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Deciphering the Crosswalk Dimension of Antibiotic Resistance between Different Reservoirs

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A special issue of Microorganisms (ISSN 2076-2607).

Deadline for manuscript submissions: closed (31 July 2020) | Viewed by 23186

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Dr. Manuela Caniça

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Laboratory of Antibiotic Resistances and Health Associated Infections, Department of Infectious Diseases, National Institute of Health Dr. Ricardo Jorge, Lisbon, Portugal
Interests: AMR mechanisms; AMR gene dissemination; genome background of AMR genes; genetic diversity; resistome; mobilome; prevent and overcoming AMR; One Health in the context of AMR
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Special Issue Information

Dear Colleagues,

Different reservoirs play a crucial role in the spread of antibiotic resistance. This is the main topic of the present Special Issue. In fact, human food of animal and vegetable origin, food-, companion-, wild-, and zoo-animals, as well as soil, air, and aquatic environment are hotspots for antibiotic resistance. The extent of the relationship between the occurrences of antibiotic-resistant bacteria and pathogens in those reservoirs should be better clarified. How resistant bacteria in the environment can offer barriers and/or opportunities for antimicrobial drug discovery is also a relevant issue today. Biofilm formation, namely in the food chain, as well as non-expressing bacteria that stay susceptible to the antibiotics although carrying potentially transmissible resistance genes, and proteins providing resistance to two structurally and functionally different classes of antibiotics by acquisition of a single gene are all interesting dimensions in the microbial adaptability, implicating the performance of antibiotics in several reservoirs. The role of vertical and horizontal gene transfer (HGT) of antibiotic resistance needs to be deepened; this HGT either directly through contact or indirectly through the different niches (people, animals, and environment) is assuming serious proportions. The responsibility of harmonization of phenotypic and genotypic methods and the implementation of guidelines is of utmost interest, namely, to measure the fitness cost of antibiotic resistance and to predict and/or decipher the real impact of this threat. How coordinated the human, veterinary, and environment sectors are/must be to prevent the spread of antibiotic resistance is also an important subtopic (such as the antibiotic consumption in all sectors). Studies regarding the “One Health” approach in the context of antibiotic resistance will be highly appreciated, as addressing emerging infectious diseases emphasizes how the health of humans is connected to the health of animals and their shared environment. These different micro- and macroscientific views of antibiotic resistance might help to decipher the problem of antibiotic resistance for times to come.

In this Special Issue, we invite you to submit contributions to the above subtopics in the form of original research articles or reviews, aiming to highlight the most current state of the art in those fields.

Prof. Dr. Manuela Canica
Guest Editor

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Keywords

antibiotic resistance
antibiotics
resistome
mobilome
metagenome
reservoirs
dissemination
ecological dimension
"omic" approaches

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Published Papers (7 papers)

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18 pages, 2708 KiB

Open AccessArticle

Temporal Resistome and Microbial Community Dynamics in an Intensive Aquaculture Facility with Prophylactic Antimicrobial Treatment

by Hemant J. Patil, Joao Gatica, Avihai Zolti, Ayana Benet-Perelberg, Alon Naor, Barak Dror, Ashraf Al Ashhab, Sophi Marman, Nur A. Hasan, Rita R. Colwell, Daniel Sher, Dror Minz and Eddie Cytryn

Microorganisms 2020, 8(12), 1984; https://doi.org/10.3390/microorganisms8121984 - 13 Dec 2020

Cited by 12 | Viewed by 3202

Abstract

Excessive use of antimicrobials in aquaculture is concerning, given possible environmental ramifications and the potential contribution to the spread of antimicrobial resistance (AR). In this study, we explored seasonal abundance of antimicrobial resistance genes and bacterial community composition in the water column of an intensive aquaculture pond stocked with Silver Carp (Hypophthalmichthys molitrix) prophylactically treated with sulfamethoprim (25% sulfadiazine; 5% trimethoprim), relative to an adjacent unstocked reservoir. Bacterial community composition was monitored using high-throughput sequencing of 16S rRNA gene amplicons in eight sampling profiles to determine seasonal dynamics, representing principal stages in the fish fattening cycle. In tandem, qPCR was applied to assess relative abundance of selected antimicrobial resistance genes (sul1, sul2, dfrA1, tetA and blaTEM) and class-1 integrons (int1). Concomitantly, resistomes were extrapolated from shotgun metagenomes in representative profiles. Analyses revealed increased relative abundance of sulfonamide and tetracycline resistance genes in fishpond-03, relative to pre-stocking and reservoir levels, whereas no significant differences were observed for genes encoding resistance to antimicrobials that were not used in the fishpond-03. Seasons strongly dictated bacterial community composition, with high abundance of cyanobacteria in summer and increased relative abundance of Flavobacterium in the winter. Our results indicate that prophylactic use of sulfonamides in intensive aquaculture ponds facilitates resistance suggesting that prophylactic use of these antimicrobials in aquaculture should be restricted. Full article

(This article belongs to the Special Issue Deciphering the Crosswalk Dimension of Antibiotic Resistance between Different Reservoirs)

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12 pages, 263 KiB

Open AccessArticle

High Colonization Rate and Heterogeneity of ESBL- and Carbapenemase-Producing Enterobacteriaceae Isolated from Gull Feces in Lisbon, Portugal

by Marta Aires-de-Sousa, Claudine Fournier, Elizeth Lopes, Hermínia de Lencastre, Patrice Nordmann and Laurent Poirel

Microorganisms 2020, 8(10), 1487; https://doi.org/10.3390/microorganisms8101487 - 28 Sep 2020

Cited by 13 | Viewed by 2549

Abstract

In order to evaluate whether seagulls living on the Lisbon coastline, Portugal, might be colonized and consequently represent potential spreaders of multidrug-resistant bacteria, a total of 88 gull fecal samples were screened for detection of extended-spectrum β-lactamase (ESBL)- or carbapenemase-producing Enterobacteriaceae for methicillin-resistant Staphylococcus aureus (MRSA) and for vancomycin-resistant Enterococci (VRE). A large proportion of samples yielded carbapenemase- or ESBL-producing Enterobacteriaceae (16% and 55%, respectively), while only two MRSA and two VRE were detected. Mating-out assays followed by PCR and whole-plasmid sequencing allowed to identify carbapenemase and ESBL encoding genes. Among 24 carbapenemase-producing isolates, there were mainly Klebsiella pneumoniae (50%) and Escherichia coli (33%). OXA-181 was the most common carbapenemase identified (54%), followed by OXA-48 (25%) and KPC-2 (17%). Ten different ESBLs were found among 62 ESBL-producing isolates, mainly being CTX-M-type enzymes (87%). Co-occurrence in single samples of multiple ESBL- and carbapenemase producers belonging to different bacterial species was observed in some cases. Seagulls constitute an important source for spreading multidrug-resistant bacteria in the environment and their gut microbiota a formidable microenvironment for transfer of resistance genes within bacterial species. Full article

(This article belongs to the Special Issue Deciphering the Crosswalk Dimension of Antibiotic Resistance between Different Reservoirs)

15 pages, 683 KiB

Open AccessArticle

by Vanessa Salgueiro, Vera Manageiro, Narcisa M. Bandarra, Eugénia Ferreira, Lurdes Clemente and Manuela Caniça

Microorganisms 2020, 8(9), 1345; https://doi.org/10.3390/microorganisms8091345 - 3 Sep 2020

Cited by 18 | Viewed by 2852

Abstract

The main aim of this study was the characterization of antibiotic resistance mechanisms in 82 Staphylococcus aureus strains isolated from humans and animals. Antibiotic susceptibility testing was performed on all S. aureus isolates accordingly, and antibiotic-resistant genes were investigated by genotypic methods. The genetic diversity of S. aureus was studied through spa, multilocus sequence typing (MLST), and agr typing methods. The majority of S. aureus from human sources were resistant to cefoxitin (and harbor the mecA gene) and fluoroquinolones, whereas only four strains of S. aureus from animal sources revealed resistance to ciprofloxacin. In the set of S. aureus isolated from humans, the most frequent spa, MLST, and agr group were t032, ST22, and I, respectively. In strains from animal origin the most common spa, MLST, and agr group found were t2383, ST398, and III/not typable, respectively. S. aureus from humans and animals were identified either in clonal complexes CC5, CC30, and CC398, suggesting that they have the same putative founder in their evolution. Considering the three CCs encompassing strains from human and animal reservoirs with different spa-types, we can hypothesize that this might reflect an adaptation to different phylogenetic lineages in those reservoirs (host species) probably associated to genetic diversification of pre-existing strains. Full article

(This article belongs to the Special Issue Deciphering the Crosswalk Dimension of Antibiotic Resistance between Different Reservoirs)

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18 pages, 387 KiB

Open AccessArticle

Bacterial Diversity and Antibiotic Susceptibility of Sparus aurata from Aquaculture

by Vanessa Salgueiro, Vera Manageiro, Narcisa M. Bandarra, Lígia Reis, Eugénia Ferreira and Manuela Caniça

Microorganisms 2020, 8(9), 1343; https://doi.org/10.3390/microorganisms8091343 - 2 Sep 2020

Cited by 23 | Viewed by 4174

Abstract

In a world where the population continues to increase and the volume of fishing catches stagnates or even falls, the aquaculture sector has great growth potential. This study aimed to contribute to the depth of knowledge of the diversity of bacterial species found in Sparus aurata collected from a fish farm and to understand which profiles of diminished susceptibility to antibiotics would be found in these bacteria that might be disseminated in the environment. One hundred thirty-six bacterial strains were recovered from the S. aurata samples. These strains belonged to Bacillaceae, Bacillales Family XII. Incertae Sedis, Comamonadaceae, Enterobacteriaceae, Enterococcaceae, Erwiniaceae, Micrococcaceae, Pseudomonadaceae and Staphylococcaceae families. Enterobacter sp. was more frequently found in gills, intestine and skin groups than in muscle groups (p ≤ 0.01). Antibiotic susceptibility tests found that non-susceptibility to phenicols was significantly higher in gills, intestine and skin samples (45%) than in muscle samples (24%) (p ≤ 0.01) and was the most frequently found non-susceptibility in both groups of samples. The group of Enterobacteriaceae from muscles presented less decreased susceptibility to florfenicol (44%) than in the group of gills, intestine and skin samples (76%). We found decreased susceptibilities to β-lactams and glycopeptides in the Bacillaceae family, to quinolones and mupirocin in the Staphylococcaceae family, and mostly to β-lactams, phenicols and quinolones in the Enterobacteriaceae and Pseudomonadaceae families. Seven Enterobacter spp. and five Pseudomonas spp. strains showed non-susceptibility to ertapenem and meropenem, respectively, which is of concern because they are antibiotics used as a last resort in serious clinical infections. To our knowledge, this is the first description of species Exiguobacterium acetylicum, Klebsiella michiganensis, Lelliottia sp. and Pantoea vagans associated with S. aurata (excluding cases where these bacteria are used as probiotics) and of plasmid-mediated quinolone resistance qnrB19-producing Leclercia adecarboxylata strain. The non-synonymous G385T and C402A mutations at parC gene (within quinolone resistance-determining regions) were also identified in a Klebsiella pneumoniae, revealing decreased susceptibility to ciprofloxacin. In this study, we found not only bacteria from the natural microbiota of fish but also pathogenic bacteria associated with fish and humans. Several antibiotics for which decreased susceptibility was found here are integrated into the World Health Organization list of “critically important antimicrobials” and “highly important antimicrobials” for human medicine. Full article

(This article belongs to the Special Issue Deciphering the Crosswalk Dimension of Antibiotic Resistance between Different Reservoirs)

12 pages, 290 KiB

Open AccessArticle

Frequency and Characterization of Antimicrobial Resistance and Virulence Genes of Coagulase-Negative Staphylococci from Wild Birds in Spain. Detection of tst-Carrying S. sciuri Isolates

by Laura Ruiz-Ripa, Paula Gómez, Carla Andrea Alonso, María Cruz Camacho, Yolanda Ramiro, Javier de la Puente, Rosa Fernández-Fernández, Miguel Ángel Quevedo, Juan Manuel Blanco, Gerardo Báguena, Myriam Zarazaga, Ursula Höfle and Carmen Torres

Microorganisms 2020, 8(9), 1317; https://doi.org/10.3390/microorganisms8091317 - 29 Aug 2020

Cited by 26 | Viewed by 3329

Abstract

The objective of this study was to determine the prevalence and diversity of coagulase-negative staphylococci (CoNS) species from wild birds in Spain, as well as to analyze the antimicrobial resistance phenotype/genotype and the virulence gene content. During 2015–2016, tracheal samples of 242 wild birds were collected in different regions of Spain for staphylococci recovery. The species identification was performed using MALDI-TOF. The antimicrobial resistance phenotype and genotype was investigated by the disk diffusion method and by PCR, respectively. The presence of the virulence genes lukF/S-PV, tst, eta, etb, etd and scn was investigated by PCR. Moreover, CoNS carrying the mecA gene were subjected to SCCmec typing. Of the tested animals, 60% were CoNS-carriers, and 173 CoNS isolates were recovered from the 146 positive animals, which belonged to 11 species, with predominance of S. sciuri (n = 118) and S. lentus (n = 25). A total of 34% of CoNS isolates showed a multidrug resistance phenotype, and 42 mecA-positive methicillin-resistant CoNS (MRCoNS) were detected. The isolates showed resistance to the following antimicrobials (percentage of resistant isolates/antimicrobial resistance genes detected): penicillin (49/ blaZ, mecA), cefoxitin (24/ mecA), erythromycin and/or clindamycin (92/ erm(B), erm(C), erm(43), msr(A), mph(C), lnu(A), lsa(B), vga(A) and sal(A)), gentamicin and/or tobramycin (5/ aac(6′)-Ie-aph(2″)-Ia, ant(4′)-Ia), streptomycin (12/str), tetracycline (17/ tet(K), tet(L), tet(M)), ciprofloxacin (4), chloramphenicol (1/ fexA), fusidic acid (86/ fusB, fusD) and trimethoprim–sulfamethoxazole (1/ dfrK). None of the isolates harbored the lukF/S-PV, eta, etb, etd and scn genes, but two S. sciuri isolates (1%) carried the tst gene. Wild birds are frequently colonized by CoNS species, especially S. sciuri. We identified scavenging on intensively produced livestock and feeding on landfills as risk factors for CoNS carriage. High proportions of MRCoNS and multidrug resistant CoNS were detected, which coupled with the presence of important virulence genes is of concern. Full article

(This article belongs to the Special Issue Deciphering the Crosswalk Dimension of Antibiotic Resistance between Different Reservoirs)

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13 pages, 1479 KiB

Open AccessArticle

Characteristics of Extended-Spectrum Beta-Lactamase-Producing Enterobacteriaceae and Contact to Animals in Estonia

by Kaidi Telling, Age Brauer, Mailis Laht, Piret Kalmus, Karolin Toompere, Veljo Kisand, Matti Maimets, Maido Remm, Tanel Tenson and Irja Lutsar

Microorganisms 2020, 8(8), 1130; https://doi.org/10.3390/microorganisms8081130 - 27 Jul 2020

Cited by 4 | Viewed by 3224

Abstract

We have attempted to define the prevalence and risk factors of extended-spectrum beta-lactamase-producing Enterobacteriaceae (ESBL-Enterobacteriaceae) carriage, and to characterize antimicrobial susceptibility, beta-lactamase genes, and major types of isolated strains in volunteers, with a specific focus on humans in contact with animals. Samples were collected from 207 volunteers (veterinarians, pig farmers, dog owners, etc.) and cultured on selective agar. Clonal relationships of the isolated ESBL-Enterobacteriaceae were determined by whole genome sequencing and multi-locus sequence typing. Beta-lactamases were detected using a homology search. Subjects filled in questionnaires analyzed by univariate and multiple logistic regression. Colonization with ESBL-Enterobacteriaceae was found in fecal samples of 14 individuals (6.8%; 95%CI: 3.75–11.09%). In multiple regression analysis, working as a pig farmer was a significant risk factor for ESBL-Enterobacteriaceae carriage (OR 4.8; 95%CI 1.2–19.1). The only species isolated was Escherichia coli that distributed into 11 sequence types. All ESBL-Enterobacteriaceae isolates were of CTX-M genotype, with the blaCTX-M-1 being the most prevalent and more common in pig farmers than in other groups. Despite the generally low prevalence of ESBL-Enterobacteriaceae in Estonia, the pig farmers may still pose a threat to transfer resistant microorganisms. The clinical relevance of predominant blaCTX-M-1 carrying E. coli is still unclear and needs further studies. Full article

(This article belongs to the Special Issue Deciphering the Crosswalk Dimension of Antibiotic Resistance between Different Reservoirs)

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7 pages, 396 KiB

Open AccessBrief Report

Plasmid-Mediated Colistin Resistance (mcr-1) in Escherichia coli from Non-Imported Fresh Vegetables for Human Consumption in Portugal

by Vera Manageiro, Daniela Jones-Dias, Eugénia Ferreira and Manuela Caniça

Microorganisms 2020, 8(3), 429; https://doi.org/10.3390/microorganisms8030429 - 18 Mar 2020

Cited by 15 | Viewed by 3074

Abstract

In this study, we report the presence of the plasmid-mediated colistin resistance (PMCR)-encoding gene mcr-1 in an Escherichia coli isolate, INSali25, recovered from lettuce produced and marketed in Portugal. Colistin MIC from the vegetable E. coli isolate—determined by microdilution broth method according to EUCAST guidelines—revealed a non-wild-type phenotype of colistin (MIC 16 mg/L). To understand the genetic background of E. coli INSali25, we performed whole genome sequencing. Plasmid sequencing was also performed after plasmid DNA extraction from the transconjugant TcINSali25 (mcr-1). Directed bioinformatics analysis identified the mcr-1 gene in a 39,998 bp length contig, with an upstream region including the antibiotic resistance gene bla_TEM-1 in a partial transposon Tn2, truncated by the insertion sequence IS26 and showing >99% identity with previously described mcr-1-harboring IncHI2 plasmids. Further in silico analysis showed the presence of additional genes conferring resistance to β-lactams (bla_TEM-1), aminoglycosides (aadA1, aph(4)-Ia, aph(6)-Id, aac(3)-Iv), macrolides (mdf(A)-type), phenicol (floR-type), tetracycline (tetA), and sulphonamides (sul2). INSali25 isolate belonged to the ST1716 lineage and showed the fimH54 and fumC27 alleles. Lettuce is a vegetable that is commonly consumed fresh and not subjected to any cooking process, which may amplify human food safety risks. Moreover, the occurrence of plasmid-mediated colistin resistance in a sample that was not imported and was acquired in a large retail store reinforces the widespread distribution of mcr-1. Full article

(This article belongs to the Special Issue Deciphering the Crosswalk Dimension of Antibiotic Resistance between Different Reservoirs)

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