Multidrug-Resistant Bacteria in the Environment, Their Resistance and Transfer Mechanisms

A special issue of Microorganisms (ISSN 2076-2607). This special issue belongs to the section "Antimicrobial Agents and Resistance".

Deadline for manuscript submissions: closed (31 October 2022) | Viewed by 25152

Special Issue Editors


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Guest Editor
School of Life Sciences and Technology, Beuth University of Applied Sciences Berlin, Berlin, Germany
Interests: conjugative plasmid transfer mechanism; plasmids; type IV secretion systems; Enterococcus; antibiotic resistance; biofilm inhibition; antimicrobial surfaces; molecular ecology of antibiotic resistance

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Guest Editor
Federal Research Centre for Cultivated Plants (JKI), Institute for Epidemiology and Pathogen Diagnostics, Messeweg 11-12, 38104 Braunschweig, Germany
Interests: bacterial pathogens; interaction of antagonists; pathogens and microbial communities in the rhizosphere; ecology of bacterial antibiotic resistance genes

Special Issue Information

Dear Colleagues,

Antibiotic-resistant bacteria (ARB) were found in the environment long before antibiotics were used by humans, e.g., antibiotics producers protecting themselves against their own antibiotics. Thus, one must clearly differentiate between this intrinsic environmental resistome and the acquired transferable resistome whose increasing abundance is a big concern as it can largely affect the health of humans and animals. Following the One Health approach, it is of primordial importance to monitor and control the release of selecting and co-selecting pollutants (antibiotics, heavy metals, and disinfectants), ARB, and their antibiotic resistance genes (ARGs) from hospitals, nursing homes, animal clinics, and industrial livestock farming into the environment via the release of wastewater (treated, partially treated, non-treated) into surface waters and soils.

In addition, organic wastewater solids (biosolids) are not only valuable organic fertilizers having numerous beneficial effects on soil characteristics—they are also recognized as one of the main anthropogenic sources of chemical pollutants, ARGs, and mobile genetic elements (MGEs) in agricultural soil. Thus, biosolids and partially treated irrigation water cannot only contribute to changes in the soil microbial community composition but also to increased ARG loads and, likely, to their persistence and dissemination via co-selection when applied to soils. Due to the presence of microbial communities, originating from different sources, together with selective compounds and a high nutrient availability, facilitating metabolic activities and high cell densities, wastewater treatment plants are regarded as hot spots of horizontal gene transfer (HGT), and therefore, biosolids are an important potential transfer gateway between clinical and environmental bacteria.

The concentration of ARB and ARGs released into the environment is not controlled in any case. When ARB, like multi-drug resistant (MDR) pathogens, arrive in the environment, they compete with the indigenous microbiome. Even if they are outcompeted by the autochthonous microbial communities and do not survive, however, they still spread their ARGs to environmental microbes, thereby generating MDR bacteria. These can contaminate crops and are eventually taken up by crops. Thus, there is an urgent need to monitor the release of ARGs on one hand and to assess their transferability in the environment on the other hand to enable appropriate countermeasures.

This Special Issue is open to any high-quality research dealing with:

-Following the path of ARGs and ARB from hospitals, nursing homes, intensive animal husbandry, and municipal wastewater treatment plants to the environment and/or the way back;

-The mechanisms of spread of ARGs and ARB in the environment (mainly focusing on soils and plants);

-The quantification of horizontal gene transfer (HGT) of ARGs in the environment, including the design and application of new methods for quantitative monitoring of ARG transfer on one hand and identification of hot spots of ARG transfer on the other hand.

Prof. Dr. Elisabeth Grohmann
Prof. Dr. Kornelia Smalla
Guest Editors

Manuscript Submission Information

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Please visit the Instructions for Authors page before submitting a manuscript. The Article Processing Charge (APC) for publication in this open access journal is 2700 CHF (Swiss Francs). Submitted papers should be well formatted and use good English. Authors may use MDPI's English editing service prior to publication or during author revisions.

Keywords

  • multidrug resistance
  • antibiotic resistance genes (ARGs)
  • antibiotic resistant bacteria (ARB)
  • One Health approach
  • environment
  • wastewater treatment plants
  • pollutant release
  • biosolids
  • co-selection
  • mobile genetic elements (MGE)
  • ARG/ARB uptake by plants
  • horizontal gene transfer (HGT) of ARGs
  • antibiotic resistance transfer mechanisms
  • antibiotic resistance transfer monitoring
  • risk assessment

Published Papers (9 papers)

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Editorial

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3 pages, 194 KiB  
Editorial
Special Issue “Multidrug-Resistant Bacteria in the Environment, Their Resistance and Transfer Mechanisms”
by Elisabeth Grohmann
Microorganisms 2023, 11(4), 981; https://0-doi-org.brum.beds.ac.uk/10.3390/microorganisms11040981 - 10 Apr 2023
Viewed by 1047
Abstract
Multidrug-resistant bacteria are an emerging issue which is not restricted to clinics and the health care sector, but is increasingly affecting the environment [...] Full article

Research

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25 pages, 1298 KiB  
Article
Analysis of Whole-Genome Sequences of Pathogenic Gram-Positive and Gram-Negative Isolates from the Same Hospital Environment to Investigate Common Evolutionary Trends Associated with Horizontal Gene Exchange, Mutations and DNA Methylation Patterning
by Ilya S. Korotetskiy, Sergey V. Shilov, Tatyana Kuznetsova, Bahkytzhan Kerimzhanova, Nadezhda Korotetskaya, Lyudmila Ivanova, Natalya Zubenko, Raikhan Parenova and Oleg N. Reva
Microorganisms 2023, 11(2), 323; https://0-doi-org.brum.beds.ac.uk/10.3390/microorganisms11020323 - 27 Jan 2023
Cited by 4 | Viewed by 2098
Abstract
Hospital-acquired infections are a generally recognized problem for healthcare professionals. Clinical variants of Gram-negative and Gram-positive pathogens are characterized with enhanced antibiotic resistance and virulence due to mutations and the horizontal acquisition of respective genetic determinants. In this study, two Escherichia coli, two [...] Read more.
Hospital-acquired infections are a generally recognized problem for healthcare professionals. Clinical variants of Gram-negative and Gram-positive pathogens are characterized with enhanced antibiotic resistance and virulence due to mutations and the horizontal acquisition of respective genetic determinants. In this study, two Escherichia coli, two Klebsiella pneumoniae, three Pseudomonas aeruginosa, two Staphylococcus aureus, one Staphylococcus epidermidis and one Streptococcus pneumoniae showing broad spectra of antibiotic resistance were isolated from patients suffering from nosocomial infections in a local hospital in Almaty, Kazakhstan. The aim of the study was to compare general and species-specific pathways of the development of virulence and antibiotic resistance through opportunistic pathogens causing hospital-acquired infections. The whole-genome PacBio sequencing of the isolates allowed for the genotyping and identification of antibiotic resistance and virulence genetic determinants located in the chromosomes, plasmids and genomic islands. It was concluded that long-read sequencing is a useful tool for monitoring the epidemiological situation in hospitals. Marker antibiotic resistance mutations common for different microorganisms were identified, which were acquired due to antibiotic-selective pressure in the same clinical environment. The genotyping and identification of strain-specific DNA methylation motifs were found to be promising in estimating the risks associated with hospital infection outbreaks and monitoring the distribution and evolution of nosocomial pathogens. Full article
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13 pages, 1558 KiB  
Communication
Fate of Horizontal-Gene-Transfer Markers and Beta-Lactamase Genes during Thermophilic Composting of Human Excreta
by Katharina A. Werner, Lara Feyen, Tobias Hübner, Nicolas Brüggemann, Katharina Prost and Elisabeth Grohmann
Microorganisms 2023, 11(2), 308; https://doi.org/10.3390/microorganisms11020308 - 24 Jan 2023
Cited by 1 | Viewed by 1370
Abstract
Thermophilic composting is a suitable treatment for the recycling of organic wastes for agriculture. However, using human excreta as feedstock for composting raises concerns about antibiotic resistances. We analyzed samples from the start and end of a thermophilic composting trial of human excreta, [...] Read more.
Thermophilic composting is a suitable treatment for the recycling of organic wastes for agriculture. However, using human excreta as feedstock for composting raises concerns about antibiotic resistances. We analyzed samples from the start and end of a thermophilic composting trial of human excreta, together with green cuttings and straw, with and without biochar. Beta-lactamase genes blaCTX-M, blaIMP, and blaTEM conferring resistance to broad-spectrum beta-lactam antibiotics, as well as horizontal gene transfer marker genes, intI1 and korB, were quantified using qPCR. We found low concentrations of the beta-lactamase genes in all samples, with non-significant mean decreases in blaCTX-M and blaTEM copy numbers and a mean increase in blaIMP copy numbers. The decrease in both intI1 and korB genes from start to end of composting indicated that thermophilic composting can decrease the horizontal spread of resistance genes. Thus, thermophilic composting can be a suitable treatment for the recycling of human excreta. Full article
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19 pages, 2693 KiB  
Article
Impact of Swine and Cattle Manure Treatment on the Microbial Composition and Resistome of Soil and Drainage Water
by Phil Colgan, Elizabeth L. Rieke, Khurram Nadeem, Thomas B. Moorman, Michelle L. Soupir, Adina Howe and Nicole Ricker
Microorganisms 2023, 11(1), 17; https://0-doi-org.brum.beds.ac.uk/10.3390/microorganisms11010017 - 21 Dec 2022
Cited by 5 | Viewed by 1657
Abstract
Evaluating potential environmental and clinical impacts of industrial antibiotic use is critical in mitigating the spread of antimicrobial resistance. Using soil columns to simulate field application of swine or cattle manure and subsequent rain events, and a targeted qPCR-based approach, we tracked resistance [...] Read more.
Evaluating potential environmental and clinical impacts of industrial antibiotic use is critical in mitigating the spread of antimicrobial resistance. Using soil columns to simulate field application of swine or cattle manure and subsequent rain events, and a targeted qPCR-based approach, we tracked resistance genes from source manures and identified important differences in antimicrobial resistance gene transport and enrichment over time in the soil and water of artificially drained cropland. The source manures had distinct microbial community and resistance gene profiles, and these differences were also reflected in the soil columns after manure application. Antibiotic resistance genes (ARGs) were only significantly enriched in effluent samples following the first rain event (day 11) for both soil types compared to the control columns, illustrating the high background level of resistance present in the control soils chosen. For swine, the genes tetQ, tet(36), tet44, tetM, sul2 and ant(6)-ib persisted in the soil columns, whereas tetO, strB and sul1 persisted in effluent samples. Conversely, for cattle manure sul2 and strB persisted in both soil and effluent. The distinct temporal dynamics of ARG distribution between soil and effluent water for each manure type can be used to inform potential mitigation strategies in the future. Full article
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13 pages, 2392 KiB  
Article
Insights into the Bacterial Diversity and Detection of Opportunistic Pathogens in Mexican Chili Powder
by Yoali Fernanda Hernández Gómez, Jacqueline González Espinosa, Miguel Ángel Ramos López, Jackeline Lizzeta Arvizu Gómez, Carlos Saldaña, José Alberto Rodríguez Morales, María Carlota García Gutiérrez, Victor Pérez Moreno, Erika Álvarez Hidalgo, Jorge Nuñez Ramírez, George H. Jones, José Luis Hernández Flores and Juan Campos Guillén
Microorganisms 2022, 10(8), 1677; https://0-doi-org.brum.beds.ac.uk/10.3390/microorganisms10081677 - 20 Aug 2022
Cited by 4 | Viewed by 2449
Abstract
Chili powder is the most frequently consumed spice in Mexican diets. Thus, the dissemination of microorganisms associated with chili powder derived from Capsicum annuum L. is significant during microbial quality analysis, with special attention on detection of potential pathogens. The results presented here [...] Read more.
Chili powder is the most frequently consumed spice in Mexican diets. Thus, the dissemination of microorganisms associated with chili powder derived from Capsicum annuum L. is significant during microbial quality analysis, with special attention on detection of potential pathogens. The results presented here describe the initial characterization of bacterial community structure in commercial chili powder samples. Our results demonstrate that, within the domain Bacteria, the most abundant family was Bacillaceae, with a relative abundance of 99% in 71.4% of chili powder samples, while 28.6% of samples showed an average relative abundance of 60% for the Enterobacteriaceae family. Bacterial load for aerobic mesophilic bacteria (AMB) ranged from 104 to 106 cfu/g, while for sporulated mesophilic bacteria (SMB), the count ranged from 102 to 105 cfu/g. Bacillus cereus sensu lato (s.l.) was observed at ca. ˂600 cfu/g, while the count for Enterobacteriaceae ranged from 103 to 106 cfu/g, Escherichia coli and Salmonella were not detected. Fungal and yeast counts ranged from 102 to 105 cfu/g. Further analysis of the opportunistic pathogens isolated, such as B. cereus s.l. and Kosakonia cowanii, using antibiotic-resistance profiles and toxinogenic characteristics, revealed the presence of extended-spectrum β-lactamases (ESBLs) and Metallo-β-lactamases (MBLs) in these organisms. These results extend our knowledge of bacterial diversity and the presence of opportunistic pathogens associated with Mexican chili powder and highlight the potential health risks posed by its use through the spread of antibiotic-resistance and the production of various toxins. Our findings may be useful in developing procedures for microbial control during chili powder production. Full article
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17 pages, 1529 KiB  
Article
Genome-Wide Association Study Reveals Host Factors Affecting Conjugation in Escherichia coli
by Laetitia Van Wonterghem, Matteo De Chiara, Gianni Liti, Jonas Warringer, Anne Farewell, Natalie Verstraeten and Jan Michiels
Microorganisms 2022, 10(3), 608; https://0-doi-org.brum.beds.ac.uk/10.3390/microorganisms10030608 - 12 Mar 2022
Cited by 3 | Viewed by 3702
Abstract
The emergence and dissemination of antibiotic resistance threaten the treatment of common bacterial infections. Resistance genes are often encoded on conjugative elements, which can be horizontally transferred to diverse bacteria. In order to delay conjugative transfer of resistance genes, more information is needed [...] Read more.
The emergence and dissemination of antibiotic resistance threaten the treatment of common bacterial infections. Resistance genes are often encoded on conjugative elements, which can be horizontally transferred to diverse bacteria. In order to delay conjugative transfer of resistance genes, more information is needed on the genetic determinants promoting conjugation. Here, we focus on which bacterial host factors in the donor assist transfer of conjugative plasmids. We introduced the broad-host-range plasmid pKJK10 into a diverse collection of 113 Escherichia coli strains and measured by flow cytometry how effectively each strain transfers its plasmid to a fixed E. coli recipient. Differences in conjugation efficiency of up to 2.7 and 3.8 orders of magnitude were observed after mating for 24 h and 48 h, respectively. These differences were linked to the underlying donor strain genetic variants in genome-wide association studies, thereby identifying candidate genes involved in conjugation. We confirmed the role of fliF, fliK, kefB and ucpA in the donor ability of conjugative elements by validating defects in the conjugation efficiency of the corresponding lab strain single-gene deletion mutants. Based on the known cellular functions of these genes, we suggest that the motility and the energy supply, the intracellular pH or salinity of the donor affect the efficiency of plasmid transfer. Overall, this work advances the search for targets for the development of conjugation inhibitors, which can be administered alongside antibiotics to more effectively treat bacterial infections. Full article
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14 pages, 1807 KiB  
Communication
Conjugation Operons in Gram-Positive Bacteria with and without Antitermination Systems
by Andrés Miguel-Arribas, Ling Juan Wu, Claudia Michaelis, Ken-ichi Yoshida, Elisabeth Grohmann and Wilfried J. J. Meijer
Microorganisms 2022, 10(3), 587; https://0-doi-org.brum.beds.ac.uk/10.3390/microorganisms10030587 - 08 Mar 2022
Cited by 2 | Viewed by 2603
Abstract
Genes involved in the same cellular process are often clustered together in an operon whose expression is controlled by an upstream promoter. Generally, the activity of the promoter is strictly controlled. However, spurious transcription undermines this strict regulation, particularly affecting large operons. The [...] Read more.
Genes involved in the same cellular process are often clustered together in an operon whose expression is controlled by an upstream promoter. Generally, the activity of the promoter is strictly controlled. However, spurious transcription undermines this strict regulation, particularly affecting large operons. The negative effects of spurious transcription can be mitigated by the presence of multiple terminators inside the operon, in combination with an antitermination system. Antitermination systems modify the transcription elongation complexes and enable them to bypass terminators. Bacterial conjugation is the process by which a conjugative DNA element is transferred from a donor to a recipient cell. Conjugation involves many genes that are mostly organized in one or a few large operons. It has recently been shown that many conjugation operons present on plasmids replicating in Gram-positive bacteria possess a bipartite antitermination system that allows not only many terminators inside the conjugation operon to be bypassed, but also the differential expression of a subset of genes. Here, we show that some conjugation operons on plasmids belonging to the Inc18 family of Gram-positive broad host-range plasmids do not possess an antitermination system, suggesting that the absence of an antitermination system may have advantages. The possible (dis)advantages of conjugation operons possessing (or not) an antitermination system are discussed. Full article
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Review

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19 pages, 1638 KiB  
Review
Occurrence of Antimicrobial Resistance in the Environment in Germany, Austria, and Switzerland: A Narrative Review of Existing Evidence
by Marina Treskova, Alexander Kuhlmann, Fritjof Freise, Lothar Kreienbrock and Sandra Brogden
Microorganisms 2022, 10(4), 728; https://0-doi-org.brum.beds.ac.uk/10.3390/microorganisms10040728 - 29 Mar 2022
Cited by 6 | Viewed by 2519
Abstract
(1) Background: This study summarizes the current research on antibiotic resistance (AR) in the environment conducted in Austria, Germany, and Switzerland; (2) Methods: A narrative systematic literature review of epidemiological studies based on searches in EMBASE and CAB abstracts (up to 16 June2021) [...] Read more.
(1) Background: This study summarizes the current research on antibiotic resistance (AR) in the environment conducted in Austria, Germany, and Switzerland; (2) Methods: A narrative systematic literature review of epidemiological studies based on searches in EMBASE and CAB abstracts (up to 16 June2021) was conducted. Environmental reservoirs included water sources, wastewater, animal husbandry, wildlife, soil, and sediment; (3) Results: Four hundred and four records were screened, and 52 studies were included. Thirteen studies examined aquatic environments, and eleven investigated wastewater. Eight studies investigated both wildlife and animal husbandry. Less evidence was available for sediments, soil, and air. Considerable heterogeneity in research focus, study design, sampling, and measurement of resistance was observed. Resistance to all categories of antimicrobials in the WHO CIA list was identified. Resistance to critically important and highly important substances was reported most frequently; (4) Conclusions: The current research scope presents data-gathering efforts. Usage of a unified protocol for isolate collection, selecting sampling sites, and susceptibility testing is required to provide results that can be compared between the studies and reservoirs. Epidemiological, environmental, and ecological factors should be considered in surveys of the environmental dissemination of AR. Systematic epidemiological studies investigating AR at the interface of human, animal, and environmental health are needed. Full article
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22 pages, 571 KiB  
Review
Reduced Susceptibility and Increased Resistance of Bacteria against Disinfectants: A Systematic Review
by Urška Rozman, Marko Pušnik, Sergej Kmetec, Darja Duh and Sonja Šostar Turk
Microorganisms 2021, 9(12), 2550; https://0-doi-org.brum.beds.ac.uk/10.3390/microorganisms9122550 - 10 Dec 2021
Cited by 37 | Viewed by 6532
Abstract
Disinfectants are used to reduce the concentration of pathogenic microorganisms to a safe level and help to prevent the transmission of infectious diseases. However, bacteria have a tremendous ability to respond to chemical stress caused by biocides, where overuse and improper use of [...] Read more.
Disinfectants are used to reduce the concentration of pathogenic microorganisms to a safe level and help to prevent the transmission of infectious diseases. However, bacteria have a tremendous ability to respond to chemical stress caused by biocides, where overuse and improper use of disinfectants can be reflected in a reduced susceptibility of microorganisms. This review aims to describe whether mutations and thus decreased susceptibility to disinfectants occur in bacteria during disinfectant exposure. A systematic literature review following PRISMA guidelines was conducted with the databases PubMed, Science Direct and Web of Science. For the final analysis, 28 sources that remained of interest were included. Articles describing reduced susceptibility or the resistance of bacteria against seven different disinfectants were identified. The important deviation of the minimum inhibitory concentration was observed in multiple studies for disinfectants based on triclosan and chlorhexidine. A reduced susceptibility to disinfectants and potentially related problems with antibiotic resistance in clinically important bacterial strains are increasing. Since the use of disinfectants in the community is rising, it is clear that reasonable use of available and effective disinfectants is needed. It is necessary to develop and adopt strategies to control disinfectant resistance. Full article
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