Chromosomal toxin–antitoxin loci can diminish large-scale genome reductions in the absence of selection

Authors

  • Silvia Szekeres,

    1. Division of Clinical Integrative Biology, Sunnybrook Health Sciences Centre, 2075 Bayview Avenue, S1-26A, Toronto, Ontario, M4N 3N5, Canada.
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    • These authors contributed equally to this work.

  • Mira Dauti,

    1. Division of Clinical Integrative Biology, Sunnybrook Health Sciences Centre, 2075 Bayview Avenue, S1-26A, Toronto, Ontario, M4N 3N5, Canada.
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    • These authors contributed equally to this work.

  • Caroline Wilde,

    1. Division of Clinical Integrative Biology, Sunnybrook Health Sciences Centre, 2075 Bayview Avenue, S1-26A, Toronto, Ontario, M4N 3N5, Canada.
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  • Didier Mazel,

    1. Unité Postulante Plasticité du Génome Bactérien, Département Génomes et Génétique, Institut Pasteur, 25 rue du Dr Roux, 75724 Paris cedex 15, Paris, France.
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  • Dean A. Rowe-Magnus

    Corresponding author
    1. Division of Clinical Integrative Biology, Sunnybrook Health Sciences Centre, 2075 Bayview Avenue, S1-26A, Toronto, Ontario, M4N 3N5, Canada.
    2. Department of Laboratory Medicine and Pathobiology, Faculty of Medicine, University of Toronto, Toronto, Canada.
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E-mail dean.rowe-magnus@sri.utoronto.ca; Tel. (+1) 416 480 6100 ext. 3318; Fax (+1) 416 480 5737.

Summary

Superintegrons (SIs) are chromosomal genetic elements containing assemblies of genes, each flanked by a recombination sequence (attC site) targeted by the integron integrase. SIs may contain hundreds of attC sites and intrinsic instability is anticipated; yet SIs are remarkably stable. This implies that either selective pressure maintains the genes or mechanisms exist which favour their persistence in the absence of selection. Toxin/antitoxin (TA) systems encode a stable toxin and a specific, unstable antitoxin. Once activated, the continued synthesis of the unstable antitoxin is necessary for cell survival. A bioinformatic search of accessible microbial genomes for SIs and TA systems revealed that large SIs harboured TA gene cassettes while smaller SIs did not. We demonstrated the function of TA loci in different genomic contexts where large-scale deletions can occur; in SIs and in a 165 kb dispensable region of the Escherichia coli genome. When devoid of TA loci, large-scale genome loss was evident in both environments. The inclusion of two TA loci, relBE1 and parDE1, which we identified in the Vibrio vulnificus SI rendered these environments refractory to gene loss. Thus, chromosomal TA loci can stabilize massive SI arrays and limit the extensive gene loss that is a hallmark of reductive evolution.

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