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. 2020 Feb 4:11:67.
doi: 10.3389/fmicb.2020.00067. eCollection 2020.

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

Jorianne Alves  1 , Larissa Dias  1 , Jackeline Mateus  2 , Joana Marques  1 , Diego Graças  1 , Rommel Ramos  1 , Lucy Seldin  2 , Isabel Henriques  3   4 , Artur Silva  1 , Adriana Folador  1
Affiliations

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

Jorianne Alves et al. Front Microbiol. .

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.

Keywords: Lake Bolonha; bacteria resistant to antibiotics; metagenome; resistome; β-lactams.

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Figures

FIGURE 1
FIGURE 1
Map of Lake Bolonha with the sampling sites marked.
FIGURE 2
FIGURE 2
Principal component analysis (PCA) score plot of each replicate at each collection site. The replicates of the same site group together and each site’s grouping was different from the others among the three sampling sites. Blue: the replicates of site P1; red: the replicates of site P2; and green: the replicates of site P3.
FIGURE 3
FIGURE 3
Relative abundance of reads affiliated with domains (A), bacterial phyla (B), Proteobacteria classes (C) and Firmicutes classes (D) at the three sites (P1, P2, and P3).
FIGURE 4
FIGURE 4
Classification of metagenomic data obtained from sites P1, P2, and P3 in subsystems according to MG-RAST.
FIGURE 5
FIGURE 5
Distribution of the genes conferring resistance to different classes of antibiotics identified by comparison with the CARD database at sites P1, P2, and P3.
FIGURE 6
FIGURE 6
Incidence of resistance to antibiotics among isolates. Amoxicillin (AMX), amoxicillin/clavulanic acid (AMC), ampicillin (AMP), ceftazidime (CAZ), cephalothin (CEF), cefotaxime (CTX), cefepime (FEP), imipenem (IMP), ciprofloxacin (CIP), gentamicin (GEN), chloramphenicol (CHL), sulfamethoxazole/trimethoprim (SXT), kanamycin (KAN), aztreonam (ATM), nalidixic acid (NAL), and tetracycline (TET).
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