Resistome in Lake Bolonha, Brazilian Amazon: Identification of Genes Related to Resistance to Broad-Spectrum Antibiotics

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Abstract

Resistance to antibiotics is one of the most relevant public health concerns in the world. Aquatic environments play an important role because they are reservoirs for antibiotic resistance genes and antibiotic-resistant strains, contributing to the spread of resistance. The present study investigated the resistome in Lake Bolonha (three sampling sites) in the Amazon region using a metagenomics approach and culture-dependent methods. Whole-metagenome-based results showed that the most abundant phyla were Protobacteria, Actinobacteria, Firmicutes, Bacteroidetes and Cyanobacteria. The composition of the resistome demonstrated that the genes that confer resistance to β-lactams were prevalent at all sampling sites, followed by genes conferring resistance to aminoglycosides and tetracycline. Acquired genes encoding extended-spectrum β-lactamases (e.g., bla _CTX–M) and resistance to carbapenems (e.g., bla _IMP and bla _VIM) were detected through metagenome analysis. Bacteria were isolated from culture medium supplemented with cefotaxime or imipenem, and isolates were identified and analyzed for their antibiotic susceptibility profiles and resistance genes. In total, 98 bacterial isolates belonging to the genera Pseudomonas (37), Acinetobacter (32), Klebsiella (13), Enterobacter (9), Pantoe (3), Stenotrophomonas (3), and Methylobacterium (1) were obtained. Among isolates, the most abundant genes were bla _CTX–M (28.3%), bla _SHV (22.6%) and bla _TEM (18.8%) in isolates from cefotaxime-supplemented medium and bla _VIM (28.8%) and bla _IMP (22.2%) in isolates recovered from imipenem-supplemented medium. The genes intl1 and intl2 were detected in 19.3% and 7.1% of isolates. Antibiograms showed that 94.9% (from cefotaxime-supplemented medium) and 85.7% (from imipenem-supplemented medium) of the isolates were multidrug resistant. Besides cefotaxime and imipenem, isolates were mostly resistant to aztreonam (91.8%), amoxicillin (98.8%), ampicillin (82.6%), and nalidixic acid (77.5%). Hence, the present study demonstrates that Lake Bolonha is a reservoir of bacteria resistant to antibiotics and resistance genes, some of which are of critical importance to human health.

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Most cited references 73

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Tetracycline antibiotics: mode of action, applications, molecular biology, and epidemiology of bacterial resistance.

Ian Chopra, Marilyn Roberts (2001)

Tetracyclines were discovered in the 1940s and exhibited activity against a wide range of microorganisms including gram-positive and gram-negative bacteria, chlamydiae, mycoplasmas, rickettsiae, and protozoan parasites. They are inexpensive antibiotics, which have been used extensively in the prophlylaxis and therapy of human and animal infections and also at subtherapeutic levels in animal feed as growth promoters. The first tetracycline-resistant bacterium, Shigella dysenteriae, was isolated in 1953. Tetracycline resistance now occurs in an increasing number of pathogenic, opportunistic, and commensal bacteria. The presence of tetracycline-resistant pathogens limits the use of these agents in treatment of disease. Tetracycline resistance is often due to the acquisition of new genes, which code for energy-dependent efflux of tetracyclines or for a protein that protects bacterial ribosomes from the action of tetracyclines. Many of these genes are associated with mobile plasmids or transposons and can be distinguished from each other using molecular methods including DNA-DNA hybridization with oligonucleotide probes and DNA sequencing. A limited number of bacteria acquire resistance by mutations, which alter the permeability of the outer membrane porins and/or lipopolysaccharides in the outer membrane, change the regulation of innate efflux systems, or alter the 16S rRNA. New tetracycline derivatives are being examined, although their role in treatment is not clear. Changing the use of tetracyclines in human and animal health as well as in food production is needed if we are to continue to use this class of broad-spectrum antimicrobials through the present century.

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Antibiotic resistance in the environment: a link to the clinic?

Gerard D. Wright (2010)

The emergence of resistance to all classes of antibiotics in previously susceptible bacterial pathogens is a major challenge to infectious disease medicine. The origin of the genes associated with resistance has long been a mystery. There is a growing body of evidence that is demonstrating that environmental microbes are highly drug resistant. The genes that make up this environmental resistome have the potential to be transferred to pathogens and indeed there is some evidence that at least some clinically relevant resistance genes have originated in environmental microbes. Understanding the extent of the environmental resistome and its mobilization into pathogenic bacteria is essential for the management and discovery of antibiotics. Copyright © 2010 Elsevier Ltd. All rights reserved.

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Sequence heterogeneities of genes encoding 16S rRNAs in Paenibacillus polymyxa detected by temperature gradient gel electrophoresis.

U Nübel, B. Engelen, A Felske … (1996)

Sequence heterogeneities in 16S rRNA genes from individual strains of Paenibacillus polymyxa were detected by sequence-dependent separation of PCR products by temperature gradient gel electrophoresis (TGGE). A fragment of the 16S rRNA genes, comprising variable regions V6 to V8, was used as a target sequence for amplifications. PCR products from P. polymyxa (type strain) emerged as a well-defined pattern of bands in the gradient gel. Six plasmids with different inserts, individually demonstrating the migration characteristics of single bands of the pattern, were obtained by cloning the PCR products. Their sequences were analyzed as a representative sample of the total heterogeneity. An amount of 10 variant nucleotide positions in the fragment of 347 bp was observed, with all substitutions conserving the relevant secondary structures of the V6 and V8 regions in the RNA molecules. Hybridizations with specifically designed probes demonstrated different chromosomal locations of the respective rRNA genes. Amplifications of reverse-transcribed rRNA from ribosome preparations, as well as whole-cell hybridizations, revealed a predominant representation of particular sequences in ribosomes of exponentially growing laboratory cultures. Different strains of P. polymyxa showed not only remarkably differing patterns of PCR products in TGGE analysis but also discriminative whole-cell labeling with the designed oligonucleotide probes, indicating the different representation of individual sequences in active ribosomes. Our results demonstrate the usefulness of TGGE for the structural analysis of heterogeneous rRNA genes together with their expression, stress problems of the generation of meaningful data for 16S rRNA sequences and probe designs, and might have consequences for evolutionary concepts.

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Author and article information

Contributors

Jorianne Alves: URI : http://loop.frontiersin.org/people/778339/overview

Jackeline Mateus: URI : http://loop.frontiersin.org/people/755846/overview

Diego Graças: URI : http://loop.frontiersin.org/people/604871/overview

Rommel Ramos: URI : http://loop.frontiersin.org/people/425394/overview

Lucy Seldin: URI : http://loop.frontiersin.org/people/252277/overview

Isabel Henriques: URI : http://loop.frontiersin.org/people/58460/overview

Artur Silva: URI : http://loop.frontiersin.org/people/891870/overview

Adriana Folador: URI : http://loop.frontiersin.org/people/534845/overview

Journal

Journal ID (nlm-ta): Front Microbiol

Journal ID (iso-abbrev): Front Microbiol

Journal ID (publisher-id): Front. Microbiol.

Title: Frontiers in Microbiology

Publisher: Frontiers Media S.A.

ISSN (Electronic): 1664-302X

Publication date (Electronic): 04 February 2020

Publication date Collection: 2020

Volume: 11

Electronic Location Identifier: 67

Affiliations

[1] ¹Laboratório de Genômica e Bioinformática, Centro De Genômica e Biologia de Sistemas, Universidade Federal Do Pará , Belém, Brazil

[2] ²Instituto de Microbiologia Paulo de Góes, Universidade Federal do Rio de Janeiro , Rio de Janeiro, Brazil

[3] ³Center for Environmental and Marine Studies (CESAM), University of Aveiro , Aveiro, Portugal

[4] ⁴Department of Life Sciences, Faculty of Science and Technology, University of Coimbra , Coimbra, Portugal

Author notes

Edited by: Xian-Zhi Li, Health Canada, Canada

Reviewed by: Benjamin Andrew Evans, University of East Anglia, United Kingdom; Indranil Samanta, West Bengal University of Animal and Fishery Sciences, India

*Correspondence: Adriana Folador, arcarneiro@ 123456ufpa.br ; carneiroar@ 123456gmail.com

This article was submitted to Antimicrobials, Resistance and Chemotherapy, a section of the journal Frontiers in Microbiology

Article

DOI: 10.3389/fmicb.2020.00067

PMC ID: 7010645

PubMed ID: 32117110

SO-VID: 3c903e60-24c8-4b9c-a400-1aabfbd0905a

License:

This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

History

Date received : 18 April 2019

Date accepted : 14 January 2020

Page count

Figures: 6, Tables: 2, Equations: 0, References: 88, Pages: 13, Words: 0

Funding

Funded by: Conselho Nacional de Desenvolvimento Científico e Tecnológico 10.13039/501100003593

Funded by: Coordenação de Aperfeiçoamento de Pessoal de Nível Superior 10.13039/501100002322

Funded by: Centro de Estudos Ambientais e Marinhos, Universidade de Aveiro 10.13039/100013239

Resistome in Lake Bolonha, Brazilian Amazon: Identification of Genes Related to Resistance to Broad-Spectrum Antibiotics

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Microbial Genomics

Most cited references 73

Tetracycline antibiotics: mode of action, applications, molecular biology, and epidemiology of bacterial resistance.

Antibiotic resistance in the environment: a link to the clinic?

Sequence heterogeneities of genes encoding 16S rRNAs in Paenibacillus polymyxa detected by temperature gradient gel electrophoresis.

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