Convergent amino acid signatures in polyphyletic Campylobacter jejuni sub-populations suggest human niche tropism

Guillaume Méric, Alan McNally, Alberto Pessia, Evangelos Mourkas, Ben Pascoe, Leonardos Mageiros, Minna Vehkala, Jukka Corander, Samuel K Sheppard

Research output: Contribution to journalArticle

3 Citations (Scopus)

Abstract

Human infection with the gastrointestinal pathogen Campylobacter jejuni is dependent upon the opportunity for zoonotic transmission and the ability of strains to colonize the human host. Certain lineages of this diverse organism are more common in human infection but the factors underlying this overrepresentation are not fully understood. We analyzed 601 isolate genomes from agricultural animals and human clinical cases, including isolates from the multihost (ecological generalist) ST-21 and ST-45 clonal complexes (CCs). Combined nucleotide and amino acid sequence analysis identified 12 human-only amino acid KPAX clusters among polyphyletic lineages within the common disease causing CC21 group isolates, with no such clusters among CC45 isolates. Isolate sequence types within human-only CC21 group KPAX clusters have been sampled from other hosts, including poultry, so rather than representing unsampled reservoir hosts, the increase in relative frequency in human infection potentially reflects a genetic bottleneck at the point of human infection. Consistent with this, sequence enrichment analysis identified nucleotide variation in genes with putative functions related to human colonization and pathogenesis, in human-only clusters. Furthermore, the tight clustering and polyphyly of human-only lineage clusters within a single CC suggest the repeated evolution of human association through acquisition of genetic elements within this complex. Taken together, combined nucleotide and amino acid analysis of large isolate collections may provide clues about human niche tropism and the nature of the forces that promote the emergence of clinically important C. jejuni lineages.

Original languageEnglish
Pages (from-to)763-774
Number of pages12
JournalGenome biology and evolution
Volume10
Issue number3
Early online date14 Feb 2018
DOIs
Publication statusPublished - 1 Mar 2018

Fingerprint

tropisms
Campylobacter jejuni
Tropism
subpopulation
human population
niche
niches
amino acid
Amino Acids
amino acids
Population
population bottleneck
poultry
generalist
colonization
genome
pathogen
Nucleotides
nucleotides
Infection

Keywords

  • Animals
  • Campylobacter Infections/microbiology
  • Campylobacter jejuni/genetics
  • Chickens/genetics
  • Genetic Variation
  • Genotype
  • Host-Pathogen Interactions/genetics
  • Humans
  • Multilocus Sequence Typing
  • Phylogeny
  • Poultry/microbiology

Cite this

Convergent amino acid signatures in polyphyletic Campylobacter jejuni sub-populations suggest human niche tropism. / Méric, Guillaume; McNally, Alan; Pessia, Alberto; Mourkas, Evangelos; Pascoe, Ben; Mageiros, Leonardos; Vehkala, Minna; Corander, Jukka; Sheppard, Samuel K.

In: Genome biology and evolution, Vol. 10, No. 3, 01.03.2018, p. 763-774.

Research output: Contribution to journalArticle

@article{e982a9d78e3d4f30b3a0c9d5926211d1,
title = "Convergent amino acid signatures in polyphyletic Campylobacter jejuni sub-populations suggest human niche tropism",
abstract = "Human infection with the gastrointestinal pathogen Campylobacter jejuni is dependent upon the opportunity for zoonotic transmission and the ability of strains to colonize the human host. Certain lineages of this diverse organism are more common in human infection but the factors underlying this overrepresentation are not fully understood. We analyzed 601 isolate genomes from agricultural animals and human clinical cases, including isolates from the multihost (ecological generalist) ST-21 and ST-45 clonal complexes (CCs). Combined nucleotide and amino acid sequence analysis identified 12 human-only amino acid KPAX clusters among polyphyletic lineages within the common disease causing CC21 group isolates, with no such clusters among CC45 isolates. Isolate sequence types within human-only CC21 group KPAX clusters have been sampled from other hosts, including poultry, so rather than representing unsampled reservoir hosts, the increase in relative frequency in human infection potentially reflects a genetic bottleneck at the point of human infection. Consistent with this, sequence enrichment analysis identified nucleotide variation in genes with putative functions related to human colonization and pathogenesis, in human-only clusters. Furthermore, the tight clustering and polyphyly of human-only lineage clusters within a single CC suggest the repeated evolution of human association through acquisition of genetic elements within this complex. Taken together, combined nucleotide and amino acid analysis of large isolate collections may provide clues about human niche tropism and the nature of the forces that promote the emergence of clinically important C. jejuni lineages.",
keywords = "Animals, Campylobacter Infections/microbiology, Campylobacter jejuni/genetics, Chickens/genetics, Genetic Variation, Genotype, Host-Pathogen Interactions/genetics, Humans, Multilocus Sequence Typing, Phylogeny, Poultry/microbiology",
author = "Guillaume M{\'e}ric and Alan McNally and Alberto Pessia and Evangelos Mourkas and Ben Pascoe and Leonardos Mageiros and Minna Vehkala and Jukka Corander and Sheppard, {Samuel K}",
note = "{\circledC} The Author(s) 2018. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution.",
year = "2018",
month = "3",
day = "1",
doi = "10.1093/gbe/evy026",
language = "English",
volume = "10",
pages = "763--774",
journal = "Genome biology and evolution",
issn = "1759-6653",
publisher = "Oxford University Press",
number = "3",

}

TY - JOUR

T1 - Convergent amino acid signatures in polyphyletic Campylobacter jejuni sub-populations suggest human niche tropism

AU - Méric, Guillaume

AU - McNally, Alan

AU - Pessia, Alberto

AU - Mourkas, Evangelos

AU - Pascoe, Ben

AU - Mageiros, Leonardos

AU - Vehkala, Minna

AU - Corander, Jukka

AU - Sheppard, Samuel K

N1 - © The Author(s) 2018. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution.

PY - 2018/3/1

Y1 - 2018/3/1

N2 - Human infection with the gastrointestinal pathogen Campylobacter jejuni is dependent upon the opportunity for zoonotic transmission and the ability of strains to colonize the human host. Certain lineages of this diverse organism are more common in human infection but the factors underlying this overrepresentation are not fully understood. We analyzed 601 isolate genomes from agricultural animals and human clinical cases, including isolates from the multihost (ecological generalist) ST-21 and ST-45 clonal complexes (CCs). Combined nucleotide and amino acid sequence analysis identified 12 human-only amino acid KPAX clusters among polyphyletic lineages within the common disease causing CC21 group isolates, with no such clusters among CC45 isolates. Isolate sequence types within human-only CC21 group KPAX clusters have been sampled from other hosts, including poultry, so rather than representing unsampled reservoir hosts, the increase in relative frequency in human infection potentially reflects a genetic bottleneck at the point of human infection. Consistent with this, sequence enrichment analysis identified nucleotide variation in genes with putative functions related to human colonization and pathogenesis, in human-only clusters. Furthermore, the tight clustering and polyphyly of human-only lineage clusters within a single CC suggest the repeated evolution of human association through acquisition of genetic elements within this complex. Taken together, combined nucleotide and amino acid analysis of large isolate collections may provide clues about human niche tropism and the nature of the forces that promote the emergence of clinically important C. jejuni lineages.

AB - Human infection with the gastrointestinal pathogen Campylobacter jejuni is dependent upon the opportunity for zoonotic transmission and the ability of strains to colonize the human host. Certain lineages of this diverse organism are more common in human infection but the factors underlying this overrepresentation are not fully understood. We analyzed 601 isolate genomes from agricultural animals and human clinical cases, including isolates from the multihost (ecological generalist) ST-21 and ST-45 clonal complexes (CCs). Combined nucleotide and amino acid sequence analysis identified 12 human-only amino acid KPAX clusters among polyphyletic lineages within the common disease causing CC21 group isolates, with no such clusters among CC45 isolates. Isolate sequence types within human-only CC21 group KPAX clusters have been sampled from other hosts, including poultry, so rather than representing unsampled reservoir hosts, the increase in relative frequency in human infection potentially reflects a genetic bottleneck at the point of human infection. Consistent with this, sequence enrichment analysis identified nucleotide variation in genes with putative functions related to human colonization and pathogenesis, in human-only clusters. Furthermore, the tight clustering and polyphyly of human-only lineage clusters within a single CC suggest the repeated evolution of human association through acquisition of genetic elements within this complex. Taken together, combined nucleotide and amino acid analysis of large isolate collections may provide clues about human niche tropism and the nature of the forces that promote the emergence of clinically important C. jejuni lineages.

KW - Animals

KW - Campylobacter Infections/microbiology

KW - Campylobacter jejuni/genetics

KW - Chickens/genetics

KW - Genetic Variation

KW - Genotype

KW - Host-Pathogen Interactions/genetics

KW - Humans

KW - Multilocus Sequence Typing

KW - Phylogeny

KW - Poultry/microbiology

UR - http://www.scopus.com/inward/record.url?scp=85052787765&partnerID=8YFLogxK

U2 - 10.1093/gbe/evy026

DO - 10.1093/gbe/evy026

M3 - Article

VL - 10

SP - 763

EP - 774

JO - Genome biology and evolution

JF - Genome biology and evolution

SN - 1759-6653

IS - 3

ER -