Distinct Campylobacter fetus lineages adapted as livestock pathogens and human pathobionts in the intestinal microbiota

Gregorio Iraola, Samuel C. Forster, Nitin Kumar, Philippe Lehours, Sadjia Bekal, Francisco J. García-Peña, Fernando Paolicchi, Claudia Morsella, Helmut Hotzel, Po Ren Hsueh, Ana Vidal, Simon Lévesque, Wataru Yamazaki, Claudia Balzan, Agueda Vargas, Alessandra Piccirillo, Bonnie Chaban, Janet E. Hill, Laura Betancor, Luis Collado & 8 others Isabelle Truyers, Anne C. Midwinter, Hatice T. Dagi, Francis Mégraud, Lucía Calleros, Ruben Pérez, Hugo Naya, Trevor D. Lawley

Research output: Contribution to journalArticleResearchpeer-review

6 Citations (Scopus)

Abstract

Campylobacter fetus is a venereal pathogen of cattle and sheep, and an opportunistic human pathogen. It is often assumed that C. fetus infection occurs in humans as a zoonosis through food chain transmission. Here we show that mammalian C. fetus consists of distinct evolutionary lineages, primarily associated with either human or bovine hosts. We use whole-genome phylogenetics on 182 strains from 17 countries to provide evidence that C. fetus may have originated in humans around 10,500 years ago and may have "jumped" into cattle during the livestock domestication period. We detect C. fetus genomes in 8% of healthy human fecal metagenomes, where the human-associated lineages are the dominant type (78%). Thus, our work suggests that C. fetus is an unappreciated human intestinal pathobiont likely spread by human to human transmission. This genome-based evolutionary framework will facilitate C. fetus epidemiology research and the development of improved molecular diagnostics and prevention schemes for this neglected pathogen.

Original languageEnglish
Article number1367
Number of pages8
JournalNature Communications
Volume8
Issue number1
DOIs
Publication statusPublished - 1 Dec 2017

Cite this

Iraola, Gregorio ; Forster, Samuel C. ; Kumar, Nitin ; Lehours, Philippe ; Bekal, Sadjia ; García-Peña, Francisco J. ; Paolicchi, Fernando ; Morsella, Claudia ; Hotzel, Helmut ; Hsueh, Po Ren ; Vidal, Ana ; Lévesque, Simon ; Yamazaki, Wataru ; Balzan, Claudia ; Vargas, Agueda ; Piccirillo, Alessandra ; Chaban, Bonnie ; Hill, Janet E. ; Betancor, Laura ; Collado, Luis ; Truyers, Isabelle ; Midwinter, Anne C. ; Dagi, Hatice T. ; Mégraud, Francis ; Calleros, Lucía ; Pérez, Ruben ; Naya, Hugo ; Lawley, Trevor D. / Distinct Campylobacter fetus lineages adapted as livestock pathogens and human pathobionts in the intestinal microbiota. In: Nature Communications. 2017 ; Vol. 8, No. 1.
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abstract = "Campylobacter fetus is a venereal pathogen of cattle and sheep, and an opportunistic human pathogen. It is often assumed that C. fetus infection occurs in humans as a zoonosis through food chain transmission. Here we show that mammalian C. fetus consists of distinct evolutionary lineages, primarily associated with either human or bovine hosts. We use whole-genome phylogenetics on 182 strains from 17 countries to provide evidence that C. fetus may have originated in humans around 10,500 years ago and may have {"}jumped{"} into cattle during the livestock domestication period. We detect C. fetus genomes in 8{\%} of healthy human fecal metagenomes, where the human-associated lineages are the dominant type (78{\%}). Thus, our work suggests that C. fetus is an unappreciated human intestinal pathobiont likely spread by human to human transmission. This genome-based evolutionary framework will facilitate C. fetus epidemiology research and the development of improved molecular diagnostics and prevention schemes for this neglected pathogen.",
author = "Gregorio Iraola and Forster, {Samuel C.} and Nitin Kumar and Philippe Lehours and Sadjia Bekal and Garc{\'i}a-Pe{\~n}a, {Francisco J.} and Fernando Paolicchi and Claudia Morsella and Helmut Hotzel and Hsueh, {Po Ren} and Ana Vidal and Simon L{\'e}vesque and Wataru Yamazaki and Claudia Balzan and Agueda Vargas and Alessandra Piccirillo and Bonnie Chaban and Hill, {Janet E.} and Laura Betancor and Luis Collado and Isabelle Truyers and Midwinter, {Anne C.} and Dagi, {Hatice T.} and Francis M{\'e}graud and Luc{\'i}a Calleros and Ruben P{\'e}rez and Hugo Naya and Lawley, {Trevor D.}",
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Iraola, G, Forster, SC, Kumar, N, Lehours, P, Bekal, S, García-Peña, FJ, Paolicchi, F, Morsella, C, Hotzel, H, Hsueh, PR, Vidal, A, Lévesque, S, Yamazaki, W, Balzan, C, Vargas, A, Piccirillo, A, Chaban, B, Hill, JE, Betancor, L, Collado, L, Truyers, I, Midwinter, AC, Dagi, HT, Mégraud, F, Calleros, L, Pérez, R, Naya, H & Lawley, TD 2017, 'Distinct Campylobacter fetus lineages adapted as livestock pathogens and human pathobionts in the intestinal microbiota', Nature Communications, vol. 8, no. 1, 1367. https://doi.org/10.1038/s41467-017-01449-9

Distinct Campylobacter fetus lineages adapted as livestock pathogens and human pathobionts in the intestinal microbiota. / Iraola, Gregorio; Forster, Samuel C.; Kumar, Nitin; Lehours, Philippe; Bekal, Sadjia; García-Peña, Francisco J.; Paolicchi, Fernando; Morsella, Claudia; Hotzel, Helmut; Hsueh, Po Ren; Vidal, Ana; Lévesque, Simon; Yamazaki, Wataru; Balzan, Claudia; Vargas, Agueda; Piccirillo, Alessandra; Chaban, Bonnie; Hill, Janet E.; Betancor, Laura; Collado, Luis; Truyers, Isabelle; Midwinter, Anne C.; Dagi, Hatice T.; Mégraud, Francis; Calleros, Lucía; Pérez, Ruben; Naya, Hugo; Lawley, Trevor D.

In: Nature Communications, Vol. 8, No. 1, 1367, 01.12.2017.

Research output: Contribution to journalArticleResearchpeer-review

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AU - Iraola, Gregorio

AU - Forster, Samuel C.

AU - Kumar, Nitin

AU - Lehours, Philippe

AU - Bekal, Sadjia

AU - García-Peña, Francisco J.

AU - Paolicchi, Fernando

AU - Morsella, Claudia

AU - Hotzel, Helmut

AU - Hsueh, Po Ren

AU - Vidal, Ana

AU - Lévesque, Simon

AU - Yamazaki, Wataru

AU - Balzan, Claudia

AU - Vargas, Agueda

AU - Piccirillo, Alessandra

AU - Chaban, Bonnie

AU - Hill, Janet E.

AU - Betancor, Laura

AU - Collado, Luis

AU - Truyers, Isabelle

AU - Midwinter, Anne C.

AU - Dagi, Hatice T.

AU - Mégraud, Francis

AU - Calleros, Lucía

AU - Pérez, Ruben

AU - Naya, Hugo

AU - Lawley, Trevor D.

PY - 2017/12/1

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N2 - Campylobacter fetus is a venereal pathogen of cattle and sheep, and an opportunistic human pathogen. It is often assumed that C. fetus infection occurs in humans as a zoonosis through food chain transmission. Here we show that mammalian C. fetus consists of distinct evolutionary lineages, primarily associated with either human or bovine hosts. We use whole-genome phylogenetics on 182 strains from 17 countries to provide evidence that C. fetus may have originated in humans around 10,500 years ago and may have "jumped" into cattle during the livestock domestication period. We detect C. fetus genomes in 8% of healthy human fecal metagenomes, where the human-associated lineages are the dominant type (78%). Thus, our work suggests that C. fetus is an unappreciated human intestinal pathobiont likely spread by human to human transmission. This genome-based evolutionary framework will facilitate C. fetus epidemiology research and the development of improved molecular diagnostics and prevention schemes for this neglected pathogen.

AB - Campylobacter fetus is a venereal pathogen of cattle and sheep, and an opportunistic human pathogen. It is often assumed that C. fetus infection occurs in humans as a zoonosis through food chain transmission. Here we show that mammalian C. fetus consists of distinct evolutionary lineages, primarily associated with either human or bovine hosts. We use whole-genome phylogenetics on 182 strains from 17 countries to provide evidence that C. fetus may have originated in humans around 10,500 years ago and may have "jumped" into cattle during the livestock domestication period. We detect C. fetus genomes in 8% of healthy human fecal metagenomes, where the human-associated lineages are the dominant type (78%). Thus, our work suggests that C. fetus is an unappreciated human intestinal pathobiont likely spread by human to human transmission. This genome-based evolutionary framework will facilitate C. fetus epidemiology research and the development of improved molecular diagnostics and prevention schemes for this neglected pathogen.

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