Locke, C. J., Stacy, C. L., Zhang, Q., & Lewis, J. A. (2024) · Figshare · doi:10.6084/m9.figshare.26743424
Additional file 4 of Natural variation in yeast reveals multiple paths for acquiring higher stress resistance
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Additional file 6 of Natural variation in yeast reveals multiple paths for acquiring higher stress resistance
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Additional file 9 of Natural variation in yeast reveals multiple paths for acquiring higher stress resistance
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Additional file 3 of Natural variation in yeast reveals multiple paths for acquiring higher stress resistance
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Additional file 11 of Natural variation in yeast reveals multiple paths for acquiring higher stress resistance
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Authors: Mitchell, A., Romano, G. H., Groisman, B., Yona, A., Dekel, E., Kupiec, M., Dahan, O., & Pilpel, Y.
Affiliations: Weizmann Institute of Science (IL)
Tel Aviv University (IL)
Harvard University (US)
Corresponding author: Pilpel, Yitzhak
ORCID: Mitchell, Amir
Yona, Avihu
Kupiec, Martin
Dahan, Orna
Pilpel, Yitzhak
Venue: Nature
Publisher: Springer Science and Business Media LLC
Published: 2009-06-17
Volume: 460
Issue: 7252
Pages: 220-224
ISSN: 0028-0836 (ISSN-L)
1476-4687
DOI: 10.1038/nature08112
OpenAlex: W2165081628
Cited by: 581
References: 28
Citations by year: 2026: 26 · 2025: 28 · 2024: 31 · 2023: 47 · 2022: 38 · 2021: 32 · 2020: 40 · 2019: 35 · 2018: 57 · 2017: 37 · 2016: 30 · 2015: 30 · 2014: 27 · 2013: 30 · 2012: 30
FWCI: 12.38
Type: journal article
Language: en
Open access: closed
Licence: www.springer.com/tdm (tdm)
Locations: Nature (publishedVersion)
PubMed (publishedVersion)
RePEc: Research Papers in Economics (submittedVersion)
Funders: European Science Foundation
Israel Science Foundation
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gene Regulatory Network Analysis
Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Evolution and Genetic Dynamics
Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Bacterial Genetics and Biotechnology
Keywords: classical conditioning, Escherichia coli, Saccharomyces cerevisiae, gene expression regulation, regulatory networks, adaptive evolution, conditioned response, memory loss, fitness, gut microbiota, yeast fermentation
MeSH terms: Adaptation, Physiological, Carbon, Environment, Escherichia coli, Biological Evolution, Fermentation, Gene Expression Regulation, Lactose, Maltose, Osmotic Pressure, Saccharomyces cerevisiae, Time Factors, Oxidative Stress, Heat-Shock Response, Cell Respiration, Genomics, Carbohydrate Metabolism

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