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Properties of genes encoding transfer RNAs as integration sites for genomic islands and prophages in Klebsiella pneumoniae

Camilo Berríos-Pastén, Rodolfo Acevedo, Patricio Arros, Macarena A. Varas, View ORCID ProfileKelly L. Wyres, View ORCID ProfileMargaret M. C. Lam, View ORCID ProfileKathryn E. Holt, View ORCID ProfileRosalba Lagos, View ORCID ProfileAndrés E. Marcoleta
doi: https://doi.org/10.1101/2020.11.02.365908
Camilo Berríos-Pastén
1Grupo de Microbiología Integrativa, Laboratorio de Biología Estructural y Molecular BEM, Departamento de Biología, Facultad de Ciencias, Universidad de Chile. Las Palmeras 3425, Ñuñoa, Santiago, Chile
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Rodolfo Acevedo
1Grupo de Microbiología Integrativa, Laboratorio de Biología Estructural y Molecular BEM, Departamento de Biología, Facultad de Ciencias, Universidad de Chile. Las Palmeras 3425, Ñuñoa, Santiago, Chile
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Patricio Arros
1Grupo de Microbiología Integrativa, Laboratorio de Biología Estructural y Molecular BEM, Departamento de Biología, Facultad de Ciencias, Universidad de Chile. Las Palmeras 3425, Ñuñoa, Santiago, Chile
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Macarena A. Varas
1Grupo de Microbiología Integrativa, Laboratorio de Biología Estructural y Molecular BEM, Departamento de Biología, Facultad de Ciencias, Universidad de Chile. Las Palmeras 3425, Ñuñoa, Santiago, Chile
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Kelly L. Wyres
2Department of Infectious Diseases, Central Clinical School, Monash University, Melbourne 3004, Australia
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Margaret M. C. Lam
2Department of Infectious Diseases, Central Clinical School, Monash University, Melbourne 3004, Australia
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Kathryn E. Holt
2Department of Infectious Diseases, Central Clinical School, Monash University, Melbourne 3004, Australia
3London School of Hygiene & Tropical Medicine, London WC1E 7HT, UK
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Rosalba Lagos
1Grupo de Microbiología Integrativa, Laboratorio de Biología Estructural y Molecular BEM, Departamento de Biología, Facultad de Ciencias, Universidad de Chile. Las Palmeras 3425, Ñuñoa, Santiago, Chile
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Andrés E. Marcoleta
1Grupo de Microbiología Integrativa, Laboratorio de Biología Estructural y Molecular BEM, Departamento de Biología, Facultad de Ciencias, Universidad de Chile. Las Palmeras 3425, Ñuñoa, Santiago, Chile
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  • For correspondence: amarcoleta@uchile.cl
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ABSTRACT

The evolution of traits including antibiotic resistance, virulence, and increased fitness in Klebsiella pneumoniae and related species has been linked to the acquisition of mobile genetic elements through horizontal transfer. Among them, genomic islands (GIs) preferentially integrating at genes encoding tRNAs and the tmRNA (t(m)DNAs) would be significant in promoting chromosomal diversity. Here, we studied the whole set of t(m)DNAs present in 66 Klebsiella chromosomes, investigating their usage as integration sites and the properties of the integrated GIs. A total of 5,624 t(m)DNAs were classified based on their sequence conservation, genomic context, and prevalence. 161 different GIs and prophages were found at these sites, hosting 3,540 gene families including various related to virulence and drug resistance. Phylogenetic analyses supported the acquisition of several of these elements through horizontal gene transfer, likely mediated by a highly diverse set of encoded integrases targeting specific t(m)DNAs and sublocations inside them. Only a subset of the t(m)DNAs had integrated GIs and even identical tDNA copies showed dissimilar usage frequencies, suggesting that the genomic context would influence the integration site selection. This usage bias, likely towards avoiding disruption of polycistronic transcriptional units, would be conserved across Gammaproteobacteria. The systematic comparison of the t(m)DNAs across different strains allowed us to discover an unprecedented number of K. pneumoniae GIs and prophages and to raise important questions and clues regarding the fundamental properties of t(m)DNAs as targets for the integration of mobile genetic elements and drivers of bacterial genome evolution and pathogen emergence.

Competing Interest Statement

The authors have declared no competing interest.

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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 November 03, 2020.
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Properties of genes encoding transfer RNAs as integration sites for genomic islands and prophages in Klebsiella pneumoniae
Camilo Berríos-Pastén, Rodolfo Acevedo, Patricio Arros, Macarena A. Varas, Kelly L. Wyres, Margaret M. C. Lam, Kathryn E. Holt, Rosalba Lagos, Andrés E. Marcoleta
bioRxiv 2020.11.02.365908; doi: https://doi.org/10.1101/2020.11.02.365908
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Properties of genes encoding transfer RNAs as integration sites for genomic islands and prophages in Klebsiella pneumoniae
Camilo Berríos-Pastén, Rodolfo Acevedo, Patricio Arros, Macarena A. Varas, Kelly L. Wyres, Margaret M. C. Lam, Kathryn E. Holt, Rosalba Lagos, Andrés E. Marcoleta
bioRxiv 2020.11.02.365908; doi: https://doi.org/10.1101/2020.11.02.365908

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