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The qacC Gene Has Recently Spread between Rolling Circle Plasmids of Staphylococcus , Indicative of a Novel Gene Transfer Mechanism

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ABSTRACT

Resistance of Staphylococcus species to quaternary ammonium compounds, frequently used as disinfectants and biocides, can be attributed to qac genes. Most qac gene products belong to the Small Multidrug Resistant (SMR) protein family, and are often encoded by rolling-circle (RC) replicating plasmids. Four classes of SMR-type qac gene families have been described in Staphylococcus species: qacC, qacG, qacJ, and qacH. Within their class, these genes are highly conserved, but qacC genes are extremely conserved, although they are found in variable plasmid backgrounds. The lower degree of sequence identity of these plasmids compared to the strict nucleotide conservation of their qacC means that this gene has recently spread. In the absence of insertion sequences or other genetic elements explaining the mobility, we sought for an explanation of mobilization by sequence comparison. Publically available sequences of qac genes, their flanking genes and the replication gene that is invariably present in RC-plasmids were compared to reconstruct the evolutionary history of these plasmids and to explain the recent spread of qacC. Here we propose a new model that explains how qacC is mobilized and transferred to acceptor RC-plasmids without assistance of other genes, by means of its location in between the Double Strand replication Origin (DSO) and the Single-Strand replication Origin (SSO). The proposed mobilization model of this DSO-qacC-SSO element represents a novel mechanism of gene mobilization in RC-plasmids, which has also been employed by other genes, such as lnuA (conferring lincomycin resistance). The proposed gene mobility has aided to the wide spread of clinically relevant resistance genes in Staphylococcus populations.

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Relationship between Types I/II and Type III plasmids. (A) Type III could be formed from the qacC element by a single duplication event whereby the downstream flank is inserted into a hotspot for recombination, positioned 45 nt upstream of qacC. (B) Alternatively, a precursor can be hypothesized with qacC next to DSO and SSO. A duplication of the SSO-bearing segment would result in Type III, after which a deletion would produce the qacC element.
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Figure 4: Relationship between Types I/II and Type III plasmids. (A) Type III could be formed from the qacC element by a single duplication event whereby the downstream flank is inserted into a hotspot for recombination, positioned 45 nt upstream of qacC. (B) Alternatively, a precursor can be hypothesized with qacC next to DSO and SSO. A duplication of the SSO-bearing segment would result in Type III, after which a deletion would produce the qacC element.

Mentions: Two models can be proposed how the qac locus of Type III plasmids relates to Types I and II, shown in Figure 4. The simplest model (Figure 4A) proposes that Type III is formed from a Type I or II qacC plasmid by duplication of the downstream flank inserted into the upstream flank, at position −45 nt. Alternatively (Figure 4B), Types I and II are formed from Type III, which requires a hypothesized precursor in which upstream sequences have been duplicated into the downstream flank. Although that model requires two steps, it may be the more likely scenario, because in the hypothesized precursor a DSO and SSO would be separated by 316 nt, a distance that is more typical for staphylococcal RC-plasmids that only contain a rep gene (e.g., pSK6 of S. aureus, acc. nr. NC_001995).


The qacC Gene Has Recently Spread between Rolling Circle Plasmids of Staphylococcus , Indicative of a Novel Gene Transfer Mechanism
Relationship between Types I/II and Type III plasmids. (A) Type III could be formed from the qacC element by a single duplication event whereby the downstream flank is inserted into a hotspot for recombination, positioned 45 nt upstream of qacC. (B) Alternatively, a precursor can be hypothesized with qacC next to DSO and SSO. A duplication of the SSO-bearing segment would result in Type III, after which a deletion would produce the qacC element.
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC5037232&req=5

Figure 4: Relationship between Types I/II and Type III plasmids. (A) Type III could be formed from the qacC element by a single duplication event whereby the downstream flank is inserted into a hotspot for recombination, positioned 45 nt upstream of qacC. (B) Alternatively, a precursor can be hypothesized with qacC next to DSO and SSO. A duplication of the SSO-bearing segment would result in Type III, after which a deletion would produce the qacC element.
Mentions: Two models can be proposed how the qac locus of Type III plasmids relates to Types I and II, shown in Figure 4. The simplest model (Figure 4A) proposes that Type III is formed from a Type I or II qacC plasmid by duplication of the downstream flank inserted into the upstream flank, at position −45 nt. Alternatively (Figure 4B), Types I and II are formed from Type III, which requires a hypothesized precursor in which upstream sequences have been duplicated into the downstream flank. Although that model requires two steps, it may be the more likely scenario, because in the hypothesized precursor a DSO and SSO would be separated by 316 nt, a distance that is more typical for staphylococcal RC-plasmids that only contain a rep gene (e.g., pSK6 of S. aureus, acc. nr. NC_001995).

View Article: PubMed Central - PubMed

ABSTRACT

Resistance of Staphylococcus species to quaternary ammonium compounds, frequently used as disinfectants and biocides, can be attributed to qac genes. Most qac gene products belong to the Small Multidrug Resistant (SMR) protein family, and are often encoded by rolling-circle (RC) replicating plasmids. Four classes of SMR-type qac gene families have been described in Staphylococcus species: qacC, qacG, qacJ, and qacH. Within their class, these genes are highly conserved, but qacC genes are extremely conserved, although they are found in variable plasmid backgrounds. The lower degree of sequence identity of these plasmids compared to the strict nucleotide conservation of their qacC means that this gene has recently spread. In the absence of insertion sequences or other genetic elements explaining the mobility, we sought for an explanation of mobilization by sequence comparison. Publically available sequences of qac genes, their flanking genes and the replication gene that is invariably present in RC-plasmids were compared to reconstruct the evolutionary history of these plasmids and to explain the recent spread of qacC. Here we propose a new model that explains how qacC is mobilized and transferred to acceptor RC-plasmids without assistance of other genes, by means of its location in between the Double Strand replication Origin (DSO) and the Single-Strand replication Origin (SSO). The proposed mobilization model of this DSO-qacC-SSO element represents a novel mechanism of gene mobilization in RC-plasmids, which has also been employed by other genes, such as lnuA (conferring lincomycin resistance). The proposed gene mobility has aided to the wide spread of clinically relevant resistance genes in Staphylococcus populations.

No MeSH data available.


Related in: MedlinePlus