Vertical and horizontal gene transfer tradeoffs direct plasmid fitness

Bethke, Jonathan H.; Riuró, Helena; Tsoi, Ryan; Cheng, Li; Xiao, Mei; Li, You

doi:10.15252/msb.202211300

Cited by 26 publications

(21 citation statements)

References 51 publications

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“…Dynamic consortia with transferable plasmids require 2 n ODEs to model, where n is the number of plasmids in the system. We assume that the conjugation of the plasmids does not incur an additional metabolic burden on the host cells (66) . For the two-module case, we can model the DDOL community with four ODEs: where S 00 is the empty strain ( δ A = δ B = 0), S 10 carries only plasmid A encoding the first step of the pathway ( δ A = 1, δ B = 0), S 01 carries only plasmid B ( δ A = 0, δ B = 1), and S 11 carries both plasmids ( δ A = δ B = 1).…”

Section: Methodsmentioning

confidence: 99%

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Programming dynamic division of labor using horizontal gene transfer

Hamrick,

Maddamsetti,

Son

et al. 2023

Preprint

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The metabolic engineering of microbes has broad applications, including in biomanufacturing, bioprocessing, and environmental remediation. The introduction of a complex, multi-step pathway often imposes a substantial metabolic burden on the host cell, restraining the accumulation of productive biomass and limiting pathway efficiency. One strategy to alleviate metabolic burden is division of labor (DOL), in which different subpopulations carry out different parts of the pathway and work together to convert a substrate into a final product. However, the maintenance of different engineered subpopulations is challenging due to competition and convoluted inter-strain population dynamics. Through modeling, we show that dynamic division of labor (DDOL) mediated by horizontal gene transfer (HGT) can overcome these limitations and enable the robust maintenance of burdensome, multi-step pathways. We also use plasmid genomics to uncover evidence that DDOL is a strategy utilized by natural microbial communities. Our work suggests that bioengineers can harness HGT to stabilize synthetic metabolic pathways in microbial communities, enabling the development of robust engineered systems for deployment in a variety of contexts.

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Section: Methodsmentioning

confidence: 99%

“…Dynamic consortia with transferable plasmids require 2 𝑛 ODEs to model, where 𝑛 is the number of plasmids in the system. We assume that the conjugation of the plasmids does not incur an additional metabolic burden on the host cells (66). For the two-module case, we can model the DDOL community with four ODEs:…”

Section: Modeling Population Dynamicsmentioning

confidence: 99%

Programming dynamic division of labor using horizontal gene transfer

Hamrick,

Maddamsetti,

Son

et al. 2023

Preprint

Self Cite

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“…Interactions between these two levels have important implications for the evolution of plasmids and for their contribution to the evolution of their hosts. For example, there is a trade-off between rates of vertical and horizontal transmission of plasmids [15,100,128]: the costs to the host of conjugation mean that increased horizontal transmission reduces vertical transmission. A similar tradeoff also leads to conflicting selection pressures on the plasmid copy number: a plasmid variant with a higher copy number outcompetes a variant with a lower copy number at the intracellular level, but if the copy number increases too much, the burden on the host cell may become too high [129,259].…”

Section: Multilevel Selectionmentioning

confidence: 99%

“…Vertical fitness of plasmids is directly dependent on host fitness, while horizontal fitness is more independent (although plasmid spread by horizontal transmission still requires persistence of the host). In general, there may be strong trade-offs between vertical and horizontal transmission [128, 129], for example due to the fitness costs of conjugation to the host. Since both contribute to total plasmid fitness, there will often be different possible successful life history strategies with a different emphasis on horizontal versus vertical transmission [15] (the extreme case being nontransmissible plasmids that rely entirely on vertical transmission).…”

Section: Ecology Of Plasmidsmentioning

confidence: 99%

A mathematician’s guide to plasmids: an introduction to plasmid biology for modellers

Dewan,

Uecker

2023

Microbiology

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Plasmids, extrachromosomal DNA molecules commonly found in bacterial and archaeal cells, play an important role in bacterial genetics and evolution. Our understanding of plasmid biology has been furthered greatly by the development of mathematical models, and there are many questions about plasmids that models would be useful in answering. In this review, we present an introductory, yet comprehensive, overview of the biology of plasmids suitable for modellers unfamiliar with plasmids who want to get up to speed and to begin working on plasmid-related models. In addition to reviewing the diversity of plasmids and the genes they carry, their key physiological functions, and interactions between plasmid and host, we also highlight selected plasmid topics that may be of particular interest to modellers and areas where there is a particular need for theoretical development. The world of plasmids holds a great variety of subjects that will interest mathematical biologists, and introducing new modellers to the subject will help to expand the existing body of plasmid theory.

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“…Horizontal plasmid transmission can in principle make up for a deficit in vertical transmission, although conjugation rates vary considerably depending on the plasmid type (7,8). The fate of plasmids in bacterial populations is thus determined by the interplay between horizontal and vertical transmission dynamics (and their evolution) (9)(10)(11)(12). Multiple theoretical and experimental studies have investigated plasmid dynamics in clonal bacterial populations (7,8,(13)(14)(15)(16)(17).…”

Section: Introductionmentioning

confidence: 99%

Antimicrobial resistance level and conjugation permissiveness shape plasmid distribution in clinical enterobacteria

Valle

Toribio-Celestino

Quirant

et al. 2023

Preprint

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Conjugative plasmids can transfer both vertically and horizontally in bacterial communities, playing a key role in the dissemination of antimicrobial resistance (AMR) genes across bacterial pathogens. AMR plasmids are widespread in clinical settings, but their distribution is not random, and certain associations between plasmids and bacterial clones are particularly successful. However, knowledge remains limited about the contribution made by vertical and horizontal transmission dynamics to plasmid distribution and maintenance in clinically relevant bacterial communities. In this study, we used a collection of wild type enterobacterial strains isolated from hospitalized patients to perform a comprehensive analysis of the transmission dynamics of the globally spread carbapenem resistance plasmid pOXA-48. We combined in vitro and in vivo experimental approaches to quantify key traits responsible for vertical (the level of AMR) and horizontal (conjugation frequency) plasmid transmission. Our results reveal significant variability in these traits across different bacterial hosts, with Klebsiella spp. strains showing higher pOXA-48-mediated AMR and conjugation frequencies than Escherichia coli strains. Using experimentally determined parameters, we developed a simple mathematical model to interrogate the contribution of vertical and horizontal transmission to plasmid distribution in bacterial communities. These simulations revealed that a small subset of clones, combining high vertical and horizontal plasmid transmission ability, play a critical role in stabilizing the plasmid in different polyclonal microbial communities. Our results indicate that strain-specific differences in plasmid transmission dynamics dictate successful associations between plasmids and bacterial clones, shaping AMR evolution.

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Vertical and horizontal gene transfer tradeoffs direct plasmid fitness

Cited by 26 publications

References 51 publications

Programming dynamic division of labor using horizontal gene transfer

Programming dynamic division of labor using horizontal gene transfer

A mathematician’s guide to plasmids: an introduction to plasmid biology for modellers

Antimicrobial resistance level and conjugation permissiveness shape plasmid distribution in clinical enterobacteria

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