Phylogenetic barriers to horizontal transfer of antimicrobial peptide resistance genes in the human gut microbiota

Bálint Kintses, Orsolya Méhi, Eszter Ari, Mónika Számel, Ádám Györkei, Pramod K. Jangir, István Nagy, Ferenc Pál, Gergely Fekete, Roland Tengölics, Ákos Nyerges, István Likó, Anita Bálint, T. Molnár, Balázs Bálint, Bálint Márk Vásárhelyi, Misshelle Bustamante, B. Papp, C. Pál

Research output: Contribution to journalArticle

7 Citations (Scopus)

Abstract

The human gut microbiota has adapted to the presence of antimicrobial peptides (AMPs), which are ancient components of immune defence. Despite its medical importance, it has remained unclear whether AMP resistance genes in the gut microbiome are available for genetic exchange between bacterial species. Here, we show that AMP resistance and antibiotic resistance genes differ in their mobilization patterns and functional compatibilities with new bacterial hosts. First, whereas AMP resistance genes are widespread in the gut microbiome, their rate of horizontal transfer is lower than that of antibiotic resistance genes. Second, gut microbiota culturing and functional metagenomics have revealed that AMP resistance genes originating from phylogenetically distant bacteria have only a limited potential to confer resistance in Escherichia coli, an intrinsically susceptible species. Taken together, functional compatibility with the new bacterial host emerges as a key factor limiting the genetic exchange of AMP resistance genes. Finally, our results suggest that AMPs induce highly specific changes in the composition of the human microbiota, with implications for disease risks.

Original languageEnglish
JournalNature Microbiology
DOIs
Publication statusAccepted/In press - Jan 1 2018

Fingerprint

Peptides
Genes
Microbial Drug Resistance
Metagenomics
Microbiota
Gastrointestinal Microbiome
Escherichia coli
Bacteria

ASJC Scopus subject areas

  • Microbiology
  • Immunology
  • Applied Microbiology and Biotechnology
  • Genetics
  • Microbiology (medical)
  • Cell Biology

Cite this

Phylogenetic barriers to horizontal transfer of antimicrobial peptide resistance genes in the human gut microbiota. / Kintses, Bálint; Méhi, Orsolya; Ari, Eszter; Számel, Mónika; Györkei, Ádám; Jangir, Pramod K.; Nagy, István; Pál, Ferenc; Fekete, Gergely; Tengölics, Roland; Nyerges, Ákos; Likó, István; Bálint, Anita; Molnár, T.; Bálint, Balázs; Vásárhelyi, Bálint Márk; Bustamante, Misshelle; Papp, B.; Pál, C.

In: Nature Microbiology, 01.01.2018.

Research output: Contribution to journalArticle

Kintses, B, Méhi, O, Ari, E, Számel, M, Györkei, Á, Jangir, PK, Nagy, I, Pál, F, Fekete, G, Tengölics, R, Nyerges, Á, Likó, I, Bálint, A, Molnár, T, Bálint, B, Vásárhelyi, BM, Bustamante, M, Papp, B & Pál, C 2018, 'Phylogenetic barriers to horizontal transfer of antimicrobial peptide resistance genes in the human gut microbiota', Nature Microbiology. https://doi.org/10.1038/s41564-018-0313-5
Kintses, Bálint ; Méhi, Orsolya ; Ari, Eszter ; Számel, Mónika ; Györkei, Ádám ; Jangir, Pramod K. ; Nagy, István ; Pál, Ferenc ; Fekete, Gergely ; Tengölics, Roland ; Nyerges, Ákos ; Likó, István ; Bálint, Anita ; Molnár, T. ; Bálint, Balázs ; Vásárhelyi, Bálint Márk ; Bustamante, Misshelle ; Papp, B. ; Pál, C. / Phylogenetic barriers to horizontal transfer of antimicrobial peptide resistance genes in the human gut microbiota. In: Nature Microbiology. 2018.
@article{4cb790172049469ab1da3066aead7ecb,
title = "Phylogenetic barriers to horizontal transfer of antimicrobial peptide resistance genes in the human gut microbiota",
abstract = "The human gut microbiota has adapted to the presence of antimicrobial peptides (AMPs), which are ancient components of immune defence. Despite its medical importance, it has remained unclear whether AMP resistance genes in the gut microbiome are available for genetic exchange between bacterial species. Here, we show that AMP resistance and antibiotic resistance genes differ in their mobilization patterns and functional compatibilities with new bacterial hosts. First, whereas AMP resistance genes are widespread in the gut microbiome, their rate of horizontal transfer is lower than that of antibiotic resistance genes. Second, gut microbiota culturing and functional metagenomics have revealed that AMP resistance genes originating from phylogenetically distant bacteria have only a limited potential to confer resistance in Escherichia coli, an intrinsically susceptible species. Taken together, functional compatibility with the new bacterial host emerges as a key factor limiting the genetic exchange of AMP resistance genes. Finally, our results suggest that AMPs induce highly specific changes in the composition of the human microbiota, with implications for disease risks.",
author = "B{\'a}lint Kintses and Orsolya M{\'e}hi and Eszter Ari and M{\'o}nika Sz{\'a}mel and {\'A}d{\'a}m Gy{\"o}rkei and Jangir, {Pramod K.} and Istv{\'a}n Nagy and Ferenc P{\'a}l and Gergely Fekete and Roland Teng{\"o}lics and {\'A}kos Nyerges and Istv{\'a}n Lik{\'o} and Anita B{\'a}lint and T. Moln{\'a}r and Bal{\'a}zs B{\'a}lint and V{\'a}s{\'a}rhelyi, {B{\'a}lint M{\'a}rk} and Misshelle Bustamante and B. Papp and C. P{\'a}l",
year = "2018",
month = "1",
day = "1",
doi = "10.1038/s41564-018-0313-5",
language = "English",
journal = "Nature Microbiology",
issn = "2058-5276",
publisher = "Nature Publishing Group",

}

TY - JOUR

T1 - Phylogenetic barriers to horizontal transfer of antimicrobial peptide resistance genes in the human gut microbiota

AU - Kintses, Bálint

AU - Méhi, Orsolya

AU - Ari, Eszter

AU - Számel, Mónika

AU - Györkei, Ádám

AU - Jangir, Pramod K.

AU - Nagy, István

AU - Pál, Ferenc

AU - Fekete, Gergely

AU - Tengölics, Roland

AU - Nyerges, Ákos

AU - Likó, István

AU - Bálint, Anita

AU - Molnár, T.

AU - Bálint, Balázs

AU - Vásárhelyi, Bálint Márk

AU - Bustamante, Misshelle

AU - Papp, B.

AU - Pál, C.

PY - 2018/1/1

Y1 - 2018/1/1

N2 - The human gut microbiota has adapted to the presence of antimicrobial peptides (AMPs), which are ancient components of immune defence. Despite its medical importance, it has remained unclear whether AMP resistance genes in the gut microbiome are available for genetic exchange between bacterial species. Here, we show that AMP resistance and antibiotic resistance genes differ in their mobilization patterns and functional compatibilities with new bacterial hosts. First, whereas AMP resistance genes are widespread in the gut microbiome, their rate of horizontal transfer is lower than that of antibiotic resistance genes. Second, gut microbiota culturing and functional metagenomics have revealed that AMP resistance genes originating from phylogenetically distant bacteria have only a limited potential to confer resistance in Escherichia coli, an intrinsically susceptible species. Taken together, functional compatibility with the new bacterial host emerges as a key factor limiting the genetic exchange of AMP resistance genes. Finally, our results suggest that AMPs induce highly specific changes in the composition of the human microbiota, with implications for disease risks.

AB - The human gut microbiota has adapted to the presence of antimicrobial peptides (AMPs), which are ancient components of immune defence. Despite its medical importance, it has remained unclear whether AMP resistance genes in the gut microbiome are available for genetic exchange between bacterial species. Here, we show that AMP resistance and antibiotic resistance genes differ in their mobilization patterns and functional compatibilities with new bacterial hosts. First, whereas AMP resistance genes are widespread in the gut microbiome, their rate of horizontal transfer is lower than that of antibiotic resistance genes. Second, gut microbiota culturing and functional metagenomics have revealed that AMP resistance genes originating from phylogenetically distant bacteria have only a limited potential to confer resistance in Escherichia coli, an intrinsically susceptible species. Taken together, functional compatibility with the new bacterial host emerges as a key factor limiting the genetic exchange of AMP resistance genes. Finally, our results suggest that AMPs induce highly specific changes in the composition of the human microbiota, with implications for disease risks.

UR - http://www.scopus.com/inward/record.url?scp=85058845405&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=85058845405&partnerID=8YFLogxK

U2 - 10.1038/s41564-018-0313-5

DO - 10.1038/s41564-018-0313-5

M3 - Article

AN - SCOPUS:85058845405

JO - Nature Microbiology

JF - Nature Microbiology

SN - 2058-5276

ER -