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Comprehensive mutation identification in an evolved bacterial cooperator and its cheating ancestor

  1. Gregory J. Velicer † , ‡ ,
  2. Günter Raddatz § ,
  3. Heike Keller † ,
  4. Silvia Deiss † ,
  5. Christa Lanz † ,
  6. Iris Dinkelacker † , and
  7. Stephan C. Schuster
  1. †Max Planck Institute for Developmental Biology, 72076 Tübingen, Germany;
  2. §Max Planck Institute for Biological Cybernetics, 72076 Tübingen, Germany; and
  3. Pennsylvania State University, State College, PA 16802

  1. Edited by W. Ford Doolittle, Dalhousie University, Halifax, NS, Canada, and approved March 23, 2006 (received for review December 13, 2005)

Abstract

Precise characterization of the mutation histories of evolutionary lineages is crucial for understanding the evolutionary process, yet mutation identification has been constrained by traditional techniques. We sought to identify all accumulated mutations in an experimentally evolved lineage of the cooperative bacterium Myxococcus xanthus, which constructs fruiting bodies by a process of social multicellular development in response to starvation. This lineage had undergone two major transitions in social phenotype: from an ancestral cooperator to a socially defective cheater, and from the cheater to a competitively dominant cooperator that re-evolved social and developmental proficiency. The 9.14-Mb genome of the evolved, dominant cooperator (strain “PX”) was sequenced to ≈19-fold coverage by using recent “sequencing-by-synthesis” technology and partially sequenced (≈45%) by using capillary technology. The resulting data revealed 15 single-nucleotide mutations relative to the laboratory ancestor of PX after the two phases of experimental evolution but no evidence of duplications, transpositions, or multiple-base deletions. No mutations were identified by capillary sequencing beyond those found by pyrosequencing, resulting in a high probability that all mutations were discovered. Seven errors in the reference strain previously sequenced by the Sanger approach were revealed, as were five mutational differences between two distinct laboratory stocks of the reference strain. A single mutation responsible for the restoration of development in strain PX was identified, whereas 14 mutations occurred during the prior phase of experimental evolution. These results provide insight into the genetic basis of two large adaptive transitions in a social bacterium.

Footnotes

  • ‡To whom correspondence should be addressed. E-mail: gregory.velicer{at}tuebingen.mpg.de

  • Author contributions: G.J.V. and S.C.S. designed research; G.J.V., G.R., H.K., S.D., C.L., and I.D. performed research; G.J.V. contributed new reagents/analytic tools; G.J.V., G.R., and S.C.S. analyzed data; and G.J.V. and S.C.S. wrote the paper.

  • Conflict of interest statement: No conflicts declared.

  • This paper was submitted directly (Track II) to the PNAS office.

  • Abbreviations:

    Abbreviation:

    TIGR,
    The Institute for Genomic Research.

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