Intensive targeting of regulatory competence genes by transposable elements in streptococci

Fléchard, Maud; Lucchetti-Miganeh, Céline; Hallet, Bernard; Hols, Pascal; Gilot, Philippe

doi:10.1007/s00438-018-1507-5

Cited by 7 publications

(3 citation statements)

References 84 publications

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“…The prophages belonging to subgroups D2 and G were inserted into the com X gene encoding the master regulator of competence in streptococci. The same locus is frequently targeted by transposable elements in streptococci with possible impact on the induction of transformability [ 57 ]. Integration sites localized in com genes were also observed for S. agalactiae prophages in previous studies [ 10 , 17 , 56 ].…”

Section: Discussionmentioning

confidence: 99%

Characterization of Clinical and Carrier Streptococcus agalactiae and Prophage Contribution to the Strain Variability

Lichvariková

Šoltýs

Szemes

et al. 2020

Viruses

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Streptococcus agalactiae (group B Streptococcus, GBS) represents a leading cause of invasive bacterial infections in newborns and is also responsible for diseases in older and immunocompromised adults. Prophages represent an important factor contributing to the genome plasticity and evolution of new strains. In the present study, prophage content was analyzed in human GBS isolates. Thirty-seven prophages were identified in genomes of 20 representative sequenced strains. On the basis of the sequence comparison, we divided the prophages into eight groups named A–H. This division also corresponded to the clustering of phage integrase, even though several different integration sites were observed in some relative prophages. Next, PCR method was used for detection of the prophages in 123 GBS strains from adult hospitalized patients and from pregnancy screening. At least one prophage was present in 105 isolates (85%). The highest prevalence was observed for prophage group A (71%) and satellite prophage group B (62%). Other groups were detected infrequently (1–6%). Prophage distribution did not differ between clinical and screening strains, but it was unevenly distributed in MLST (multi locus sequence typing) sequence types. High content of full-length and satellite prophages detected in present study implies that prophages could be beneficial for the host bacterium and could contribute to evolution of more adapted strains.

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Section: Discussionmentioning

confidence: 99%

Characterization of Clinical and Carrier Streptococcus agalactiae and Prophage Contribution to the Strain Variability

Lichvariková

Šoltýs

Szemes

et al. 2020

Viruses

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“…In a systematic study of the competence regulon in S. pyogenes , it was noted that despite harboring all the genes needed for natural transformation, a number of the strains analyzed had mutations in the genes encoding the DNA uptake system ( 23 ). A high incidence of transposable elements in the vicinity of genes involved in competence in S. pyogenes has also been reported ( 27 ). Additionally, a prophage-encoded protein known as paratox has been shown to inhibit competence induction by preventing the interaction between XIP and ComR in S. pyogenes ( 28 , 29 ).…”

Section: Introductionmentioning

confidence: 99%

Genetic modification of Streptococcus dysgalactiae by natural transformation

Mårli,

Oppegaard,

Porcellato

et al. 2024

mSphere

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Streptococcus dysgalactiae is an emerging human and animal pathogen. Functional studies of genes involved in virulence of S. dysgalactiae and other pyogenic group streptococci are often hampered by limited genetic tractability. It is known that pyogenic streptococci carry genes required for competence for natural transformation; however, in contrast to other streptococcal subgroups, there is limited evidence for gene transfer by natural transformation in these bacteria. In this study, we systematically assessed the genomes of 179 S . dysgalactiae strains of both human and animal origins (subsp. equisimilis and dysgalactiae, respectively) for the presence of genes required for natural transformation. While a considerable fraction of the strains contained inactive genes, the majority (64.2%) of the strains had an intact gene set. In selected strains, we examined the dynamics of competence activation after addition of competence-inducing pheromones using transcriptional reporter assays and exploratory RNA-seq. Based on these findings, we were able to establish a protocol allowing us to utilize natural transformation to construct deletion mutants by allelic exchange in several S. dysgalactiae strains of both subspecies. As part of the work, we deleted putative lactose utilization genes to study their role in growth on lactose. The data presented here provide new knowledge on the potential of horizonal gene transfer by natural transformation in S. dysgalactiae and, importantly, demonstrates the possibility to exploit natural transformation for genetic engineering in these bacteria. IMPORTANCE Numerous Streptococcus spp. exchange genes horizontally through natural transformation, which also facilitates efficient genetic engineering in these organisms. However, for the pyogenic group of streptococci, including the emerging pathogen Streptococcus dysgalactiae , there is limited experimental evidence for natural transformation. In this study, we demonstrate that natural transformation in vitro indeed is possible in S. dysgalactiae strains under optimal conditions. We utilized this method to perform gene deletion through allelic exchange in several strains, thereby paving the way for more efficient gene engineering methods in pyogenic streptococci.

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“…Thus, a form of genetic conflict may exist between bacteria and MGEs. In that sense, a growing list of MGEs are found to counteract transformation through diverse strategies (39)(40)(41)(42)(43)(44)(45), suggesting an evolutionary response of MGEs against the cleansing activity of bacteria from transformation. However, the consequences of transformation inhibition on the evolutionary success of MGEs remains underappreciated.…”

Section: Introductionmentioning

confidence: 99%

Manipulation of natural transformation by AbaR-type islands promotes fixation of antibiotic resistance inAcinetobacter baumanniipopulations

Tuffet,

Carvalho,

Godeux

et al. 2023

Preprint

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International public health organizations consider the multidrug resistant and opportunistic pathogenAcinetobacter baumannii, as a major global health concern. This species hosts multiple variants of AbaR-type genomic islands which carry several antibiotic resistance, including to carbapenems (AbaR4 variant). How these islands, conferring multidrug resistance, persist inA. baumanniipopulations remains elusive.Using complementary approaches, we investigated whether the manipulation of natural transformation by AbaRs, via their insertion strategy in the bacterial chromosome, might give them a selective advantage and contribute to the persistence of antibiotic resistance genes inA. baumanniipopulations. Natural transformation is a process through which bacteria can import and recombine exogenous DNA, facilitating gene transfer and allelic recombination. Although transformation promotes acquisition of mobile genetic elements (MGEs), it is also proposed to serve as a mechanism to purge them from the chromosome. Several MGEs inhibit transformation, suggesting that natural transformation can impede their evolutionary dynamics.We established an experimental model in which natural transformation spontaneously occurs inA. baumanniipopulations, allowing us to determine the rate of acquisition and removal of MGEs. We found that the majority of AbaRs disrupt thecomMgene, causing differential inhibition of MGE acquisition, removal and allelic transfer events. A mathematical evolutionary model shows that AbaRs inserting into thecomMgene gain a selective advantage over AbaRs whose insertion site either do not inhibit or completely inhibit transformation. ThecomMinsertion strategy is clearly advantageous when the model incorporates some degree of environmental complexity, such as combined antibiotic stress or changes in environmental resources.Our work highlights how AbaRs, and potentially other MGEs, can manipulate natural transformation to persist in populations, resulting in the high prevalence of multidrug resistance.

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Intensive targeting of regulatory competence genes by transposable elements in streptococci

Cited by 7 publications

References 84 publications

Characterization of Clinical and Carrier Streptococcus agalactiae and Prophage Contribution to the Strain Variability

Characterization of Clinical and Carrier Streptococcus agalactiae and Prophage Contribution to the Strain Variability

Genetic modification of Streptococcus dysgalactiae by natural transformation

Manipulation of natural transformation by AbaR-type islands promotes fixation of antibiotic resistance inAcinetobacter baumanniipopulations

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