Functional genomics in Campylobacter coli identified a novel streptomycin resistance gene located in a hypervariable genomic region

Satu Olkkola, Alejandra Culebro Escandon y Perez, Pekka Juntunen, Marja-Liisa Hänninen, Mirko Rossi

Research output: Contribution to journalArticleScientificpeer-review

Abstract

Numerous aminoglycoside resistance genes have been reported in Campylobacter spp. often resembling those from Gram-positive bacterial species and located in transferable genetic elements with other resistance genes. We discovered a new streptomycin (STR) resistance gene in Campylobacter coli showing 27–34 % amino acid identity to aminoglycoside 6-nucleotidyl-transferases described previously in Campylobacter. STR resistance was verified by gene expression and insertional inactivation. This ant-like gene differs from the previously described aminoglycoside resistance genes in Campylobacter spp. in several aspects. It does not appear to originate from Gram-positive bacteria and is located in a region corresponding to a previously described hypervariable region 14 of C. jejuni with no other known resistance genes detected in close proximity. Finally, it does not belong to a multiple drug resistance plasmid or transposon. This novel ant-like gene appears widely spread among C. coli as it is found in strains originating both from Europe and the United States and from several, apparently unrelated, hosts and environmental sources. The closest homologue (60 % amino acid identity) was found in certain C. jejuni and C. coli strains in a similar genomic location, but an association with STR resistance was not detected. Based on the findings presented here, we hypothesize that Campylobacter ant-like gene A has originated from a common ancestral proto-resistance element in Campylobacter spp., possibly encoding a protein with a different function. In conclusion, whole genome sequencing allowed us to fill in a knowledge gap concerning STR resistance in C. coli by revealing a novel STR resistance gene possibly inherent to Campylobacter.

Original languageEnglish
JournalMicrobiology
Volume162
Pages (from-to)1157-1166
Number of pages10
ISSN1350-0872
DOIs
Publication statusPublished - Jul 2016
MoE publication typeA1 Journal article-refereed

Fields of Science

  • 413 Veterinary science
  • AMINOGLYCOSIDE-MODIFYING ENZYMES
  • ANTIMICROBIAL RESISTANCE
  • MYCOBACTERIUM-TUBERCULOSIS
  • THERMOPHILIC CAMPYLOBACTER
  • RPSL GENE
  • JEJUNI
  • PLASMID
  • ANTIBIOTICS
  • MUTATIONS
  • SEQUENCE
  • 1183 Plant biology, microbiology, virology

Cite this

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title = "Functional genomics in Campylobacter coli identified a novel streptomycin resistance gene located in a hypervariable genomic region",
abstract = "Numerous aminoglycoside resistance genes have been reported in Campylobacter spp. often resembling those from Gram-positive bacterial species and located in transferable genetic elements with other resistance genes. We discovered a new streptomycin (STR) resistance gene in Campylobacter coli showing 27–34 {\%} amino acid identity to aminoglycoside 6-nucleotidyl-transferases described previously in Campylobacter. STR resistance was verified by gene expression and insertional inactivation. This ant-like gene differs from the previously described aminoglycoside resistance genes in Campylobacter spp. in several aspects. It does not appear to originate from Gram-positive bacteria and is located in a region corresponding to a previously described hypervariable region 14 of C. jejuni with no other known resistance genes detected in close proximity. Finally, it does not belong to a multiple drug resistance plasmid or transposon. This novel ant-like gene appears widely spread among C. coli as it is found in strains originating both from Europe and the United States and from several, apparently unrelated, hosts and environmental sources. The closest homologue (60 {\%} amino acid identity) was found in certain C. jejuni and C. coli strains in a similar genomic location, but an association with STR resistance was not detected. Based on the findings presented here, we hypothesize that Campylobacter ant-like gene A has originated from a common ancestral proto-resistance element in Campylobacter spp., possibly encoding a protein with a different function. In conclusion, whole genome sequencing allowed us to fill in a knowledge gap concerning STR resistance in C. coli by revealing a novel STR resistance gene possibly inherent to Campylobacter.",
keywords = "413 Veterinary science, AMINOGLYCOSIDE-MODIFYING ENZYMES , ANTIMICROBIAL RESISTANCE , MYCOBACTERIUM-TUBERCULOSIS , THERMOPHILIC CAMPYLOBACTER , RPSL GENE , JEJUNI , PLASMID , ANTIBIOTICS , MUTATIONS , SEQUENCE, 1183 Plant biology, microbiology, virology",
author = "Satu Olkkola and {Culebro Escandon y Perez}, Alejandra and Pekka Juntunen and Marja-Liisa H{\"a}nninen and Mirko Rossi",
year = "2016",
month = "7",
doi = "10.1099/mic.0.000304",
language = "English",
volume = "162",
pages = "1157--1166",
journal = "Microbiology",
issn = "1350-0872",
publisher = "American Society for Microbiology",

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Functional genomics in Campylobacter coli identified a novel streptomycin resistance gene located in a hypervariable genomic region. / Olkkola, Satu ; Culebro Escandon y Perez, Alejandra; Juntunen, Pekka ; Hänninen, Marja-Liisa; Rossi, Mirko.

In: Microbiology, Vol. 162, 07.2016, p. 1157-1166.

Research output: Contribution to journalArticleScientificpeer-review

TY - JOUR

T1 - Functional genomics in Campylobacter coli identified a novel streptomycin resistance gene located in a hypervariable genomic region

AU - Olkkola, Satu

AU - Culebro Escandon y Perez, Alejandra

AU - Juntunen, Pekka

AU - Hänninen, Marja-Liisa

AU - Rossi, Mirko

PY - 2016/7

Y1 - 2016/7

N2 - Numerous aminoglycoside resistance genes have been reported in Campylobacter spp. often resembling those from Gram-positive bacterial species and located in transferable genetic elements with other resistance genes. We discovered a new streptomycin (STR) resistance gene in Campylobacter coli showing 27–34 % amino acid identity to aminoglycoside 6-nucleotidyl-transferases described previously in Campylobacter. STR resistance was verified by gene expression and insertional inactivation. This ant-like gene differs from the previously described aminoglycoside resistance genes in Campylobacter spp. in several aspects. It does not appear to originate from Gram-positive bacteria and is located in a region corresponding to a previously described hypervariable region 14 of C. jejuni with no other known resistance genes detected in close proximity. Finally, it does not belong to a multiple drug resistance plasmid or transposon. This novel ant-like gene appears widely spread among C. coli as it is found in strains originating both from Europe and the United States and from several, apparently unrelated, hosts and environmental sources. The closest homologue (60 % amino acid identity) was found in certain C. jejuni and C. coli strains in a similar genomic location, but an association with STR resistance was not detected. Based on the findings presented here, we hypothesize that Campylobacter ant-like gene A has originated from a common ancestral proto-resistance element in Campylobacter spp., possibly encoding a protein with a different function. In conclusion, whole genome sequencing allowed us to fill in a knowledge gap concerning STR resistance in C. coli by revealing a novel STR resistance gene possibly inherent to Campylobacter.

AB - Numerous aminoglycoside resistance genes have been reported in Campylobacter spp. often resembling those from Gram-positive bacterial species and located in transferable genetic elements with other resistance genes. We discovered a new streptomycin (STR) resistance gene in Campylobacter coli showing 27–34 % amino acid identity to aminoglycoside 6-nucleotidyl-transferases described previously in Campylobacter. STR resistance was verified by gene expression and insertional inactivation. This ant-like gene differs from the previously described aminoglycoside resistance genes in Campylobacter spp. in several aspects. It does not appear to originate from Gram-positive bacteria and is located in a region corresponding to a previously described hypervariable region 14 of C. jejuni with no other known resistance genes detected in close proximity. Finally, it does not belong to a multiple drug resistance plasmid or transposon. This novel ant-like gene appears widely spread among C. coli as it is found in strains originating both from Europe and the United States and from several, apparently unrelated, hosts and environmental sources. The closest homologue (60 % amino acid identity) was found in certain C. jejuni and C. coli strains in a similar genomic location, but an association with STR resistance was not detected. Based on the findings presented here, we hypothesize that Campylobacter ant-like gene A has originated from a common ancestral proto-resistance element in Campylobacter spp., possibly encoding a protein with a different function. In conclusion, whole genome sequencing allowed us to fill in a knowledge gap concerning STR resistance in C. coli by revealing a novel STR resistance gene possibly inherent to Campylobacter.

KW - 413 Veterinary science

KW - AMINOGLYCOSIDE-MODIFYING ENZYMES

KW - ANTIMICROBIAL RESISTANCE

KW - MYCOBACTERIUM-TUBERCULOSIS

KW - THERMOPHILIC CAMPYLOBACTER

KW - RPSL GENE

KW - JEJUNI

KW - PLASMID

KW - ANTIBIOTICS

KW - MUTATIONS

KW - SEQUENCE

KW - 1183 Plant biology, microbiology, virology

U2 - 10.1099/mic.0.000304

DO - 10.1099/mic.0.000304

M3 - Article

VL - 162

SP - 1157

EP - 1166

JO - Microbiology

JF - Microbiology

SN - 1350-0872

ER -