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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.

No MeSH data available.


Model for formation of the qacC' fragment present in Types Ia and IIa plasmids. A single nt insertion 137 nt downstream of qacC (indicated by the asterisk) is present in some Type II plasmids (e.g., pLUH01) and conserved in both Types Ia and IIa. This is evidence that the duplication of the 142 nt-long qacC' fragment, inserted at position −45, occurred in a Type II plasmid to form Type IIa, after which the complete locus was mobilized to give Type Ia.
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Figure 3: Model for formation of the qacC' fragment present in Types Ia and IIa plasmids. A single nt insertion 137 nt downstream of qacC (indicated by the asterisk) is present in some Type II plasmids (e.g., pLUH01) and conserved in both Types Ia and IIa. This is evidence that the duplication of the 142 nt-long qacC' fragment, inserted at position −45, occurred in a Type II plasmid to form Type IIa, after which the complete locus was mobilized to give Type Ia.

Mentions: Plasmids containing the 142-nt duplication of qacC' are designated Type Ia or Type IIa, depending on their Rep (Table 1). That this partial duplication can be variably present on both types can be explained in two ways. Either the qacC locus was distributed to Type I and Type II plasmids first, after which an identical qacC' duplication occurred independently in both, or the duplication occurred first and the locus with or without the duplication spread independently in both types of plasmids. Analysis of the downstream sequences provides a clue as to which scenario is more likely. A single-nucleotide insertion is found 137 nt downstream of qacC in all known Type Ia and Type IIa loci (indicated by an asterisk in Figure 2), and it is also present in some Type II loci (e.g., pSA1308 or pLUH01, see Table 1). It is therefore proposed that the duplication occurred in such a Type II plasmid (Figure 3), after which the whole locus including the duplication was distributed over Type I plasmids. This observation supports the hypothesis that the QacC locus is transferable.


The qacC Gene Has Recently Spread between Rolling Circle Plasmids of Staphylococcus , Indicative of a Novel Gene Transfer Mechanism
Model for formation of the qacC' fragment present in Types Ia and IIa plasmids. A single nt insertion 137 nt downstream of qacC (indicated by the asterisk) is present in some Type II plasmids (e.g., pLUH01) and conserved in both Types Ia and IIa. This is evidence that the duplication of the 142 nt-long qacC' fragment, inserted at position −45, occurred in a Type II plasmid to form Type IIa, after which the complete locus was mobilized to give Type Ia.
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
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Figure 3: Model for formation of the qacC' fragment present in Types Ia and IIa plasmids. A single nt insertion 137 nt downstream of qacC (indicated by the asterisk) is present in some Type II plasmids (e.g., pLUH01) and conserved in both Types Ia and IIa. This is evidence that the duplication of the 142 nt-long qacC' fragment, inserted at position −45, occurred in a Type II plasmid to form Type IIa, after which the complete locus was mobilized to give Type Ia.
Mentions: Plasmids containing the 142-nt duplication of qacC' are designated Type Ia or Type IIa, depending on their Rep (Table 1). That this partial duplication can be variably present on both types can be explained in two ways. Either the qacC locus was distributed to Type I and Type II plasmids first, after which an identical qacC' duplication occurred independently in both, or the duplication occurred first and the locus with or without the duplication spread independently in both types of plasmids. Analysis of the downstream sequences provides a clue as to which scenario is more likely. A single-nucleotide insertion is found 137 nt downstream of qacC in all known Type Ia and Type IIa loci (indicated by an asterisk in Figure 2), and it is also present in some Type II loci (e.g., pSA1308 or pLUH01, see Table 1). It is therefore proposed that the duplication occurred in such a Type II plasmid (Figure 3), after which the whole locus including the duplication was distributed over Type I plasmids. This observation supports the hypothesis that the QacC locus is transferable.

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.