Crosstalk between bacterial conjugation and motility is mediated by plasmid‐borne regulators

Luque, Ainara; Paytubi, Sònia; Sánchez-Montejo, Javier; Gibert, M. Alsina; Balsalobre, Carlos; Madrid, Cristina

doi:10.1111/1758-2229.12784

Cited by 18 publications

(12 citation statements)

References 39 publications

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“…Although this latter observation may be a consequence of the manipulation of the bacterial cells for electron microscopy observation, it is apparent that the likely consequence of the interaction of the RSP protein with the flagella must be the alteration of flagellar function, which, in turn, leads to the observed reduced bacterial cell motility. IncHI plasmids reducing bacterial cell motility also appears to occur by another mechanism: R27 plasmid encoded regulators downregulate flagella synthesis [53]. The results presented both in this latter report and in the present paper support the view that the cell motility is reduced when IncHI plasmid conjugation is prompted.…”

Section: Discussionsupporting

confidence: 85%

Expression of a novel class of bacterial Ig-like proteins is required for IncHI plasmid conjugation

Hüttener¹,

Prieto²,

Aznar³

et al. 2019

PLoS Genet

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Antimicrobial resistance (AMR) is currently one of the most important challenges to the treatment of bacterial infections. A critical issue to combat AMR is to restrict its spread. In several instances, bacterial plasmids are involved in the global spread of AMR. Plasmids belonging to the incompatibility group (Inc)HI are widespread in Enterobacteriaceae and most of them express multiple antibiotic resistance determinants. They play a relevant role in the recent spread of colistin resistance. We present in this report novel findings regarding IncHI plasmid conjugation. Conjugative transfer in liquid medium of an IncHI plasmid requires expression of a plasmid-encoded, large-molecular-mass protein that contains an Ig-like domain. The protein, termed RSP, is encoded by a gene (ORF R0009) that maps in the Tra2 region of the IncHI1 R27 plasmid. The RSP protein is exported outside the cell by using the plasmid-encoded type IV secretion system that is also used for its transmission to new cells. Expression of the protein reduces cell motility and enables plasmid conjugation. Flagella are one of the cellular targets of the RSP protein. The RSP protein is required for a high rate of plasmid transfer in both flagellated and nonflagellated Salmonella cells. This effect suggests that RSP interacts with other cellular structures as well as with flagella. These unidentified interactions must facilitate mating pair formation and, hence, facilitate IncHI plasmid conjugation. Due to its location on the outer surfaces of the bacterial cell, targeting the RSP protein could be a means of controlling IncHI plasmid conjugation in natural environments or of combatting infections caused by AMR enterobacteria that harbor IncHI plasmids.

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Section: Discussionsupporting

confidence: 85%

Expression of a novel class of bacterial Ig-like proteins is required for IncHI plasmid conjugation

Hüttener¹,

Prieto²,

Aznar³

et al. 2019

PLoS Genet

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“…For IncHI plasmids, R27 isolated from S . Typhi and prototypical founder for the IncHI1 plasmid group remains one of the best studied plasmids of this type ( Sherburne et al, 2000 ; Lawley et al, 2003 ; Huttener et al, 2019 ; Luque et al, 2019 ). In S .…”

Section: Discussionmentioning

confidence: 99%

“…In this instance, the ISEc27 element that has undergone expansion in numbers in the E. coli K12 J53 (pMG101-A) host strain is inserted on the opposite strand of Tra2 rsp, is transcribed in the opposite direction to all other genes encoded in the gene operon and may well also be exerting polar effects on genes downstream that are recognised as being essential for conjugal transfer (trhFWUN). For IncHI plasmids, R27 isolated from S. Typhi and prototypical founder for the IncHI1 plasmid group remains one of the best studied plasmids of this type (Sherburne et al, 2000;Lawley et al, 2003;Huttener et al, 2019;Luque et al, 2019). In S. Typhimurium SL1344, the 155.4 kDa RSP was initially identified in cell-free supernatants and found to be expressed in a temperature-dependent manner (optimal expression 25°C).…”

Section: Discussionmentioning

confidence: 99%

Laboratory Stock Variants of the Archetype Silver Resistance Plasmid pMG101 Demonstrate Plasmid Fusion, Loss of Transmissibility, and Transposition of Tn7/pco/sil Into the Host Chromosome

et al. 2021

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Salmonella Typhimurium carrying the multidrug resistance (MDR) plasmid pMG101 was isolated from three burns patients in Boston United States in 1973. pMG101 was transferrable into other Salmonella spp. and Escherichia coli hosts and carried what was a novel and unusual combination of AMR genes and silver resistance. Previously published short-read DNA sequence of pMG101 showed that it was a 183.5Kb IncHI plasmid, where a Tn7-mediated transposition of pco/sil resistance genes into the chromosome of the E. coli K-12 J53 host strain had occurred. We noticed differences in streptomycin resistance and plasmid size between two stocks of E. coli K-12 J53 pMG101 we possessed, which had been obtained from two different laboratories (pMG101-A and pMG101-B). Long-read sequencing (PacBio) of the two strains unexpectedly revealed plasmid and chromosomal rearrangements in both. pMG101-A is a non-transmissible 383Kb closed-circular plasmid consisting of an IncHI2 plasmid sequence fused to an IncFI/FIIA plasmid. pMG101-B is a mobile closed-circular 154 Kb IncFI/FIIA plasmid. Sequence identity of pMG101-B with the fused IncFI/IncFIIA region of pMG101-A was >99%. Assembled host sequence reads of pMG101-B showed Tn7-mediated transposition of pco/sil into the E. coli J53 chromosome between yhiM and yhiN. Long read sequence data in combination with laboratory experiments have demonstrated large scale changes in pMG101. Loss of conjugation function and movement of resistance genes into the chromosome suggest that even under long-term laboratory storage, mobile genetic elements such as transposons and insertion sequences can drive the evolution of plasmids and host. This study emphasises the importance of utilising long read sequencing technologies of plasmids and host strains at the earliest opportunity.

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“…IncHI plasmids and Salmonella participate in regulatory crosstalk that, is based on the expression of both the tetracycline determinant and other plasmid-encoded genes [54,55]. One of the effects of the crosstalk is the alteration in cellular motility, which is mediated by both plasmid-borne regulators [56] and the binding of the RSP and RSP2 proteins to the flagellar structure ([47], this work). Nevertheless, these proteins also play a second and critical role in IncHI plasmid conjugation.…”

Section: Discussionmentioning

confidence: 99%

Roles of proteins containing immunoglobulin-like domains in the conjugation of bacterial plasmids

Hüttener

Hergueta

Bernabeu

et al. 2021

Preprint

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Horizontal transfer of bacterial plasmids generates genetic variability and contributes to the dissemination of the genes that enable bacterial cells to develop antimicrobial resistance (AMR). Several aspects of the conjugative process have long been known, namely, those related to the proteins that participate in the establishment of cell-to-cell contact and to the enzymatic processes associated with the processing of plasmid DNA and its transfer to the recipient cell. In this work, we describe the role of newly identified proteins that influence the conjugation of several plasmids. Genes encoding high-molecular-weight proteins that contain one or several immunoglobulin-like domains (Big) are located in the transfer regions of several plasmids that usually harbor AMR determinants. These Big proteins are exported to the external medium and target two extracellular organelles: the flagella and the conjugative pili. The plasmid-encoded Big proteins facilitate conjugation by reducing cell motility (by binding to flagella) and facilitating cell-to-cell contact (by binding to the conjugative pilus). They use the same export machinery as that used by the conjugative pilus components. In the examples characterized in this paper, these proteins influence conjugation at environmental temperatures (i.e., 25C). This suggests that they may play relevant roles in the dissemination of plasmids in natural environments. As they are located in outer surface organelles, they could be targeted to control the dissemination of different bacterial plasmids carrying AMR determinants.

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Crosstalk between bacterial conjugation and motility is mediated by plasmid‐borne regulators

Cited by 18 publications

References 39 publications

Expression of a novel class of bacterial Ig-like proteins is required for IncHI plasmid conjugation

Expression of a novel class of bacterial Ig-like proteins is required for IncHI plasmid conjugation

Laboratory Stock Variants of the Archetype Silver Resistance Plasmid pMG101 Demonstrate Plasmid Fusion, Loss of Transmissibility, and Transposition of Tn7/pco/sil Into the Host Chromosome

Roles of proteins containing immunoglobulin-like domains in the conjugation of bacterial plasmids

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