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Cross-species evolutionary rewiring in the enteric bacterium Campylobacter

Aidan J. Taylor, View ORCID ProfileGuillaume Méric, View ORCID ProfileKoji Yahara, View ORCID ProfileBen Pascoe, View ORCID ProfileLeonardos Mageiros, View ORCID ProfileEvangelos Mourkas, View ORCID ProfileJessica K Calland, View ORCID ProfileSanteri Puranen, View ORCID ProfileMatthew D. Hitchings, View ORCID ProfileSion Bayliss, View ORCID ProfileKeith A. Jolley, View ORCID ProfileCarolin M. Kobras, View ORCID ProfileNicola J. Williams, View ORCID ProfileArnoud H. M. van Vliet, View ORCID ProfileJulian Parkhill, View ORCID ProfileMartin C. J. Maiden, View ORCID ProfileJukka Corander, View ORCID ProfileDaniel Falush, View ORCID ProfileXavier Didelot, View ORCID ProfileDavid J. Kelly, View ORCID ProfileSamuel K. Sheppard
doi: https://doi.org/10.1101/2021.03.15.435406
Aidan J. Taylor
1Department of Molecular Biology and Biotechnology, The University of Sheffield, Sheffield S10 2TN, United Kingdom
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Guillaume Méric
2The Milner Centre for Evolution, Department of Biology and Biochemistry, University of Bath, Bath BA2 7AY, UK
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Koji Yahara
3Antimicrobial Resistance Research Centre, National Institute of Infectious Diseases, Tokyo, Japan
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Ben Pascoe
2The Milner Centre for Evolution, Department of Biology and Biochemistry, University of Bath, Bath BA2 7AY, UK
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Leonardos Mageiros
2The Milner Centre for Evolution, Department of Biology and Biochemistry, University of Bath, Bath BA2 7AY, UK
4Department of Infectious Diseases, Central Clinical School, Monash University, Melbourne, Victoria 3004, Australia
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Evangelos Mourkas
2The Milner Centre for Evolution, Department of Biology and Biochemistry, University of Bath, Bath BA2 7AY, UK
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Jessica K Calland
2The Milner Centre for Evolution, Department of Biology and Biochemistry, University of Bath, Bath BA2 7AY, UK
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Santeri Puranen
5Department of Mathematics and Statistics, Helsinki Institute for Information Technology, University of Helsinki, Helsinki, Finland
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  • ORCID record for Santeri Puranen
Matthew D. Hitchings
6Swansea University Medical School, Institute of Life Science, Swansea SA2 8PP, UK
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Sion Bayliss
2The Milner Centre for Evolution, Department of Biology and Biochemistry, University of Bath, Bath BA2 7AY, UK
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Keith A. Jolley
7Department of Zoology, University of Oxford, South Parks Road, Oxford OX1 3PS, UK
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Carolin M. Kobras
1Department of Molecular Biology and Biotechnology, The University of Sheffield, Sheffield S10 2TN, United Kingdom
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Nicola J. Williams
8Department of Epidemiology and Population Health, Institute of Infection & Global Health, University of Liverpool, Leahurst Campus, Wirral, UK
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Arnoud H. M. van Vliet
9School of Veterinary Medicine, University of Surrey, Guildford GU2 7AL, UK
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Julian Parkhill
10Department of Veterinary Medicine, University of Cambridge, Madingley Rd, Cambridge CB3 0ES, UK
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Martin C. J. Maiden
7Department of Zoology, University of Oxford, South Parks Road, Oxford OX1 3PS, UK
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Jukka Corander
5Department of Mathematics and Statistics, Helsinki Institute for Information Technology, University of Helsinki, Helsinki, Finland
11Department of Biostatistics, University of Oslo, Oslo, Norway
12Parasites and Microbes, Wellcome Sanger Institute, Cambridge, UK
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Daniel Falush
13The Centre for Microbes, Development and Health, Institut Pasteur of Shanghai, Shanghai, China
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Xavier Didelot
14School of Life Sciences and Department of Statistics, University of Warwick, Coventry CV4 7AL, UK
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David J. Kelly
1Department of Molecular Biology and Biotechnology, The University of Sheffield, Sheffield S10 2TN, United Kingdom
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  • For correspondence: d.kelly@sheffield.ac.uk s.k.sheppard@bath.ac.uk
Samuel K. Sheppard
2The Milner Centre for Evolution, Department of Biology and Biochemistry, University of Bath, Bath BA2 7AY, UK
7Department of Zoology, University of Oxford, South Parks Road, Oxford OX1 3PS, UK
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  • For correspondence: d.kelly@sheffield.ac.uk s.k.sheppard@bath.ac.uk
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Abstract

The lateral transfer of genes among bacterial strains and species has opposing effects, conferring potentially beneficial adaptations whilst introducing disharmony in coadapted genomes. The prevailing outcome will depend upon the fitness cost of disrupting established epistatic interactions between genes. It is challenging to understand this in nature because it requires population-scale analysis of recombination and genomic coadaptation, and laboratory confirmation of the functional significance of genotype variation. By assigning the ancestry of DNA in the genomes of two species of the world’s most common enteric bacterial pathogen, we show that up to 28% of the Campylobacter coli genome has been recently introgressed from Campylobacter jejuni. Then, by quantifying covariation across the genome we show that >83% of putative epistatic links are between introgressed C. jejuni genes in divergent genomic positions (>20kb apart), consistent with independent acquisition. Much of this covariation is between 16 genes, with just 5 genes accounting for 99% of epistatic SNP pairs. Laboratory mutagenesis and complementation cloning assays demonstrated functional links between these genes, specifically related to formate dehydrogenase (FDH) activity. These findings suggest that the genetic confederations that define genomic species may be transient. Even for complex traits such as central metabolism in the bacterial cell, conditions can arise where epistatic genes can be decoupled, transferred and reinstated in a new genetic background.

Competing Interest Statement

The authors have declared no competing interest.

Footnotes

  • https://www.ncbi.nlm.nih.gov/bioproject/PRJNA689604

  • https://www.ncbi.nlm.nih.gov/bioproject/PRJEB11972

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC-ND 4.0 International license.
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Posted March 15, 2021.
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Cross-species evolutionary rewiring in the enteric bacterium Campylobacter
Aidan J. Taylor, Guillaume Méric, Koji Yahara, Ben Pascoe, Leonardos Mageiros, Evangelos Mourkas, Jessica K Calland, Santeri Puranen, Matthew D. Hitchings, Sion Bayliss, Keith A. Jolley, Carolin M. Kobras, Nicola J. Williams, Arnoud H. M. van Vliet, Julian Parkhill, Martin C. J. Maiden, Jukka Corander, Daniel Falush, Xavier Didelot, David J. Kelly, Samuel K. Sheppard
bioRxiv 2021.03.15.435406; doi: https://doi.org/10.1101/2021.03.15.435406
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Cross-species evolutionary rewiring in the enteric bacterium Campylobacter
Aidan J. Taylor, Guillaume Méric, Koji Yahara, Ben Pascoe, Leonardos Mageiros, Evangelos Mourkas, Jessica K Calland, Santeri Puranen, Matthew D. Hitchings, Sion Bayliss, Keith A. Jolley, Carolin M. Kobras, Nicola J. Williams, Arnoud H. M. van Vliet, Julian Parkhill, Martin C. J. Maiden, Jukka Corander, Daniel Falush, Xavier Didelot, David J. Kelly, Samuel K. Sheppard
bioRxiv 2021.03.15.435406; doi: https://doi.org/10.1101/2021.03.15.435406

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