Sewage effluent from an Indian hospital harbors novel carbapenemases and integron-borne antibiotic resistance genes

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Abstract

Background

Hospital wastewaters contain fecal material from a large number of individuals, of which many are undergoing antibiotic therapy. It is, thus, plausible that hospital wastewaters could provide opportunities to find novel carbapenemases and other resistance genes not yet described in clinical strains. Our aim was therefore to investigate the microbiota and antibiotic resistome of hospital effluent collected from the city of Mumbai, India, with a special focus on identifying novel carbapenemases.

Results

Shotgun metagenomics revealed a total of 112 different mobile antibiotic resistance gene types, conferring resistance against almost all classes of antibiotics. Beta-lactamase genes, including encoding clinically important carbapenemases, such as NDM, VIM, IMP, KPC, and OXA-48, were abundant. NDM (0.9% relative abundance to 16S rRNA genes) was the most common carbapenemase gene, followed by OXA-58 (0.84% relative abundance to 16S rRNA genes). Among the investigated mobile genetic elements, class 1 integrons (11% relative abundance to 16S rRNA genes) were the most abundant. The genus Acinetobacter accounted for as many as 30% of the total 16S rRNA reads, with A. baumannii accounting for an estimated 2.5%. High throughput sequencing of amplified integron gene cassettes identified a novel functional variant of an IMP-type (proposed IMP-81) carbapenemase gene (eight aa substitutions) along with recently described novel resistance genes like sul4 and bla _RSA1. Using a computational hidden Markov model, we detected 27 unique metallo-beta-lactamase (MBL) genes in the shotgun data, of which nine were novel subclass B1 genes, one novel subclass B2, and 10 novel subclass B3 genes. Six of the seven novel MBL genes were functional when expressed in Escherichia coli.

Conclusion

By exploring hospital wastewater from India, our understanding of the diversity of carbapenemases has been extended. The study also demonstrates that the microbiota of hospital wastewater can serve as a reservoir of novel resistance genes, including previously uncharacterized carbapenemases with the potential to spread further.

Electronic supplementary material

The online version of this article (10.1186/s40168-019-0710-x) contains supplementary material, which is available to authorized users.

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The comprehensive antibiotic resistance database.

Andrew McArthur, Nicholas Waglechner, Fazmin Nizam … (2013)

The field of antibiotic drug discovery and the monitoring of new antibiotic resistance elements have yet to fully exploit the power of the genome revolution. Despite the fact that the first genomes sequenced of free living organisms were those of bacteria, there have been few specialized bioinformatic tools developed to mine the growing amount of genomic data associated with pathogens. In particular, there are few tools to study the genetics and genomics of antibiotic resistance and how it impacts bacterial populations, ecology, and the clinic. We have initiated development of such tools in the form of the Comprehensive Antibiotic Research Database (CARD; http://arpcard.mcmaster.ca). The CARD integrates disparate molecular and sequence data, provides a unique organizing principle in the form of the Antibiotic Resistance Ontology (ARO), and can quickly identify putative antibiotic resistance genes in new unannotated genome sequences. This unique platform provides an informatic tool that bridges antibiotic resistance concerns in health care, agriculture, and the environment.

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Bacterial phylogeny structures soil resistomes across habitats

Kevin J. Forsberg, Sanket Patel, Molly Gibson … (2014)

Summary Ancient and diverse antibiotic resistance genes (ARGs) have previously been identified from soil 1–3 , including genes identical to those in human pathogens 4 . Despite the apparent overlap between soil and clinical resistomes 4–6 , factors influencing ARG composition in soil and their movement between genomes and habitats remain largely unknown 3 . General metagenome functions often correlate with the underlying structure of bacterial communities 7–12 . However, ARGs are hypothesized to be highly mobile 4,5,13 , prompting speculation that resistomes may not correlate with phylogenetic signatures or ecological divisions 13,14 . To investigate these relationships, we performed functional metagenomic selections for resistance to 18 antibiotics from 18 agricultural and grassland soils. The 2895 ARGs we discovered were predominantly novel, and represent all major resistance mechanisms 15 . We demonstrate that distinct soil types harbor distinct resistomes, and that nitrogen fertilizer amendments strongly influenced soil ARG content. Resistome composition also correlated with microbial phylogenetic and taxonomic structure, both across and within soil types. Consistent with this strong correlation, mobility elements syntenic with ARGs were rare in soil compared to sequenced pathogens, suggesting that ARGs in the soil may not transfer between bacteria as readily as is observed in the clinic. Together, our results indicate that bacterial community composition is the primary determinant of soil ARG content, challenging previous hypotheses that horizontal gene transfer effectively decouples resistomes from phylogeny 13,14 .

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Acinetobacter baumannii: evolution of a global pathogen

Luísa C.S. Antunes, Paolo Visca, Kevin Towner (2014)

Acinetobacter baumannii is an opportunistic nosocomial pathogen and one of the six most important multidrug-resistant microorganisms in hospitals worldwide. This human pathogen is responsible for a vast array of infections, of which ventilator-associated pneumonia and bloodstream infections are the most common, and mortality rates can reach 35%. Community-acquired infections have also been reported, but few strains have been recovered from environmental sources and infection reservoirs external to the hospital have not been identified. The majority of A. baumannii infections are caused by two main population clones with worldwide distribution. Infection outbreaks are often associated with multidrug resistance, including the recent emergence of strains resistant to all available antibiotics. Nevertheless, A. baumannii virulence traits and pathogenic potential have mostly remained elusive. The recent expansion of A. baumannii sequenced genomes has permitted the development of large-array phylogenomic and phenotypic analyses, which can offer valuable insights into the evolution and adaptation of A. baumannii as a human pathogen. This review summarises these recent advances, with particular focus on A. baumannii evolutionary and genomic aspects, and proposes new avenues of research. © 2013 Federation of European Microbiological Societies. Published by John Wiley & Sons Ltd. All rights reserved.

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Author and article information

Contributors

D. G. Joakim Larsson: +46-31-3424625 , joakim.larsson@fysiologi.gu.se

Journal

Journal ID (nlm-ta): Microbiome

Journal ID (iso-abbrev): Microbiome

Title: Microbiome

Publisher: BioMed Central (London )

ISSN (Electronic): 2049-2618

Publication date (Electronic): 27 June 2019

Publication date PMC-release: 27 June 2019

Publication date Collection: 2019

Volume: 7

Electronic Location Identifier: 97

Affiliations

[1 ]ISNI 0000 0000 9919 9582, GRID grid.8761.8, Centre for Antibiotic Resistance Research (CARe), , University of Gothenburg, ; Gothenburg, Sweden

[2 ]ISNI 0000 0000 9919 9582, GRID grid.8761.8, Department of Infectious Diseases, Institute of Biomedicine, Sahlgrenska Academy, , University of Gothenburg, ; Gothenburg, Sweden

[3 ]ISNI 0000 0004 0427 3161, GRID grid.10917.3e, Institute of Marine Research (IMR), ; Bergen, Norway

[4 ]ISNI 0000 0001 0775 6028, GRID grid.5371.0, Department of Mathematical Sciences, , Chalmers University of Technology and University of Gothenburg, ; Gothenburg, Sweden

[5 ]ISNI 0000 0001 0681 2788, GRID grid.467701.3, Plant Health and Environment Laboratory (PHEL), , Ministry for Primary Industries (MPI), ; Auckland, New Zealand

[6 ]Mahatma Gandhi Mission medical college, Navi Mumbai, Maharashtra India

Article

Publisher ID: 710

DOI: 10.1186/s40168-019-0710-x

PMC ID: 6598227

PubMed ID: 31248462

SO-VID: 4d846f33-ebbd-4c65-893d-14b1365beb2b

License:

Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License ( http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver ( http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

History

Date received : 11 February 2019

Date accepted : 5 June 2019

Funding

Funded by: FundRef http://dx.doi.org/10.13039/501100001862, Svenska Forskningsrådet Formas;

Award ID: 2012-86

Award Recipient : D. G. Joakim Larsson

Funded by: FundRef http://dx.doi.org/10.13039/501100004359, Vetenskapsrådet;

Custom metadata

Keywords: antibiotic resistance,hospital effluent,carbapenemase,pathogens,hidden markov model,india

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Keywords: antibiotic resistance, hospital effluent, carbapenemase, pathogens, hidden markov model, india

Sewage effluent from an Indian hospital harbors novel carbapenemases and integron-borne antibiotic resistance genes

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Abstract

Background

Results

Conclusion

Electronic supplementary material

Related collections

Tick microbiome

Most cited references 50

The comprehensive antibiotic resistance database.

Bacterial phylogeny structures soil resistomes across habitats

Acinetobacter baumannii: evolution of a global pathogen

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Contributors

Journal

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Article

History

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