An evolutionary perspective on plasmid lifestyle modes

Hülter, Nils; Ilhan, Judith; Wein, Tanita; Kadibalban, A. Samer; Hammerschmidt, Katrin; Dagan, Tal

doi:10.1016/j.mib.2017.05.001

Cited by 91 publications

(75 citation statements)

References 62 publications

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“…It is also noteworthy that most of these plasmids possess several TA systems, as occurs with plasmids from other bacteria (see also Fig. 6) [4,57,58].…”

Section: Discussionmentioning

confidence: 76%

“…Additionally, other highly repetitive genes, such as the rulAB operon for resistance to UV light and many other DNA repair genes, are also commonly associated to virulence and other adaptive genes in P. syringae and many other bacteria [54][55][56]. All these repetitive genetic elements favour the mobility of virulence genes, promoting the high plasticity and adaptability of native plasmids [7,[19][20][21]; however, at the same time, represent recombination hotspots that can mediate deletion of key virulence genes [57], as highlighted by our results, and of many other adaptive genes. Second, the frequencies of recombination between MITEs and of transposition of IS801 were very high, suggesting that they could be very active in promoting genomic changes.…”

Section: Discussionmentioning

confidence: 99%

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Integrity and stability of virulence plasmids fromPseudomonas syringaeare modulated by mobile genetic elements and multiple toxin-antitoxin systems

Bardaji

Añorga

Echeverría

et al. 2018

Preprint

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Background: Virulence plasmids are critically exposed to genetic decay and loss, particularly in Pseudomonas syringae strains because of their high content of mobile genetic elements and their exploitation of environmental niches outside of the plant host. The demonstrated high plasticity and adaptability of P. syringae plasmids, involving the acquisition and loss of large DNA regions, contrasts with their usual high stability and the maintenance of key virulence genes in free living conditions. The identification of plasmid stability determinants and mechanisms will help to understand their evolution and adaptability to agroecosystems as well as to develop more efficient control measures. Results:We show that the three virulence plasmids of P. syringae pv. savastanoi NCPPB 3335 contain diverse functional stability determinants, including three toxin-antitoxin systems (TA) in both pPsv48A and pPsv48C, whereas one of the two replicons of pPsv48C can confer stable inheritance by itself. Loss of pPsv48A increased by two orders of magnitude upon functional inactivation of its TA systems. However, inactivation of the TA systems from pPsv48C did not result in its curing but led to the recovery of diverse deletion derivatives. One type consisted in the deletion of an 8.3 kb fragment, with a frequency of 3.8 ± 0.3 × 10 -3 , by recombination between two copies of MITEPsy2. Likewise, IS801 promoted the occurrence of deletions of variable size by one-ended transposition with a frequency of 5.5 ± 2.1 × 10 -4 , 80 % of which resulted in the loss of virulence gene idi. These deletion derivatives were stably maintained in the population by replication mediated by repJ, which is adjacent to IS801. IS801 also promoted deletions in plasmid pPsv48A, either by recombination or one-ended transposition. In all cases, functional TA systems contributed significantly to reduce the occurrence of plasmid deletions in vivo. Conclusions:Virulence plasmids from P. syringae harbour a diverse array of stability determinants with a variable contribution to plasmid persistence. Additionally, multiple TA systems favour the long-term survival and integrity of virulence plasmids, as well as the maintenance of pathogenicity genes in free-living conditions. This strategy is likely widespread amongst native plasmids of P. syringae and other bacteria.(MINECO), co-financed by the Fondo Europeo de Desarrollo Regional (FEDER).

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“…It is also noteworthy that most of these plasmids possess several TA systems, as occurs with plasmids from other bacteria (see also Fig. 6) [4,57,58].…”

Section: Discussionmentioning

confidence: 76%

Section: Discussionmentioning

confidence: 99%

Integrity and stability of virulence plasmids fromPseudomonas syringaeare modulated by mobile genetic elements and multiple toxin-antitoxin systems

Bardaji

Añorga

Echeverría

et al. 2018

Preprint

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“…Genomic island SV5 had an additional 45 bp deletion in repA (Figure 3C), and SV6 had a deletion of six syntenic CDS from the plasmid backbone likely resulting from IS 256 -mediated homologous recombination (Figure 3B). All deletion events invariably resulted in the loss of genes, or predicted loss of function of the plasmid replication machinery, which has a known role in stabilising newly integrated elements by removing any interference with chromosomal replication [48].…”

Section: Resultsmentioning

confidence: 99%

“…These findings strongly suggested that the emergence of these phylogenetically distinct but structurally similar SVs is the result of a significant but unknown evolutionary pressure acting on this pSK1-like population. There is a clear role for chromosomal integration in improving the maintenance of plasmid genes in a population, and the subsequent deletion or disruption of the plasmid replication machinery is needed for stability of the integrant [48]. In the Australian clade, almost all isolates (75/77) that have descended from an ancestral genome with an integrated pSK1-like structure have maintained it (Figure S2).…”

Section: Resultsmentioning

confidence: 99%

Remodelling of pSK1 Family Plasmids and Enhanced Chlorhexidine Tolerance in Methicillin-ResistantStaphylococcus aureus

Baines

Jensen

Firth

et al. 2018

Preprint

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26Staphylococcus aureus is a significant human pathogen whose evolution and adaptation has been 27 shaped in part by mobile genetic elements (MGEs), facilitating global spread of extensive 28 antimicrobial resistance. However, our understanding of the evolutionary dynamics surrounding 29 MGEs is incomplete, in particular how changes in the structure of multidrug-resistant (MDR) 30 plasmids may influence important staphylococcal phenotypes. Here, we undertook a population-31 and functional-genomics study of 212 methicillin-resistant S. aureus (MRSA) ST239 isolates 32 collected over 32 years to explore the evolution of the pSK1 family of MDR plasmids, illustrating 33 how these plasmids have co-evolved with and contributed to the successful adaptation of this 34 persistent MRSA lineage. Using complete genomes and temporal phylogenomics we reconstructed 35 the evolution of the pSK1 family lineage from its emergence in the late 1970s, with multiple 36 structural variants arising. Plasmid maintenance and stability was linked to IS256-and IS257-37 mediated chromosomal integration and disruption of plasmid replication machinery. Overlaying 38 genomic comparisons with phenotypic susceptibility data for gentamicin and chlorhexidine, it 39 appeared that pSK1 has contributed to enhanced resistance in ST239 MRSA through two 40 mechanisms: (i) acquisition of plasmid-borne resistance mechanisms increasing rates of 41 gentamicin resistance and reduced chlorhexidine susceptibility, and (ii) changes in plasmid 42 configuration linked with further enhancement of chlorhexidine tolerance. While the exact 43 mechanism of enhanced tolerance remains elusive, this research has uncovered a clear 44 evolutionary response of ST239 MRSA to chlorhexidine, one which may contribute to the ongoing 45 persistence and adaptation of this lineage within healthcare institutions.46 4 Importance 47The biocide chlorhexidine is fundamental to infection control practices which prevent nosocomial 48 infection and it is highly effective for decolonisation of S. aureus from human skin. There have 49 been increasing reports of staphylococcal populations evolving tolerance to chlorhexidine, 50 suggesting that the increasing use and reliance on this biocide may provide a significant selection 51 pressure influencing the evolution of staphylococcal populations. Chlorhexidine tolerance in 52 S. aureus is commonly enabled by the acquisition of an efflux pump, however alternative 53 mechanisms influencing tolerance are poorly understood. In this study we demonstrate a 54 previously unrecognised phenomenon, plasmid structural remodelling, by which S. aureus may 55 developed enhanced chlorhexidine tolerance. Further, we highlight the importance of undertaking 56 a detailed exploration of the evolutionary dynamics surrounding mobile genetic elements, which 57 contribute immensely to the evolution of microbial species and provide here a framework for how 58 such an analysis can be performed.59 60Mobile genetic elements (MGEs) play a central role in microbial e...

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“…Plasmids are secondary replicons that can rapidly move across bacterial genomes increasing genomic plasticity through a process known as horizontal gene transfer (HGT). Thousands of genes can be transferred via HGT in an instance allowing for the colonization of new niches by the acquisition of genes encoding for metabolism, antibiotic resistance, virulence factors, and symbiosis thus enabling colonization of new niches (1)(2)(3)(4)(5)(6). While plasmids could provide advantages for a bacterial cell in a given environment, horizontal gene transfer also brings many costs that may be manifested in phenotypic changes rather than lowered fitness alone (7)(8)(9)(10)(11).…”

Section: Introductionmentioning

confidence: 99%

Experimental Evolution of the Megaplasmid pMPPla107 in Pseudomonas stutzeri Enables Identification of Genes Contributing to Sensitivity to an Inhibitory Agent

Smith

Dougherty

Clark

et al. 2019

Preprint

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Horizontally transferred elements such as plasmids can, at times, burden host cells with various metabolic and fitness costs. Our previous work demonstrated that acquisition of the Pseudomonas syringae megaplasmid pMPPla107 causes sensitivity to a growth inhibiting substance that is produced in cultures during growth under standard laboratory conditions. After 500 generations of laboratory passage of P. stutzeri lines containing pMPPla107, two out of six independent lines displayed resistance to this inhibitory agent. We therefore sequenced the genomes of isolates from each independent evolutionary line to identify the genetic basis of this resistance phenotype through comparative genomics. Our analysis demonstrates that two different compensatory mutations on the megaplasmid ameliorate the sensitivity phenotype: 1) a large deletion of approximately 368kb in pMPPla107 and 2) a SNP in the gene we name skaA for Supernatant Killing Activity. These results provide further evidence that costs associated with horizontal gene transfer can be compensated through single mutational events and emphasize the power of experimental evolution and resequencing to better understand the genetic basis of evolved phenotypes.

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An evolutionary perspective on plasmid lifestyle modes

Cited by 91 publications

References 62 publications

Integrity and stability of virulence plasmids fromPseudomonas syringaeare modulated by mobile genetic elements and multiple toxin-antitoxin systems

Integrity and stability of virulence plasmids fromPseudomonas syringaeare modulated by mobile genetic elements and multiple toxin-antitoxin systems

Remodelling of pSK1 Family Plasmids and Enhanced Chlorhexidine Tolerance in Methicillin-ResistantStaphylococcus aureus

Experimental Evolution of the Megaplasmid pMPPla107 in Pseudomonas stutzeri Enables Identification of Genes Contributing to Sensitivity to an Inhibitory Agent

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