Convergent amino acid signatures in polyphyletic Campylobacter jejuni subpopulations suggest human niche tropism

Guillaume Méric, Alan McNally, Alberto Pessia, Evangelos Mourkas, Ben Pascoe, Leonardos Mageiros, Minna Emilia Vehkala, Jukka Ilmari Corander, Samuel K. Shepard

Forskningsoutput: TidskriftsbidragArtikelVetenskapligPeer review

Sammanfattning

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.
Originalspråkengelska
TidskriftGenome Biology and Evolution
Volym10
Utgåva3
Sidor (från-till)763-774
Antal sidor12
ISSN1759-6653
DOI
StatusPublicerad - 1 mar 2018
MoE-publikationstypA1 Tidskriftsartikel-refererad

Vetenskapsgrenar

  • 1184 Genetik, utvecklingsbiologi, fysiologi
  • 112 Statistik

Citera det här

Méric, Guillaume ; McNally, Alan ; Pessia, Alberto ; Mourkas, Evangelos ; Pascoe, Ben ; Mageiros, Leonardos ; Vehkala, Minna Emilia ; Corander, Jukka Ilmari ; Shepard, Samuel K. / Convergent amino acid signatures in polyphyletic Campylobacter jejuni subpopulations suggest human niche tropism. I: Genome Biology and Evolution. 2018 ; Vol. 10, Nr. 3. s. 763-774.
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title = "Convergent amino acid signatures in polyphyletic Campylobacter jejuni subpopulations 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 = "1184 Genetics, developmental biology, physiology, BAYESIAN-ANALYSIS, PHYLOGENETICS, KPAX SOFTWARE, CAMPYLOBACTER JEJUNI, ADAPTATION, PATHOGENESIS, 112 Statistics and probability",
author = "Guillaume M{\'e}ric and Alan McNally and Alberto Pessia and Evangelos Mourkas and Ben Pascoe and Leonardos Mageiros and Vehkala, {Minna Emilia} and Corander, {Jukka Ilmari} and Shepard, {Samuel K.}",
year = "2018",
month = "3",
day = "1",
doi = "10.1093/gbe/evy026",
language = "English",
volume = "10",
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journal = "Genome Biology and Evolution",
issn = "1759-6653",
publisher = "Oxford University Press",
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Convergent amino acid signatures in polyphyletic Campylobacter jejuni subpopulations suggest human niche tropism. / Méric, Guillaume; McNally, Alan; Pessia, Alberto; Mourkas, Evangelos; Pascoe, Ben; Mageiros, Leonardos; Vehkala, Minna Emilia; Corander, Jukka Ilmari; Shepard, Samuel K.

I: Genome Biology and Evolution, Vol. 10, Nr. 3, 01.03.2018, s. 763-774.

Forskningsoutput: TidskriftsbidragArtikelVetenskapligPeer review

TY - JOUR

T1 - Convergent amino acid signatures in polyphyletic Campylobacter jejuni subpopulations 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 Emilia

AU - Corander, Jukka Ilmari

AU - Shepard, Samuel K.

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 - 1184 Genetics, developmental biology, physiology

KW - BAYESIAN-ANALYSIS

KW - PHYLOGENETICS

KW - KPAX SOFTWARE

KW - CAMPYLOBACTER JEJUNI

KW - ADAPTATION

KW - PATHOGENESIS

KW - 112 Statistics and probability

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 -