Monitoring plasmid-mediated horizontal gene transfer in microbiomes: recent advances and future perspectives (original) (raw)
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Identification of bacterial plasmids based on mobility and plasmid population biology
FEMS Microbiology …
Plasmids contain a backbone of core genes that remains relatively stable for long evolutionary periods, making sense to speak about plasmid species. The identification and characterization of the core genes of a plasmid species has a special relevance in the study of its epidemiology and modes of transmission. Besides, this knowledge will help to unveil the main routes that genes, for example antibiotic resistance (AbR) genes, use to travel from environmental reservoirs to human pathogens. Global dissemination of multiple antibiotic resistances and virulence traits by plasmids is an increasing threat for the treatment of many bacterial infectious diseases. To follow the dissemination of virulence and AbR genes, we need to identify the causative plasmids and follow their path from reservoirs to pathogens. In this review, we discuss how the existing diversity in plasmid genetic structures gives rise to a large diversity in propagation strategies. We would like to propose that, using an identification methodology based on plasmid mobility types, we can follow the propagation routes of most plasmids in Gammaproteobacteria, as well as their cargo genes, in complex ecosystems. Once the dissemination routes are known, designing antidissemination drugs and testing their efficacy will become feasible.
Pathways for horizontal gene transfer in bacteria revealed by a global map of their plasmids
Nature Communications, 2020
Plasmids can mediate horizontal gene transfer of antibiotic resistance, virulence genes, and other adaptive factors across bacterial populations. Here, we analyze genomic composition and pairwise sequence identity for over 10,000 reference plasmids to obtain a global map of the prokaryotic plasmidome. Plasmids in this map organize into discrete clusters, which we call plasmid taxonomic units (PTUs), with high average nucleotide identity between its members. We identify 83 PTUs in the order Enterobacterales, 28 of them corresponding to previously described archetypes. Furthermore, we develop an automated algorithm for PTU identification, and validate its performance using stochastic blockmodeling. The algorithm reveals a total of 276 PTUs in the bacterial domain. Each PTU exhibits a characteristic host distribution, organized into a six-grade scale (I–VI), ranging from plasmids restricted to a single host species (grade I) to plasmids able to colonize species from different phyla (gr...
Plasmid Detection, Characterization, and Ecology
Microbiology Spectrum, 2015
Plasmids are important vehicles for rapid adaptation of bacterial populations to changing environmental conditions. It is thought that to reduce the cost of plasmid carriage, only a fraction of a local population carries plasmids or is permissive to plasmid uptake. Plasmids provide various accessory traits which might be beneficial under particular conditions. The genetic variation generated by plasmid carriage within populations ensures the robustness toward environmental changes. Plasmid-mediated gene transfer plays an important role not only in the mobilization and dissemination of antibiotic resistance genes but also in the spread of degradative pathways and pathogenicity determinants of pathogens. Here we summarize the state-of-the-art methods to study the occurrence, abundance, and diversity of plasmids in environmental bacteria. Increasingly, cultivation-independent total-community DNA-based methods are being used to characterize and quantify the diversity and abundance of pl...
Evolutionary paths that expand plasmid host-range: implications for spread of antibiotic resistance
Molecular Biology and Evolution, 2015
The World Health Organization has declared the emergence of antibiotic resistance to be a global threat to human health. Broad-host-range plasmids have a key role in causing this health crisis because they transfer multiple resistance genes to a wide range of bacteria. To limit the spread of antibiotic resistance, we need to gain insight into the mechanisms by which the host range of plasmids evolves. Although initially unstable plasmids have been shown to improve their persistence through evolution of the plasmid, the host, or both, the means by which this occurs are poorly understood. Here, we sought to identify the underlying genetic basis of expanded plasmid host-range and increased persistence of an antibiotic resistance plasmid using a combined experimental-modeling approach that included whole-genome resequencing, molecular genetics and a plasmid population dynamics model. In nine of the ten previously evolved clones, changes in host and plasmid each slightly improved plasmid persistence, but their combination resulted in a much larger improvement, which indicated positive epistasis. The only genetic change in the plasmid was the acquisition of a transposable element from a plasmid native to the Pseudomonas host used in these studies. The analysis of genetic deletions showed that the critical genes on this transposon encode a putative toxin-antitoxin (TA) and a cointegrate resolution system. As evolved plasmids were able to persist longer in multiple na€ ıve hosts, acquisition of this transposon also expanded the plasmid's host range, which has important implications for the spread of antibiotic resistance.
Environmental Science & Technology Letters, 2018
Wastewater treatment plants (WWTPs) have long been suggested as reservoirs and sources of antibiotic resistance genes (ARGs) in the environment. In a WWTP ecosystem, human enteric and environmental bacteria are mixed and exposed to pharmaceutical residues, potentially favoring genetic exchange and thus ARG transmission. However, the contribution of microbial communities in WWTP to ARG dissemination remains poorly understood. Here, we examined for the first time plasmid permissiveness of an activated sludge microbial community, by utilizing an established fluorescent bioreporter system. The activated sludge microbial community was challenged in standardized filter matings with one of the three multi-drug resistance plasmids (pKJK5, pB10 and RP4) harbored by Escherichia coli or Pseudomonas putida. Different donor-plasmid combinations had distinct transfer frequencies, ranging from 3 to 50 conjugation events per 100,000 cells of the WWTP microbial community. In addition, transfer was observed to a broad phylogenetic range of 13 bacterial phyla with several taxa containing potentially pathogenic species. Preferential transfer to taxa belonging to the predicted evolutionary host range of the plasmids was not observed. Overall, the ARG dissemination potential uncovered in WWTP communities calls for a thorough risk assessment of ARG transmission across the wastewater system, before identifying possible mitigation strategies.
Large-scale network analysis captures biological features of bacterial plasmids
Most bacteria exchange genetic material through Horizontal Gene Transfer (HGT). The primary vehicles for HGT are plasmids and plasmid-borne transposable elements, though their population structure and dynamics remain poorly understood. Here, we quantified genetic similarity between more than 10,000 bacterial plasmids and reconstructed a network based on their shared k-mer content. Using a community detection algorithm, we assigned plasmids into cliques which are highly correlated with plasmid gene content, bacterial host range, GC content, as well as replicon and mobility (MOB) type classifications. Resolving the plasmid population structure further allowed identification of candidates for yet-undescribed replicon genes. Our work provides biological insights into the dynamics of plasmids and plasmid-borne mobile elements, with the latter representing the main drivers of HGT at broad phylogenetic scales. Our results illustrate the potential of network-based analyses for the bacterial...
Transfer of conjugal plasmids is the main bacterial process of horizontal gene transfer to potentially 2 distantly related bacteria. These extra-chromosomal, circular DNA molecules host genes that code for their 3 own replication and transfer to other organisms. Because additional accessory genes may encode catabolic 4 pathways, virulence factors and antibiotic or metal resistances it is of environmental, evolutionary and 5 medical relevance to track and monitor the fate of plasmids in mixed microbial community. When assessing 6 the short-term and long-term implications of conjugal plasmid transfer the ability of a plasmid to invade a 7 mixed community is crucial. The main parameter that controls the possible extent of horizontal plasmid 8 transfer (HGT) in a bacterial community is the in-situ community permissiveness for the considered 9
Plasmids persist in a microbial community by providing fitness benefit to multiple phylotypes
2019
The current epidemic of antibiotic resistance has been facilitated by the wide and rapid horizontal dissemination of antibiotic resistance genes (ARGs) in microbial communities. Indeed, ARGs are often located on plasmids, which can efficiently shuttle genes across diverse taxa. While the existence conditions of plasmids have been extensively studied in a few model bacterial populations, their fate in complex bacterial communities is poorly understood. Here, we coupled plasmid transfer assays with serial growth experiments to investigate the persistence of the broad-host-range IncP-1 plasmid pKJK5 in microbial communities derived from a sewage treatment plant. The cultivation conditions combined different nutrient and oxygen levels, and were non-selective and non-conducive for liquid-phase conjugal transfer. Following initial transfer, the plasmid persisted in almost all conditions during a 10-day serial growth experiment (equivalent to 60 generations), with a transient transconjugan...
FEMS microbiology ecology, 2015
The IncP-1ε subgroup is a recently identified phylogenetic clade within IncP-1 plasmids, which plays an important role in the spread of antibiotic resistance and degradation of xenobiotic pollutants. Here, four IncP-1ε plasmids were exogenously captured from a petroleum-contaminated habitat in China and compared phylogenetically and genomically with previously reported IncP-1ε and other IncP-1 plasmids. The IncP-1ε plasmids can be clearly subdivided into two subclades, designated as ε-I and ε-II, based on phylogenetic analysis of backbone proteins TraI and TrfA. This was further supported by comparison of concatenated backbone genes. Moreover, the two subclades differed in the transposon types, phenotypes and insertion locations of the accessory elements. The accessory genes on ε-I plasmids were inserted between parA and traC, and harbored ISPa17 and Tn402-like transposon modules, typically carrying antibiotic resistance genes. In contrast, the accessory elements on ε-II plasmids we...
Targeting Plasmids to Limit Acquisition and Transmission of Antimicrobial Resistance
Frontiers in Microbiology
Antimicrobial resistance (AMR) is a significant global threat to both public health and the environment. The emergence and expansion of AMR is sustained by the enormous diversity and mobility of antimicrobial resistance genes (ARGs). Different mechanisms of horizontal gene transfer (HGT), including conjugation, transduction, and transformation, have facilitated the accumulation and dissemination of ARGs in Gram-negative and Gram-positive bacteria. This has resulted in the development of multidrug resistance in some bacteria. The most clinically significant ARGs are usually located on different mobile genetic elements (MGEs) that can move intracellularly (between the bacterial chromosome and plasmids) or intercellularly (within the same species or between different species or genera). Resistance plasmids play a central role both in HGT and as support elements for other MGEs, in which ARGs are assembled by transposition and recombination mechanisms. Considering the crucial role of MGEs in the acquisition and transmission of ARGs, a potential strategy to control AMR is to eliminate MGEs. This review discusses current progress on the development of chemical and biological approaches for the elimination of ARG carriers.