Evidence for Vertical Inheritance and Loss of the Leukotoxin Operon in Genus Mannheimia

Jesper Larsen, Anders Gorm Pedersen, Henrik Christensen, Magne Bisgaard, Øystein Angen, Peter Ahrens, John E. Olsen

    Research output: Contribution to journalJournal articlepeer-review

    Abstract

    The Mannheimia subclades belong to the same bacterial genus but have taken divergent paths toward their distinct lifestyles. M. haemolytica + M. glucosida are potential pathogens of the respiratory tract in the mammalian suborder Ruminantia, whereas M. ruminalis, the supposed sister group, lives as a commensal in the ovine rumen. We have tested the hypothesis that horizontal gene transfer of the leukotoxin operon has catalyzed pathogenic adaptation and speciation of M. haemolytica + M. glucosida, or other major subclades, by using a strategy that combines compositional and phylogenetic methods. We show that it has been vertically inherited from the last common ancestor of the diverging Mannheimia subclades, although several strains belonging to M. ruminalis have lost the operon. Our analyses support that divergence within M. ruminalis following colonization of the ovine rumen was very rapid and that functional decay of most of the leukotoxin operons occurred early when the adaptation to the rumen was fastest, suggesting that antagonistic pleiotropy was the main contributor to losses in the radiating lineages of M. ruminalis. To sum up, the scenario derived from these analyses reflects two aspects. On one hand, it opposes the hypothesis of horizontal gene transfer as a catalyst of pathogenic adaptation and speciation. On the other hand, it indicates that losses of the leukotoxin operons in the radiating lineages of M. ruminalis have catalyzed their adaptation to a commensal environment and reproductive isolation (speciation).
    Original languageEnglish
    JournalJournal of molecular evolution
    Volume64
    Issue number4
    Pages (from-to)423-437
    ISSN0022-2844
    DOIs
    Publication statusPublished - 2007

    Keywords

    • leukotoxin
    • gene loss
    • vertical inheritance
    • Manneheimia

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