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Coexistence of evolving bacteria stabilized by a shared Black Queen function.

J Jeffrey Morris1, Spiridon E Papoulis, Richard E Lenski

  • 1Department of Microbiology and Molecular Genetics, Michigan State University, East Lansing, Michigan, 48824; BEACON Center for the Study of Evolution in Action, Michigan State University, East Lansing, Michigan, 48824. jmorris@msu.edu.

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The Black Queen Hypothesis explains how losing functions can create cooperation. Experiments show that splitting hydrogen peroxide detoxification allows similar bacteria to coexist stably.

Keywords:
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Area of Science:

  • Evolutionary biology
  • Microbial ecology
  • Biochemistry

Background:

  • The Black Queen Hypothesis (BQH) posits that the loss of leaky functions can drive cooperation.
  • This hypothesis was initially proposed to explain bacterial dependence on helpers for protection against hydrogen peroxide (HOOH).

Purpose of the Study:

  • To experimentally test the Black Queen Hypothesis's prediction regarding the evolution of cooperation.
  • To investigate the stable coexistence of organisms resulting from the partitioning of essential functions.

Main Methods:

  • Evolving populations of *Escherichia coli* with a plasmid-encoding HOOH-detoxifying enzyme (KatG).
  • Comparing population dynamics in environments with and without HOOH.
  • Analyzing the costs and benefits of KatG expression and HOOH detoxification.

Main Results:

  • In the absence of HOOH, plasmid-carrying cells were outcompeted by plasmid-free segregants due to high expression costs.
  • In the presence of HOOH, plasmid-carrying and plasmid-free cells stably coexisted for over 1200 generations.
  • Evolved plasmid-bearing cells enhanced HOOH removal efficiency, while plasmid-free cells remained dependent on them.

Conclusions:

  • Partitioning of a Black Queen function, like HOOH detoxification, enables stable coexistence of competing organisms.
  • This study provides experimental evidence for the BQH in a simplified microbial system.
  • The findings highlight the evolutionary pathways leading to commensal and mutualistic interactions.