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Author Notes:

Author for correspondence: Bruce R. Levin (Email: blevin@emory.edu)

We are grateful to Roberto Kolter and Maria Zambrano not only for their useful comments, suggestions during the early phase of this project, but also for their inspiration.

We also thank Luba Beylina, Nina Walker and Mariastella Tucker for their superb technical support, Julie Cazareth at the cell sorting facility from CNRS UMR-6097 and Grégoire Lauvau at INSERM E-344 (IPMC, Valbonne, France) for invaluable help and suggestions during the FACS experiments, Anne Doye (INSERM, U627) for excellent assistance with the confocal microscopy analysis and for preparing high-quality micrographs, Xin Wang for advice and assistance in constructing glgA and glgP deletions, Lauren Ancel, Mark Jensen, Mary Reynolds, Jeff Smith, Mark Tanaka and Renata Zappala for their comments and suggestions.

We are also grateful to Ivan Matic, Mary Berlyn and her colleagues at the Coli Genetic Stock Center for providing the strains of bacteria used in this investigation, and to Arthur Altenhoefer and Stéphane Méresse for constructs needed for the fluorescent proteins.

We express a particular depth of gratitude for the intellectual and practical (space and facilities) generosity of Ramón Díaz Orejas (CIB, Madrid) in whose laboratory most of the molecular genetic experiments were performed.

Subjects:

Research Funding:

This research was supported by grants from the US Nation Institutes of Health, AI40662, GM33782 (B.R.L.), GM59969 (T.R.), CO3/14 of the Spanish Fondo de Investigaciones Sanitarias and SAF-2002-04649, BFU2005-03911/BMC (R. D. O.), BFU2004-00879 (J.B.) of the Spanish Ministerio de Educación y Ciencia, and a grant from the European Union (QLK2-CT-2001-873, and BIO2005-04278 and LSHM-CT-2005-518152 (F.B.)).

M.L. was supported by a postdoctoral fellowship from La Ligue Nationale Contre le Cancer.

M.R.B. was in part supported by the Alfonso X el Sabio University in Madrid.

Keywords:

  • Escherichia coli
  • allelopathy
  • parallel evolution
  • glycogen
  • population biology
  • mathematical models

The evolution of contact-dependent inhibition in non-growing populations of Escherichia coli

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Journal Title:

Proceedings of the Royal Society B: Biological Sciences

Volume:

Volume 275, Number 1630

Publisher:

, Pages 3-10

Type of Work:

Article | Post-print: After Peer Review

Abstract:

In the course of liquid culture, serial passage experiments with Escherichia coli K-12 bearing a mutator gene deletion (ΔmutS) we observed the evolution of strains that appeared to kill or inhibit the growth of the bacteria from where they were derived, their ancestors. We demonstrate that this inhibition occurs after the cells stop growing and requires physical contact between the evolved and ancestral bacteria. Thereby, it is referred to as stationary phase contact-dependent inhibition (SCDI). The evolution of this antagonistic relationship is not anticipated from existing theory and experiments of competition in mass (liquid) culture. Nevertheless, it occurred in the same way (parallel evolution) in the eight independent serial transfer cultures, through different single base substitutions in a gene in the glycogen synthesis pathway, glgC. We demonstrate that the observed mutations in glgC, which codes for ADP-glucose pyrophosphorylase, are responsible for both the ability of the evolved bacteria to inhibit or kill their ancestors and their immunity to that inhibition or killing. We present evidence that without additional evolution, mutator genes, or known mutations in glgC, other strains of E. coli K-12 are also capable of SCDI or sensitive to this inhibition. We interpret this, in part, as support for the generality of SCDI and also as suggesting that the glgC mutations responsible for the SCDI, which evolved in our experiments, may suppress the action of one or more genes responsible for the sensitivity of E. coli to SCDI. Using numerical solutions to a mathematical model and in vitro experiments, we explore the population dynamics of SCDI and postulate the conditions responsible for its evolution in mass culture. We conclude with a brief discussion of the potential ecological significance of SCDI and its possible utility for the development of antimicrobial agents, which unlike existing antibiotics, can kill or inhibit the growth of bacteria that are not growing.

Copyright information:

© 2007 The Royal Society

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