Long-term dynamics of catabolic plasmids introduced to a microbial community in a polluted environment: a mathematical model

Miki, Takeshi; Ueki, Masaya; Kawabata, Zen’ichiro; Yamamura, Norio

doi:10.1111/j.1574-6941.2007.00357.x

Cited by 5 publications

(9 citation statements)

References 41 publications

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“…Furthermore, many natural plasmids repress expression of their self-transfer functions (Firth et al, 1996;Lawley et al, 2004). These observations are surprising given that increased rates of conjugation aid plasmids in invading and persisting within host populations, as demonstrated by this work and others' (Stewart and Levin, 1977;Dionisio et al, 2002;De Gelder et al, 2007Miki et al, 2007). Here we show that, in a population of plasmid-bearing cells, a variant plasmid with a decreased conjugation rate can give its hosts a competitive edge.…”

Section: Discussionmentioning

confidence: 73%

Competition favours reduced cost of plasmids to host bacteria

2009

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Conjugative plasmids of Gram-negative bacteria have both vertical and horizontal modes of transmission: they are segregated to daughter cells during division, and transferred between hosts by plasmid-encoded conjugative machinery. Despite maintaining horizontal mobility, many plasmids carry fertility inhibition (fin) systems that repress their own conjugative transfer. To assess the ecological basis of self-transfer repression, we compared the invasion of bacterial populations by fin þ and fin À variants of the plasmid R1 using a computational model and co-culture competitions. We observed that the fin þ variant had a modest cost to the host (measured by reduction in growth rate), while the fin À variant incurred a larger cost. In simulations and empirical competitions the fin À plasmid invaded cultures quickly, but was subsequently displaced by the fin þ plasmid. This indicated a competitive advantage to reducing horizontal transmission and allowing increased host replication. Computational simulations predicted that the advantage associated with reduced cost to the host would be maintained over a wide range of environmental conditions and plasmid costs. We infer that vertical transmission in concert with competitive exclusion favour decreased horizontal mobility of plasmids. Similar dynamics may exert evolutionary pressure on parasites, such as temperate bacteriophages and vertically transmitted animal viruses, to limit their rates of horizontal transfer.

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Section: Discussionmentioning

confidence: 73%

Competition favours reduced cost of plasmids to host bacteria

2009

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“…The conservation of pixR in the IncX4 plasmids suggests that this gene provides an evolutionary advantage for mcr-1-bearing IncX4 in nature. pixR increases the transfer capability of IncX4 plasmids and a high rate of conjugation usually helps plasmids invade bacterial populations (19,20,37). Therefore, here we investigated the role of pixR in the persistence and invasion of mcr-1bearing IncX4 plasmids to better understand their prevalence.…”

Section: Discussionmentioning

confidence: 99%

“…The copyright holder for this preprint this version posted August 6, 2021. ; https://doi.org/10.1101/2021.08.04.455183 doi: bioRxiv preprint plasmids and a high rate of conjugation usually helps plasmids invade bacterial populations (19,20,37). Therefore, here we investigated the role of pixR in the persistence and invasion of mcr-1bearing IncX4 plasmids to better understand their prevalence.…”

Section: Discussionmentioning

confidence: 99%

“…The latest theory explaining this "plasmid-paradox" examines three main features: the rate of plasmid loss during replication, the rate of plasmid acquisition, and the plasmid fitness adaptation to the host (1,17,18). Conjugation plays an essential role in the persistence of a plasmid in a bacterial population (19)(20)(21). Previous reports have shown that IncX4 plasmids transfer at a high frequency, ~10 -2 -10 -4 (22,23).…”

Section: Introductionmentioning

confidence: 99%

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PixR, a novel activator of conjugative transfer of IncX4 resistance plasmids, mitigates the fitness cost of mcr-1 carriage in Escherichia coli

Durand

Grenier

et al. 2021

Preprint

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The emergence of the plasmid-borne colistin resistance gene mcr-1 threats public health. IncX4-type plasmids are one of the most epidemiologically successful vehicles for spreading mcr-1 worldwide. Since MCR-1 is known for imposing a fitness cost to its host bacterium, the successful spread of mcr-1-bearing plasmids might be linked to high conjugation frequency, which would enhance the maintenance of the plasmid in the host without antibiotic selection. However, the mechanism of IncX4 plasmids conjugation remains unclear. In this study, we used high-density transposon mutagenesis to identify factors required for IncX4 plasmid transfer and 18 genes were identified, including five with annotations unrelated to conjugation. The Cappable-seq and RNA-seq analysis confirmed that a novel transcriptional regulator gene, pixR, directly regulates the transfer of IncX4 plasmids by binding the promoter of 13 essential transfer genes to increase their transcription. Plasmid invasion and co-culture competition assays revealed that pixR is essential for the spread and persistence of mcr-1-bearing IncX4 plasmids in bacterial populations, and effective conjugation is crucial for alleviating the fitness cost exerted by mcr-1 carriage. The existence of the IncX4-specific pixR gene increases plasmid transmissibility while promoting the invasion and persistence of mcr-1-bearing plasmids in bacterial populations, which helps explain their global prevalence.IMPORTANCEThe spread of clinical important antibiotic resistance genes is frequently related to some epidemic plasmids. However, the underlying molecular mechanisms contributing to the successful spread of these epidemic plasmids remains unclear. The significant of our research indicated that efficient conjugation could promote the invasion and persistence of plasmids within a bacterial population, resulting in the successful dissemination of epidemic plasmids in nature. Our data also highlight the importance of developing plasmid conjugation inhibitors to solve the antibiotic resistance crisis.

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“…A previous study demonstrated that the selection and growth of donor and transconjugant cells were dependent on the presence of sufficiently high concentrations of the specific substrate ( Ravatn et al., 1998 ). To predict the long-term dynamics of catabolic plasmids in a polluted environment, a mathematical model was developed that considered the negative feedback between plasmid spread and selective advantage: when catabolic genes are highly spread, the OMP concentration will decrease faster, thereby lowering the selective advantage of plasmid-bearing bacteria ( Miki et al., 2007 ). Thus, in order to achieve long-term OMP degradation, it is necessary to find the right plasmid spread efficiency in order to maintain constant, low pollutant concentrations, as the degrading microbial community remains more stable when OMP degradation occurs slowly.…”

Section: Transfer Of Catabolic Genes As a Bioaugmentation Strategy Inmentioning

confidence: 99%

The role of mobile genetic elements in organic micropollutant degradation during biological wastewater treatment

2020

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Wastewater treatment plants (WWTPs) are crucial for producing clean effluents from polluting sources such as hospitals, industries, and municipalities. In recent decades, many new organic compounds have ended up in surface waters in concentrations that, while very low, cause (chronic) toxicity to countless organisms. These organic micropollutants (OMPs) are usually quite recalcitrant and not sufficiently removed during wastewater treatment. Microbial degradation plays a pivotal role in OMP conversion. Microorganisms can adapt their metabolism to the use of novel molecules via mutations and rearrangements of existing genes in new clusters. Many catabolic genes have been found adjacent to mobile genetic elements (MGEs), which provide a stable scaffold to host new catabolic pathways and spread these genes in the microbial community. These mobile systems could be engineered to enhance OMP degradation in WWTPs, and this review aims to summarize and better understand the role that MGEs might play in the degradation and wastewater treatment process. Available data about the presence of catabolic MGEs in WWTPs are reviewed, and current methods used to identify and measure MGEs in environmental samples are critically evaluated. Finally, examples of how these MGEs could be used to improve micropollutant degradation in WWTPs are outlined. In the near future, advances in the use of MGEs will hopefully enable us to apply selective augmentation strategies to improve OMP conversion in WWTPs.

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Long-term dynamics of catabolic plasmids introduced to a microbial community in a polluted environment: a mathematical model

Cited by 5 publications

References 41 publications

Competition favours reduced cost of plasmids to host bacteria

Competition favours reduced cost of plasmids to host bacteria

PixR, a novel activator of conjugative transfer of IncX4 resistance plasmids, mitigates the fitness cost of mcr-1 carriage in Escherichia coli

The role of mobile genetic elements in organic micropollutant degradation during biological wastewater treatment

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