Ecological dynamics of plasmid transfer and persistence in microbial communities

Bottery, Michael

doi:10.1016/j.mib.2022.102152

Cited by 32 publications

(27 citation statements)

References 68 publications

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“…Overall, among the three main mechanisms of HGT, transformation rarely occurs between bacterial species to transfer drug resistance genes [75] when compared to more efficient processes such as conjugation, since conjugative plasmids account for half of all plasmids, and these can be broad host range [64,76,77]. Antibiotic concentrations in the environment range typically from 0.01 µg L -1 in the sea to 0.1 µg L -1 in rivers, 1 µg L -1 in treated municipal sewage, 10 µg L -1 in untreated municipal sewage, and up to 100-10'000 µg L -1 found in untreated hospital effluents and industrially polluted surface water [78].…”

Section: Discussionmentioning

confidence: 99%

“…A diverse microbial community like activated sludge is composed of many potential hosts that encompass a diversity of mechanisms to maintain and transfer plasmids, including donor-mediated conjugation once the plasmid is transformed [64]. Conjugative plasmid transfer spreads ARGs even in the absence of antibiotic pressure, as reported from investigations of the gut microbiota [65].…”

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confidence: 99%

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Catch me if you can: Capturing extracellular DNA transformation in mixed cultures via Hi-C sequencing

Calderón-Franco

Loosdrecht

Abeel

et al. 2022

Preprint

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Environmental microorganisms evolve constantly under various stressors using different adaptive mechanisms, including horizontal gene transfer. Microorganisms benefit from transferring genetic information that code for antibiotic resistance via mobile genetic elements (plasmids). Due to the complexity of natural microbial ecosystems, quantitative data on the transfer of genetic information in microbial communities remain unclear. Two 1-L chemostats (one control and one test) were inoculated with activated sludge, fed with synthetic wastewater, and operated for 45 days at a hydraulic retention time of 1 day to study the transformation capacity of a rolling-circle plasmid encoding GFP and kanamycin resistance genes, at increasing concentrations of kanamycin (0.01-2.5-50-100 mg L−1) representing environmental, wastewater, lab-selection, and gut or untreated pharmaceutical wastewater discharge environments. The plasmid DNA was spiked daily at 5 µg L−1 in the test chemostat. The evolution of the microbial community composition was analyzed by 16S rRNA gene amplicon sequencing and metagenomics, and the presence of the plasmid by quantitative PCR. We used Hi-C sequencing to identify natural transformant microorganisms under steady-state conditions with low (2.5 mg L−1) and high (50 mg L−1) concentrations of kanamycin. Both chemostats selected for the same 6 predominant families of Spirosomaceae, Comamonadaceae, Rhodocyclaceae, Rhizobiaceae, Microbacteriaceae, and Chitinophagaceae, while biomass formation in the presence of kanamycin was higher with the plasmid. Hence, the antibiotic exerted the main pressure on microbial selection, while the plasmid helped these populations better resist the antibiotic treatment and grow. The kanamycin resistance gene increased in both reactors (log 7 gene copies g VSS−1). When higher antibiotic concentrations were applied, the GFP/16S ratio was increased, highlighting plasmids accumulation in the test reactor over time. The plasmid transformed mainly inside populations of Bosea sp., Runella spp., and Microbacterium sp.. This study made one significant step forward by demonstrating that microorganisms in enrichments from activated sludge biomasses can acquire exogenous synthetic plasmids by transformation.Graphical abstract

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Section: Discussionmentioning

confidence: 99%

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confidence: 99%

Catch me if you can: Capturing extracellular DNA transformation in mixed cultures via Hi-C sequencing

Calderón-Franco

Loosdrecht

Abeel

et al. 2022

Preprint

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“…Furthermore, we have assumed that the transfer rate m is constant, but ecological interactions between bacterial populations are common. In reality, the decline or rescue of the focal population could affect the external population size via competition, predation, or facilitation and thus the rate m at which inter-specific transfers occur [Bottery, 2022].…”

Section: Discussionmentioning

confidence: 99%

Limits to evolutionary rescue by conjugative plasmids

Geoffroy

Uecker

2022

Preprint

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Plasmids may carry genes coding for beneficial traits and thus contribute to adaptation of bacterial populations to environmental stress. Conjugative plasmids can horizontally transfer between cells, which a priori facilitates the spread of adaptive alleles. However, if the potential recipient cell is already colonized by another incompatible plasmid, successful transfer may be prevented. Competition between plasmids can thus limit horizontal transfer. Previous modeling has indeed shown that evolutionary rescue by a conjugative plasmid is hampered by incompatible resident plasmids in the population. In this model, the fraction of resident plasmid cells was an exogeneous parameter. If the rescue plasmid is a mutant variant of the resident plasmid, however, both plasmids transfer at the same rates. A high conjugation rate then has two, potentially opposing, effects - a direct positive effect on spread of the rescue plasmid and an increase in the fraction of resident plasmid cells. This raises the question whether a high conjugation rate always benefits evolutionary rescue. In this article, we systematically analyse three models of increasing complexity to disentangle the benefits and limits of increasing horizontal gene transfer in the presence of plasmid competition and plasmid costs, finding that the net effect can be positive or negative.

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“…Some Inc plasmid types are distributed across various bacterial species and among different clones of the same species and are referred to as “broad host range” plasmids (e.g., IncP and IncO) [ 15 ]. Broad host range plasmids contain efficient conjugation systems enabling such plasmids to move efficiently between different bacterial species and be stably maintained [ 16 ].…”

Section: Plasmid Basicsmentioning

confidence: 99%

The Significance of Epidemic Plasmids in the Success of Multidrug-Resistant Drug Pandemic Extraintestinal Pathogenic Escherichia coli

Pitout

Chen

2023

Infect Dis Ther

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Epidemic IncF plasmids have been pivotal in the selective advantage of multidrug-resistant (MDR) extraintestinal pathogenic Escherichia coli (ExPEC). These plasmids have offered several advantages to their hosts that allowed them to coevolve with the bacterial host genomes and played an integral role in the success of ExPEC. IncF plasmids are large, mosaic, and often contain various types of antimicrobial resistance (AMR) and virulence associated factor (VAF) genes. The presence of AMR, VAF genes, several addition/restriction systems combined with truncated transfer regions, led to the fixation of IncF plasmids in certain ExPEC MDR clones, such as ST131 and ST410. IncF plasmids entered the ST131 ancestral lineage in the mid 1900s and different ST131 clade/CTX-M plasmid combinations coevolved over time. The IncF_CTX-M-15/ST131-C2 subclade combination emerged during the early 2000s, spread rapidly across the globe, and is one of the greatest clone/plasmid successes of the millennium. The ST410-B3 subclade containing bla CTX-M-15 incorporated the NDM-5 carbapenemase gene into existing IncF platforms, providing an additional positive selective advantage that included the carbapenems. A ''plasmid-replacement'' clade scenario occurred in the histories of ST131 and ST410 as different subclades gained different AMR genes on different IncF platforms. The use of antimicrobial agents will generate selection pressures that enhance the risks for the continuous emergence of MDR ExPEC clone/IncF plasmid combinations. The reasons for clade/IncF replacements and associations between certain clades and specific IncF plasmid types are unknown. Such information will aid in designing management and prevention strategies to combat AMR.

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Ecological dynamics of plasmid transfer and persistence in microbial communities

Cited by 32 publications

References 68 publications

Catch me if you can: Capturing extracellular DNA transformation in mixed cultures via Hi-C sequencing

Catch me if you can: Capturing extracellular DNA transformation in mixed cultures via Hi-C sequencing

Limits to evolutionary rescue by conjugative plasmids

The Significance of Epidemic Plasmids in the Success of Multidrug-Resistant Drug Pandemic Extraintestinal Pathogenic Escherichia coli

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