Death and cannibalism in a seasonal environment facilitate bacterial coexistence

D.E. Rozen, N. Philippe, J.A.G.M. de Visser, R.E. Lenski, D. Schneider

Research output: Contribution to journalLetterAcademicpeer-review

68 Citations (Scopus)

Abstract

Bacterial populations can evolve and adapt to become diverse niche specialists, even in seemingly homogeneous environments. One source of this diversity arises from newly 'constructed' niches that result from the activities of the bacteria themselves. Ecotypes specialized to exploit these distinct niches can subsequently coexist via frequency-dependent interactions. Here, we describe a novel form of niche construction that is based upon differential death and cannibalism, and which evolved during 20 000 generations of experimental evolution in Escherichia coli in a seasonal environment with alternating growth and starvation. In one of 12 populations, two monophyletic ecotypes, S and L, evolved that stably coexist with one another. When grown and then starved in monoculture, the death rate of S exceeds that of L, whereas the reverse is observed in mixed cultures. As shown by experiments and numerical simulations, the competitive advantage of S cells is increased by extending the period of starvation, and this advantage results from their cannibalization of the debris of lysed L cells, which allows the S cells to increase both their growth rate and total cell density. At the molecular level, the polymorphism is associated with divergence in the activity of the alternative sigma factor RpoS, with S cells displaying no detectable activity, while L cells show increased activity relative to the ancestral genotype. Our results extend the repertoire of known cross-feeding mechanisms in microbes to include cannibalism during starvation, and confirm the central roles for niche construction and seasonality in the maintenance of microbial polymorphisms
Original languageEnglish
Pages (from-to)34-44
JournalEcology Letters
Volume12
Issue number1
DOIs
Publication statusPublished - 2009

Fingerprint

cannibalism
coexistence
niche
death
niches
starvation
ecotype
cells
ecotypes
polymorphism
feeding mechanism
genetic polymorphism
sigma factors
monoculture
mixed culture
seasonality
genotype
divergence
bacterium
Escherichia coli

Keywords

  • term experimental evolution
  • escherichia-coli mutants
  • general stress-response
  • stationary-phase
  • adaptive radiation
  • balanced polymorphism
  • constant environment
  • microbial microcosms
  • prolonged starvation
  • niche construction

Cite this

Rozen, D.E. ; Philippe, N. ; de Visser, J.A.G.M. ; Lenski, R.E. ; Schneider, D. / Death and cannibalism in a seasonal environment facilitate bacterial coexistence. In: Ecology Letters. 2009 ; Vol. 12, No. 1. pp. 34-44.
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Death and cannibalism in a seasonal environment facilitate bacterial coexistence. / Rozen, D.E.; Philippe, N.; de Visser, J.A.G.M.; Lenski, R.E.; Schneider, D.

In: Ecology Letters, Vol. 12, No. 1, 2009, p. 34-44.

Research output: Contribution to journalLetterAcademicpeer-review

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T1 - Death and cannibalism in a seasonal environment facilitate bacterial coexistence

AU - Rozen, D.E.

AU - Philippe, N.

AU - de Visser, J.A.G.M.

AU - Lenski, R.E.

AU - Schneider, D.

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N2 - Bacterial populations can evolve and adapt to become diverse niche specialists, even in seemingly homogeneous environments. One source of this diversity arises from newly 'constructed' niches that result from the activities of the bacteria themselves. Ecotypes specialized to exploit these distinct niches can subsequently coexist via frequency-dependent interactions. Here, we describe a novel form of niche construction that is based upon differential death and cannibalism, and which evolved during 20 000 generations of experimental evolution in Escherichia coli in a seasonal environment with alternating growth and starvation. In one of 12 populations, two monophyletic ecotypes, S and L, evolved that stably coexist with one another. When grown and then starved in monoculture, the death rate of S exceeds that of L, whereas the reverse is observed in mixed cultures. As shown by experiments and numerical simulations, the competitive advantage of S cells is increased by extending the period of starvation, and this advantage results from their cannibalization of the debris of lysed L cells, which allows the S cells to increase both their growth rate and total cell density. At the molecular level, the polymorphism is associated with divergence in the activity of the alternative sigma factor RpoS, with S cells displaying no detectable activity, while L cells show increased activity relative to the ancestral genotype. Our results extend the repertoire of known cross-feeding mechanisms in microbes to include cannibalism during starvation, and confirm the central roles for niche construction and seasonality in the maintenance of microbial polymorphisms

AB - Bacterial populations can evolve and adapt to become diverse niche specialists, even in seemingly homogeneous environments. One source of this diversity arises from newly 'constructed' niches that result from the activities of the bacteria themselves. Ecotypes specialized to exploit these distinct niches can subsequently coexist via frequency-dependent interactions. Here, we describe a novel form of niche construction that is based upon differential death and cannibalism, and which evolved during 20 000 generations of experimental evolution in Escherichia coli in a seasonal environment with alternating growth and starvation. In one of 12 populations, two monophyletic ecotypes, S and L, evolved that stably coexist with one another. When grown and then starved in monoculture, the death rate of S exceeds that of L, whereas the reverse is observed in mixed cultures. As shown by experiments and numerical simulations, the competitive advantage of S cells is increased by extending the period of starvation, and this advantage results from their cannibalization of the debris of lysed L cells, which allows the S cells to increase both their growth rate and total cell density. At the molecular level, the polymorphism is associated with divergence in the activity of the alternative sigma factor RpoS, with S cells displaying no detectable activity, while L cells show increased activity relative to the ancestral genotype. Our results extend the repertoire of known cross-feeding mechanisms in microbes to include cannibalism during starvation, and confirm the central roles for niche construction and seasonality in the maintenance of microbial polymorphisms

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