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A reservoir of 'historical' antibiotic resistance genes in remote pristine Antarctic soils

Marc W. Van Goethem, Rian Pierneef, Oliver K. I. Bezuidt, Yves Van de Peer UGent, Don A. Cowan and Thulani P. Makhalanyane (2018) MICROBIOME. 6.
abstract
Background: Soil bacteria naturally produce antibiotics as a competitive mechanism, with a concomitant evolution, and exchange by horizontal gene transfer, of a range of antibiotic resistance mechanisms. Surveys of bacterial resistance elements in edaphic systems have originated primarily from human-impacted environments, with relatively little information from remote and pristine environments, where the resistome may comprise the ancestral gene diversity. Methods: We used shotgun metagenomics to assess antibiotic resistance gene (ARG) distribution in 17 pristine and remote Antarctic surface soils within the undisturbed Mackay Glacier region. We also interrogated the phylogenetic placement of ARGs compared to environmental ARG sequences and tested for the presence of horizontal gene transfer elements flanking ARGs. Results: In total, 177 naturally occurring ARGs were identified, most of which encoded single or multi-drug efflux pumps. Resistance mechanisms for the inactivation of aminoglycosides, chloramphenicol and beta-lactam antibiotics were also common. Gram-negative bacteria harboured most ARGs (71%), with fewer genes from Gram-positive Actinobacteria and Bacilli (Firmicutes) (9%), reflecting the taxonomic composition of the soils. Strikingly, the abundance of ARGs per sample had a strong, negative correlation with species richness (r=-0.49, P < 0.05). This result, coupled with a lack of mobile genetic elements flanking ARGs, suggests that these genes are ancient acquisitions of horizontal transfer events. Conclusions: ARGs in these remote and uncontaminated soils most likely represent functional efficient historical genes that have since been vertically inherited over generations. The historical ARGs in these pristine environments carry a strong phylogenetic signal and form a monophyletic group relative to ARGs from other similar environments.
Please use this url to cite or link to this publication:
author
organization
year
type
journalArticle (original)
publication status
published
subject
keyword
MICROBIAL COMMUNITIES, DRUG-RESISTANCE, BETA-LACTAMASES, ALASKAN SOIL, BACTERIA, RESISTOME, ENVIRONMENT, DATABASE, TOOL, BIOSYNTHESIS, Antibiotic resistance genes, Soil resistome, Antarctica, Metagenomics
journal title
MICROBIOME
Microbiome
volume
6
article number
40
pages
12 pages
publisher
Biomed Central Ltd
place of publication
London
Web of Science type
Article
Web of Science id
000426382900001
ISSN
2049-2618
DOI
10.1186/s40168-018-0424-5
project
Bioinformatics: from nucleotids to networks (N2N)
language
English
UGent publication?
yes
classification
U
id
8558164
handle
http://hdl.handle.net/1854/LU-8558164
date created
2018-04-03 13:39:29
date last changed
2018-04-03 13:39:29
@article{8558164,
  abstract     = {Background: Soil bacteria naturally produce antibiotics as a competitive mechanism, with a concomitant evolution, and exchange by horizontal gene transfer, of a range of antibiotic resistance mechanisms. Surveys of bacterial resistance elements in edaphic systems have originated primarily from human-impacted environments, with relatively little information from remote and pristine environments, where the resistome may comprise the ancestral gene diversity. Methods: We used shotgun metagenomics to assess antibiotic resistance gene (ARG) distribution in 17 pristine and remote Antarctic surface soils within the undisturbed Mackay Glacier region. We also interrogated the phylogenetic placement of ARGs compared to environmental ARG sequences and tested for the presence of horizontal gene transfer elements flanking ARGs. Results: In total, 177 naturally occurring ARGs were identified, most of which encoded single or multi-drug efflux pumps. Resistance mechanisms for the inactivation of aminoglycosides, chloramphenicol and beta-lactam antibiotics were also common. Gram-negative bacteria harboured most ARGs (71\%), with fewer genes from Gram-positive Actinobacteria and Bacilli (Firmicutes) (9\%), reflecting the taxonomic composition of the soils. Strikingly, the abundance of ARGs per sample had a strong, negative correlation with species richness (r=-0.49, P {\textlangle} 0.05). This result, coupled with a lack of mobile genetic elements flanking ARGs, suggests that these genes are ancient acquisitions of horizontal transfer events. Conclusions: ARGs in these remote and uncontaminated soils most likely represent functional efficient historical genes that have since been vertically inherited over generations. The historical ARGs in these pristine environments carry a strong phylogenetic signal and form a monophyletic group relative to ARGs from other similar environments.},
  articleno    = {40},
  author       = {Van Goethem, Marc W. and Pierneef, Rian and Bezuidt, Oliver K. I. and Van de Peer, Yves and Cowan, Don A. and Makhalanyane, Thulani P.},
  issn         = {2049-2618},
  journal      = {MICROBIOME},
  keyword      = {MICROBIAL COMMUNITIES,DRUG-RESISTANCE,BETA-LACTAMASES,ALASKAN SOIL,BACTERIA,RESISTOME,ENVIRONMENT,DATABASE,TOOL,BIOSYNTHESIS,Antibiotic resistance genes,Soil resistome,Antarctica,Metagenomics},
  language     = {eng},
  pages        = {12},
  publisher    = {Biomed Central Ltd},
  title        = {A reservoir of 'historical' antibiotic resistance genes in remote pristine Antarctic soils},
  url          = {http://dx.doi.org/10.1186/s40168-018-0424-5},
  volume       = {6},
  year         = {2018},
}

Chicago
Van Goethem, Marc W., Rian Pierneef, Oliver K. I. Bezuidt, Yves Van de Peer, Don A. Cowan, and Thulani P. Makhalanyane. 2018. “A Reservoir of ‘Historical’ Antibiotic Resistance Genes in Remote Pristine Antarctic Soils.” Microbiome 6.
APA
Van Goethem, M. W., Pierneef, R., Bezuidt, O. K. I., Van de Peer, Y., Cowan, D. A., & Makhalanyane, T. P. (2018). A reservoir of “historical” antibiotic resistance genes in remote pristine Antarctic soils. MICROBIOME, 6.
Vancouver
1.
Van Goethem MW, Pierneef R, Bezuidt OKI, Van de Peer Y, Cowan DA, Makhalanyane TP. A reservoir of “historical” antibiotic resistance genes in remote pristine Antarctic soils. MICROBIOME. London: Biomed Central Ltd; 2018;6.
MLA
Van Goethem, Marc W., Rian Pierneef, Oliver K. I. Bezuidt, et al. “A Reservoir of ‘Historical’ Antibiotic Resistance Genes in Remote Pristine Antarctic Soils.” MICROBIOME 6 (2018): n. pag. Print.