Second compartment widens plasmid invasion conditions: Two-compartment pair-formation model of conjugation in the gut

Jesse B. Alderliesten; Mark P. Zwart; J. Arjan G.M. de Visser; Arjan Stegeman; Egil A.J. Fischer

doi:10.1016/j.jtbi.2021.110937

Second compartment widens plasmid invasion conditions: Two-compartment pair-formation model of conjugation in the gut

Jesse B. Alderliesten, Mark P. Zwart, J. Arjan G.M. de Visser, Arjan Stegeman, Egil A.J. Fischer^* (Corresponding author)

^*Corresponding author for this work

NIOO - Microbial Ecology (ME)

Research output: Contribution to journal/periodical › Article › Scientific › peer-review

41 Downloads (Pure)

Abstract

Understanding under which conditions conjugative plasmids encoding antibiotic resistance can invade bacterial communities in the gut is of particular interest to combat the spread of antibiotic resistance within and between animals and humans. We extended a one-compartment model of conjugation to a two-compartment model, to analyse how differences in plasmid dynamics in the gut lumen and at the gut wall affect the invasion of plasmids. We compared scenarios with one and two compartments, different migration rates between the lumen and wall compartments, and different population dynamics. We focused on the effect of attachment and detachment rates on plasmid dynamics, explicitly describing pair formation followed by plasmid transfer in the pairs. The parameter space allowing plasmid invasion in the one-compartment model is affected by plasmid costs and intrinsic conjugation rates of the transconjugant, but not by these characteristics of the donor. The parameter space allowing plasmid invasion in the two-compartment model is affected by attachment and detachment rates in the lumen and wall compartment, and by the bacterial density at the wall. The one- and two-compartment models predict the same parameter space for plasmid invasion if the conditions in both compartments are equal to the conditions in the one-compartment model. In contrast, the addition of the wall compartment widens the parameter space allowing invasion compared with the one-compartment model, if the density at the wall is higher than in the lumen, or if the attachment rate at the wall is high and the detachment rate at the wall is low. We also compared the pair-formation models with bulk-conjugation models that describe conjugation by instantaneous transfer of the plasmid at contact between cells, without explicitly describing pair formation. Our results show that pair-formation and bulk-conjugation models predict the same parameter space for plasmid invasion. From our simulations, we conclude that conditions at the gut wall should be taken into account to describe plasmid dynamics in the gut and that transconjugant characteristics rather than donor characteristics should be used to parameterize the models.

Original language	English
Article number	110937
Journal	Journal of Theoretical Biology
Volume	533
DOIs	https://doi.org/10.1016/j.jtbi.2021.110937
Publication status	Published - 2022

Keywords

Horizontal gene transfer
Mathematical modelling
Mating pair
Mucosal environment
Plasmid dynamics
national
Plan_S-Compliant-OA

Access to Document

10.1016/j.jtbi.2021.110937Licence: CC BY

7337_AlderliestenFinal published version, 1.9 MBLicence: CC BY

Cite this

@article{4665373a75d742c9b72805c74ea58484,

title = "Second compartment widens plasmid invasion conditions: Two-compartment pair-formation model of conjugation in the gut",

abstract = "Understanding under which conditions conjugative plasmids encoding antibiotic resistance can invade bacterial communities in the gut is of particular interest to combat the spread of antibiotic resistance within and between animals and humans. We extended a one-compartment model of conjugation to a two-compartment model, to analyse how differences in plasmid dynamics in the gut lumen and at the gut wall affect the invasion of plasmids. We compared scenarios with one and two compartments, different migration rates between the lumen and wall compartments, and different population dynamics. We focused on the effect of attachment and detachment rates on plasmid dynamics, explicitly describing pair formation followed by plasmid transfer in the pairs. The parameter space allowing plasmid invasion in the one-compartment model is affected by plasmid costs and intrinsic conjugation rates of the transconjugant, but not by these characteristics of the donor. The parameter space allowing plasmid invasion in the two-compartment model is affected by attachment and detachment rates in the lumen and wall compartment, and by the bacterial density at the wall. The one- and two-compartment models predict the same parameter space for plasmid invasion if the conditions in both compartments are equal to the conditions in the one-compartment model. In contrast, the addition of the wall compartment widens the parameter space allowing invasion compared with the one-compartment model, if the density at the wall is higher than in the lumen, or if the attachment rate at the wall is high and the detachment rate at the wall is low. We also compared the pair-formation models with bulk-conjugation models that describe conjugation by instantaneous transfer of the plasmid at contact between cells, without explicitly describing pair formation. Our results show that pair-formation and bulk-conjugation models predict the same parameter space for plasmid invasion. From our simulations, we conclude that conditions at the gut wall should be taken into account to describe plasmid dynamics in the gut and that transconjugant characteristics rather than donor characteristics should be used to parameterize the models.",

keywords = "Horizontal gene transfer, Mathematical modelling, Mating pair, Mucosal environment, Plasmid dynamics, national, Plan_S-Compliant-OA",

author = "Alderliesten, {Jesse B.} and Zwart, {Mark P.} and {de Visser}, {J. Arjan G.M.} and Arjan Stegeman and Fischer, {Egil A.J.}",

note = "7337, ME",

year = "2022",

doi = "10.1016/j.jtbi.2021.110937",

language = "English",

volume = "533",

journal = "Journal of Theoretical Biology",

issn = "0022-5193",

publisher = "Academic Press",

}

TY - JOUR

T1 - Second compartment widens plasmid invasion conditions

T2 - Two-compartment pair-formation model of conjugation in the gut

AU - Alderliesten, Jesse B.

AU - Zwart, Mark P.

AU - de Visser, J. Arjan G.M.

AU - Stegeman, Arjan

AU - Fischer, Egil A.J.

N1 - 7337, ME

PY - 2022

Y1 - 2022

N2 - Understanding under which conditions conjugative plasmids encoding antibiotic resistance can invade bacterial communities in the gut is of particular interest to combat the spread of antibiotic resistance within and between animals and humans. We extended a one-compartment model of conjugation to a two-compartment model, to analyse how differences in plasmid dynamics in the gut lumen and at the gut wall affect the invasion of plasmids. We compared scenarios with one and two compartments, different migration rates between the lumen and wall compartments, and different population dynamics. We focused on the effect of attachment and detachment rates on plasmid dynamics, explicitly describing pair formation followed by plasmid transfer in the pairs. The parameter space allowing plasmid invasion in the one-compartment model is affected by plasmid costs and intrinsic conjugation rates of the transconjugant, but not by these characteristics of the donor. The parameter space allowing plasmid invasion in the two-compartment model is affected by attachment and detachment rates in the lumen and wall compartment, and by the bacterial density at the wall. The one- and two-compartment models predict the same parameter space for plasmid invasion if the conditions in both compartments are equal to the conditions in the one-compartment model. In contrast, the addition of the wall compartment widens the parameter space allowing invasion compared with the one-compartment model, if the density at the wall is higher than in the lumen, or if the attachment rate at the wall is high and the detachment rate at the wall is low. We also compared the pair-formation models with bulk-conjugation models that describe conjugation by instantaneous transfer of the plasmid at contact between cells, without explicitly describing pair formation. Our results show that pair-formation and bulk-conjugation models predict the same parameter space for plasmid invasion. From our simulations, we conclude that conditions at the gut wall should be taken into account to describe plasmid dynamics in the gut and that transconjugant characteristics rather than donor characteristics should be used to parameterize the models.

AB - Understanding under which conditions conjugative plasmids encoding antibiotic resistance can invade bacterial communities in the gut is of particular interest to combat the spread of antibiotic resistance within and between animals and humans. We extended a one-compartment model of conjugation to a two-compartment model, to analyse how differences in plasmid dynamics in the gut lumen and at the gut wall affect the invasion of plasmids. We compared scenarios with one and two compartments, different migration rates between the lumen and wall compartments, and different population dynamics. We focused on the effect of attachment and detachment rates on plasmid dynamics, explicitly describing pair formation followed by plasmid transfer in the pairs. The parameter space allowing plasmid invasion in the one-compartment model is affected by plasmid costs and intrinsic conjugation rates of the transconjugant, but not by these characteristics of the donor. The parameter space allowing plasmid invasion in the two-compartment model is affected by attachment and detachment rates in the lumen and wall compartment, and by the bacterial density at the wall. The one- and two-compartment models predict the same parameter space for plasmid invasion if the conditions in both compartments are equal to the conditions in the one-compartment model. In contrast, the addition of the wall compartment widens the parameter space allowing invasion compared with the one-compartment model, if the density at the wall is higher than in the lumen, or if the attachment rate at the wall is high and the detachment rate at the wall is low. We also compared the pair-formation models with bulk-conjugation models that describe conjugation by instantaneous transfer of the plasmid at contact between cells, without explicitly describing pair formation. Our results show that pair-formation and bulk-conjugation models predict the same parameter space for plasmid invasion. From our simulations, we conclude that conditions at the gut wall should be taken into account to describe plasmid dynamics in the gut and that transconjugant characteristics rather than donor characteristics should be used to parameterize the models.

KW - Horizontal gene transfer

KW - Mathematical modelling

KW - Mating pair

KW - Mucosal environment

KW - Plasmid dynamics

KW - national

KW - Plan_S-Compliant-OA

U2 - 10.1016/j.jtbi.2021.110937

DO - 10.1016/j.jtbi.2021.110937

M3 - Article

AN - SCOPUS:85118591434

SN - 0022-5193

VL - 533

JO - Journal of Theoretical Biology

JF - Journal of Theoretical Biology

M1 - 110937

ER -

Second compartment widens plasmid invasion conditions: Two-compartment pair-formation model of conjugation in the gut

Abstract

Keywords

Access to Document

Fingerprint

Cite this