<scp>ICEA</scp> of <i><scp>M</scp>ycoplasma agalactiae</i>: a new family of self‐transmissible integrative elements that confers conjugative properties to the recipient strain

Dordet‐Frisoni, Emilie; Marenda, Marc S.; Sagné, Eveline; Nouvel, Laurent-Xavier; Guérillot, Romain; Glaser, Philippe; Blanchard, Alain; Tardy, Florence; Sirand‐Pugnet, Pascal; Baranowski, Éric; Citti, Christine

doi:10.1111/mmi.12341

Cited by 50 publications

(135 citation statements)

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“…For instance, the genome of M. agalactiae strain 5632 contains three almost identical copies of an entire ICE, ICEA 5632 , and two small regions (1.2 and 5.2 kbp, respectively) encoding ICE-related elements as remainders of past ICE insertions and decay (5,18). A vestigial ICE form displaying a reduced size and encompassing a large number of pseudogenes also occurs in M. agalactiae strain PG2 (vICEA PG2 ) (18) and was shown to be unable to transfer from cell to cell (19).…”

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“…It was then demonstrated that ICEA 5632 excision and integration are driven by a prokaryotic mutator-like transposase, a DDE transposase encoded by CDS22 of ICEA 5362 (19,21). Moreover, ICEA 5632 was shown to be self-transmissible and to disseminate horizontally from cell to cell via a conjugative process, with ICEA 5632 providing the recipient cell with the capacity to conjugate (19). Demonstration of ICEA 5632 trafficking in current mycoplasmas is an important step toward the understanding of HGT and of the contribution of ICE in this phenomenon.…”

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confidence: 99%

“…Demonstration of ICEA 5632 trafficking in current mycoplasmas is an important step toward the understanding of HGT and of the contribution of ICE in this phenomenon. Indeed, ICEA 5632 also provided the mycoplasma cell with a means for genome-wide chromosomal transfers that rely on an ICE-encoded conjugative bridge, although they are independent from ICE transfer per se (19,22).…”

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Integrative Conjugative Elements Are Widespread in Field Isolates of Mycoplasma Species Pathogenic for Ruminants

Tardy

Mick

Dordet‐Frisoni

et al. 2015

Appl Environ Microbiol

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Comparative genomics have revealed massive horizontal gene transfer (HGT) between Mycoplasma species sharing common ruminant hosts. Further results pointed toward an integrative conjugative element (ICE) as an important contributor of HGT in the small-ruminant-pathogen Mycoplasma agalactiae. To estimate the prevalence of ICEs in ruminant mycoplasmas, we surveyed their occurrence in a collection of 166 field strains representing 4 (sub)species that are recognized as major pathogens. Based on available sequenced genomes, we first defined the conserved, minimal ICE backbone as composed of 4 coding sequences (CDSs) that are evenly distributed and predicted to be essential for ICE chromosomal integration-excision and horizontal transfer. Screening of the strain collection revealed that these 4 CDSs are well represented in ruminant Mycoplasma species, suggesting widespread occurrence of ICEs. Yet their prevalence varies within and among species, with no correlation found with the individual strain history. Extrachromosomal ICE forms were also often detected, suggesting that ICEs are able to circularize in all species, a first and essential step in ICE horizontal transfer. Examination of the junction of the circular forms and comparative sequence analysis of conserved CDSs clearly pointed toward two types of ICE, the hominis and spiroplasma types, most likely differing in their mechanism of excision-integration. Overall, our data indicate the occurrence and maintenance of functional ICEs in a large number of field isolates of ruminant mycoplasmas. These may contribute to genome plasticity and gene exchanges and, presumably, to the emergence of diverse genotypes within pathogenic mycoplasmas of veterinary importance.M ycoplasma species represent a large group of wall-less bacteria belonging to the class Mollicutes that have often been portrayed as minimal cells because of the small size of their genomes and the paucity of their metabolic pathways. In the tree of life reconstructed from 31 conserved proteins (1), mycoplasmas are depicted on some of the longest branches, suggesting that they have evolved quickly. Indeed, a recent coalescent analysis supports this hypothesis by estimating the nucleotide substitution rate in Mycoplasma gallisepticum to be one of the highest reported for bacteria (2). Regarding the content of genes, it has long been considered that successive losses of genetic material were the only driving force of mycoplasma evolution (3), a scenario in agreement with these minimal bacteria having adopted a parasitic lifestyle. However, recent in silico genomic analyses revealed that mycoplasmas sharing the same habitat have exchanged a significant amount of their genome via horizontal gene transfer (HGT) (4). This was particularly true for the ruminant Mycoplasma species that are distributed into two distinct phylogenetic groups but share common animal hosts and ecological niches (e.g., the ear canal, the udder, the respiratory tract, etc.), with some having exchanged up to 18% of their genomes (5). Rumin...

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Integrative Conjugative Elements Are Widespread in Field Isolates of Mycoplasma Species Pathogenic for Ruminants

Tardy

Mick

Dordet‐Frisoni

et al. 2015

Appl Environ Microbiol

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“…ICE6013 is now the third family of integrative conjugative elements, after TnGBS and ICEA (15,16), known to use a DDE Tpase as a recombinase and the first example to use the IS30 family of Tpases. While the prototypical IS30 element from E. coli carries a single ORF (36), the IS30-like Tpase from ICE6013 is encoded by two ORFs.…”

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confidence: 99%

“…However, IS30-like Tpases acting as ICE recombinases have not yet been experimentally demonstrated. TnGBS from Streptococcus agalactiae and ICEA from Mycoplasma agalactiae are the only examples of ICEs demonstrated to use a Tpase as their recombinase (15,16); a Tpase from the p-MULT superfamily, which does not include IS30, is used for the excision of both elements (17).…”

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Transposase-Mediated Excision, Conjugative Transfer, and Diversity of ICE 6013 Elements in Staphylococcus aureus

et al. 2017

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ICE6013 represents one of two families of integrative conjugative elements (ICEs) identified in the pan-genome of the human and animal pathogen Staphylococcus aureus. Here we investigated the excision and conjugation functions of ICE6013 and further characterized the diversity of this element. ICE6013 excision was not significantly affected by growth, temperature, pH, or UV exposure and did not depend on recA. The IS30-like DDE transposase (Tpase; encoded by orf1 and orf2) of ICE6013 must be uninterrupted for excision to occur, whereas disrupting three of the other open reading frames (ORFs) on the element significantly affects the level of excision. We demonstrate that ICE6013 conjugatively transfers to different S. aureus backgrounds at frequencies approaching that of the conjugative plasmid pGO1. We found that excision is required for conjugation, that not all S. aureus backgrounds are successful recipients, and that transconjugants acquire the ability to transfer ICE6013. Sequencing of chromosomal integration sites in serially passaged transconjugants revealed a significant integration site preference for a 15-bp AT-rich palindromic consensus sequence, which surrounds the 3-bp target site that is duplicated upon integration. A sequence analysis of ICE6013 from different host strains of S. aureus and from eight other species of staphylococci identified seven divergent subfamilies of ICE6013 that include sequences previously classified as a transposon, a plasmid, and various ICEs. In summary, these results indicate that the IS30-like Tpase functions as the ICE6013 recombinase and that ICE6013 represents a diverse family of mobile genetic elements that mediate conjugation in staphylococci.IMPORTANCE Integrative conjugative elements (ICEs) encode the abilities to integrate into and excise from bacterial chromosomes and plasmids and mediate conjugation between bacteria. As agents of horizontal gene transfer, ICEs may affect bacterial evolution. ICE6013 represents one of two known families of ICEs in the pathogen Staphylococcus aureus, but its core functions of excision and conjugation are not well studied. Here, we show that ICE6013 depends on its IS30-like DDE transposase for excision, which is unique among ICEs, and we demonstrate the conjugative transfer and integration site preference of ICE6013. A sequence analysis revealed that ICE6013 has diverged into seven subfamilies that are dispersed among staphylococci.

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Alternative Ways to Exchange DNA: Unconventional Conjugation Among Bacteria

Esteban

Berenguer

2019

Horizontal Gene Transfer

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ICEA of Mycoplasma agalactiae: a new family of self‐transmissible integrative elements that confers conjugative properties to the recipient strain

Cited by 50 publications

References 47 publications

Integrative Conjugative Elements Are Widespread in Field Isolates of Mycoplasma Species Pathogenic for Ruminants

Integrative Conjugative Elements Are Widespread in Field Isolates of Mycoplasma Species Pathogenic for Ruminants

Transposase-Mediated Excision, Conjugative Transfer, and Diversity of ICE 6013 Elements in Staphylococcus aureus

Alternative Ways to Exchange DNA: Unconventional Conjugation Among Bacteria

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