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Comparative genomics of the Pasteurella multocida toxin

Publication: Genome
20 January 2021

Abstract

Pasteurella multocida is a zoonotic pathogen whose genetic heterogeneity is well known. Five serogroups (A, B, D, E, and F) and 16 serotypes of P. multocida have been recognized thus far based on capsular polysaccharide typing and lipopolysaccharide typing, respectively. Progressive atrophic rhinitis in domestic pigs is caused by P. multocida strains containing toxA, which encodes a 146 kDa heat-labile toxin. Among the five serogroups, only some strains of serogroups A and D are toxigenic. In this study, by comparative analyses of the genomes of many strains, it has been shown that toxA is sparsely distributed in P. multocida. Furthermore, full-length homologs of P. multocida toxA were found only in two other bacterial species. It has also been shown that toxA is usually associated with a prophage, and that some strains contain an orthologous prophage but not toxA. Among the toxA-containing prophages that were compared, an operon putatively encoding a type II restriction-modification system was present only in strains LFB3, HN01, and HN06. These results indicate that the selection and maintenance of the heat-labile toxin and the type II restriction-modification system are evolutionarily less favorable among P. multocida strains. Phylogenetic analysis using the alignment- and parameter-free method CVTree3 showed that deduced proteome sequences can be used as effectively as whole/core genome single nucleotide polymorphisms to group P. multocida strains in relation to their serotypes and (or) genotypes. It remains to be determined if the toxA-containing prophages in strains HN01 and HN06 are inducible, and if they can be used for lysogenic transfer of toxA to other bacteria.

Résumé

Le Pasteurella multocida est un agent pathogène zoonotique dont l’hétérogénéité génétique est bien connue. Cinq sérogroupes (A, B, D, E et F) et 16 sérotypes du P. multocida ont été créés sur la base, respectivement, des polysaccharides et des lipopolysaccharides de la capsule. La rhinite atrophique progressive chez les porcs est causée par des souches du P. multocida contenant le gène toxA, lequel code pour une toxine de 146 kDa thermolabile. Parmi les cinq sérogroupes, seules certaines souches des sérogroupes A et D sont toxigènes. Dans ce travail, il est montré par analyse comparée des génomes de plusieurs souches que le gène toxA est peu répandu chez le P. multocida. De plus, des homologues complets de toxA du P. multocida ont été trouvés chez seulement deux autres espèces bactériennes. Il a également été montré que toxA est habituellement associé avec un prophage et que certaines souches contiennent un prophage orthologue mais pas toxA. Parmi les prophages contenant toxA qui ont fait l’objet d’une comparaison, un opéron codant potentiellement pour un système de restriction-modification de type II était présent seulement chez les souches LFB3, HN01 et HN06. Ces résultats indiquent que la sélection et le maintien de la toxine thermolabile et du système de restriction-modification sont peu favorisés par l’évolution au sein des souches du P. multocida. Une analyse phylogénétique faisant appel à une méthode CVTree3 sans alignement et sans paramètres a montré que les séquences prédites du protéome peuvent s’avérer tout aussi utiles pour grouper les souches du P. multocida en sérotypes ou en génotypes que les polymorphismes mononucléotidiques du génome entier/commun. Il reste à déterminer si les prophages contenant toxA dans les souches HN01 et HN06 sont inductibles et s’ils peuvent opérer un transfert lysogène de toxA à d’autres bactéries. [Traduit par la Rédaction]

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Supplementary Material

Supplementary data (gen-2020-0176suppl.zip)

Information & Authors

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Published In

cover image Genome
Genome
Volume 64Number 7July 2021
Pages: 679 - 692

History

Received: 17 October 2020
Accepted: 14 January 2021
Accepted manuscript online: 20 January 2021
Version of record online: 20 January 2021

Notes

This article commemorates the 45th anniversary of the 1975 report by Il’ina and Zasukhin on the discovery of toxigenic isolates of Pasteurella multocida in pigs manifesting atrophic rhinitis.

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Key Words

  1. Pasteurella
  2. toxA
  3. PMT
  4. prophage
  5. HGT
  6. phylogenomics

Mots-clés

  1. Pasteurella
  2. toxA
  3. PMT
  4. prophage
  5. HGT
  6. phylogénomique

Authors

Affiliations

Shivakumara Siddaramappa [email protected]
Institute of Bioinformatics and Applied Biotechnology, Biotech Park, Electronic City, Bengaluru, Karnataka 560100, India.

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3. Pasteurella multocida toxin – lessons learned from a mitogenic toxin

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