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Investigating prevalence and transmission of antibiotic resistance in the environment at multiple scales

The discovery of antibiotics has been considered as one of the most remarkable scientific accomplishments of the last century. However, the extensive usage of antibiotics has led to the rapid emergence of antibiotic resistance genes (ARGs) and antibiotic resistant bacteria (ARB), which have been recognized as one of the biggest threats to human and environmental health. While ARGs and ARB are ubiquitous in diverse environments, aquatic environments play a particularly crucial role in their prevalence and dissemination. Furthermore, the microbial complexity and various pollutants persisting in aquatic environments significantly contribute to the evolution and spread of ARGs and ARB. However, the knowledge regarding the distribution pattern of ARGs on a large scale, as well as the interaction between microbial community, specific pollutants, and ARGs and ARB, is currently limited. In this study, I conducted systematic work at multiple scales, to fill crucial knowledge gaps that could support the future management of the spread of antimicrobial resistance. In particular, on the ecosystems level I depict the biogeographical patterns of ARGs in freshwater reservoirs, on the community level I explored the selection patterns of combinations of antibiotics on multidrug resistant strains in complex community context, and finally, on the population level I investigated the impact of cigarette smoke, and waste products on the dissemination of ARGs.
In my first study, samples were collected from 24 freshwater reservoirs across southeast China and the biogeographical patterns of bacterial communities and ARG profile were characterized using 16S rRNA gene high-throughput sequencing and high-throughput-quantitative PCR. A distance-decay pattern for both, microbial communities and ARG profiles, were observed. However, larger differences between reservoir ARG profiles than microbial community compositions were detected. Further, I found that the biogeographical patterns of bacterial communities were simultaneously driven by stochastic and deterministic processes, while ARG profiles were not explained by stochastic processes, and the relationship between bacterial communities and ARG profiles was weak. In summary, this study indicated a decoupling of bacterial community composition and ARG profiles in inland waters under relatively low-human-impact at a large scale.
In a second study, the selection dynamics for multidrug resistance between isogenic pairs of E. coli strains under exposure to multiple selective agents in the absence and presence of the microbial community were investigated using microcosm experiments. The presence of the community significantly decreased the selection for multidrug resistant strain under exposure to a single antibiotic. While pressure through the second antibiotic significantly decreased the activity and diversity of the community, its ability to reduce selection was consistently maintained at levels comparable to those recorded in the absence of the second antibiotic. This indicates that the observed effects of community context on selection dynamics are rather based on competitive or protective effects between the focal strains and a small proportion of bacteria within the community, than on general competition for nutrients.
Last but not least, the effect of cigarette-derived pollutants on the proliferation of ARGs was explored using multifaced approaches. Cigarette smoke condensate in an artificial lung sputum medium significantly elevated the transfer rates of a multi-drug-resistance encoding plasmid between Pseudomonas strains. The overproduction of reactive oxygen species (ROS) as part of the bacterial stress response was directly connected to the increasing transfer rates. Similarly, cigarette ash leachate in an environmental medium significantly increased the plasmid transfer rates, and overproduction of ROS was equally detected. Furthermore, used cigarette filters with entrapped toxicants were submerged in a wastewater stream and colonized by distinct microbial communities compared to those colonizing unused control filters. The microbial communities colonizing used cigarette filters were significantly enriched in AMR, potential pathogenic bacteria and mobile genetic elements.
Overall, the insights gained within this thesis into the spread of AMR at multiple scales constitute a valuable contribution to support future management and monitoring of ARGs in diverse ecosystems.

Identiferoai:union.ndltd.org:DRESDEN/oai:qucosa:de:qucosa:91014
Date25 April 2024
CreatorsFang, Peiju
ContributorsBerendonk, Thomas U., Guan, Kaomei, Technische Universität Dresden
Source SetsHochschulschriftenserver (HSSS) der SLUB Dresden
LanguageEnglish
Detected LanguageEnglish
Typeinfo:eu-repo/semantics/publishedVersion, doc-type:doctoralThesis, info:eu-repo/semantics/doctoralThesis, doc-type:Text
Rightsinfo:eu-repo/semantics/openAccess

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