Abstract
Most methicillin resistant Staphylococcus aureus (MRSA) isolates harboring mecC gene belong to clonal complex CC130. This lineage has traditionally been regarded as animal-associated as it lacks the human specific immune evasion cluster (IEC), and has been recovered from a broad range of animal hosts. Nevertheless, sporadic mecC-MRSA human infections have been reported, with evidence of zoonotic transmission in some cases. The objective of this study was to investigate the whole-genome sequences of 18 S. aureus CC130 isolates [13 methicillin-resistant (mecC-MRSA) and five methicillin-susceptible (MSSA)] from different sequences types, obtained from a variety of host species and origins (human, livestock, wild birds and mammals, and water), and from different geographic locations, in order to identify characteristic markers and genomic features. Antibiotic resistance genes found among MRSA-CC130 were those associated with the SSCmecXI element. Most MRSA-CC130 strains carried a similar virulence gene profile. Additionally, six MRSA-CC130 possessed scn-sak and one MSSA-ST130 had lukMF’. The MSSA-ST700 strains were most divergent in their resistance and virulence genes. The pan-genome analysis showed that 29 genes were present solely in MRSA-CC130 (associated with SCCmecXI) and 21 among MSSA-CC130 isolates (associated with phages). The SCCmecXI, PBP3, GdpP, and AcrB were identical at the amino acid level in all strains, but some differences were found in PBP1, PBP2, PBP4, and YjbH proteins. An examination of the host markers showed that the 3’ region of the bacteriophage φ3 was nearly identical to the reference sequence. Truncated hlb gene was also found in scn-negative strains (two of them carrying sak-type gene). The dtlB gene of wild rabbit isolates included novel mutations. The vwbp gene was found in the three MSSA-ST700 strains from small ruminants and in one MSSA-ST130 from a red deer; these strains also carried a scn-type gene, different from the human and equine variants. Finally, a phylogenetic analysis showed that the three MSSA-ST700 strains and the two MSSA-ST130 strains cluster separately from the remaining MRSA-CC130 strains with the etD2 gene as marker for the main lineage. The presence of the human IEC cluster in some mecC-MRSA-CC130 strains suggests that these isolates may have had a human origin.
Highlights
Staphylococcus aureus is a common colonizer of the nasopharynx and skin of animals and humans; it is a versatile opportunistic pathogen causing a wide variety of diseases from mild skin problems to life-threatening bacteraemias
In order to better understand the genetic characteristics of S. aureus CC130, the objective of this study was to analyze data from whole genome sequencing (WGS) of a collection of CC130 S. aureus strains (MRSA and methicillin-susceptible S. aureus (MSSA)) belonging to different sequences types, obtained from various host species, and from different geographic locations, in order to identify distinctive markers and genomic features of public health relevance
These strains were as follows: (1) 13 methicillin-resistant S. aureus (MRSA), carrying the mecC gene, and belonging to the sequence types ST130, ST1945, ST3061, ST1571, ST1581, and ST1583; (2) two MSSA-ST130; and (3) three MSSA-ST700. These 18 MRSA-CC130, MSSA-ST130, and MSSA-ST700 strains were studied by WGS, having been collected during previous studies from different host samples: animals from extensive farms [four red deer (Cervus elaphus), two sheep (Ovis sp.), and one goat (Capra sp.)] (Gharsa et al, 2015; Gómez et al, 2015), wildlife [four magpies (Pica pica), two wild rabbits (Oryctolagus cuniculus), one wood mouse (Apodemus sylvaticus), one white stork (Ciconia ciconia), and one cinereous vulture (Aegypius monachus)] (Gómez et al, 2014, 2016; Ruiz-Ripa et al, 2019), the environment (Gómez et al, 2017), and humans] (Benito et al, 2016)
Summary
Staphylococcus aureus is a common colonizer of the nasopharynx and skin of animals and humans; it is a versatile opportunistic pathogen causing a wide variety of diseases from mild skin problems to life-threatening bacteraemias. The prevalence of mecC-MRSA in people seems to be low (Paterson et al, 2014a,b; Lozano et al, 2020), the zoonotic transmission from livestock to people has been reported (Harrison et al, 2013), as well as its ability to cause disease (Petersen et al, 2013) This mecC-MRSA-CC130 lineage seems to be susceptible to many non-β-lactam agents and lacks major human virulence factors (Cuny et al, 2011; Monecke et al, 2013; Paterson et al, 2014a). None of the mecC-MRSA reported strains harbored the scn gene (essential for the IEC system) (Lozano et al, 2020), with the exception of a few isolates belonging to ST1945, ST1581, and ST1583 previously described by our group from wildlife and extensively farmed domestic animals (Gómez et al, 2014, 2015; Ruiz-Ripa et al, 2019) and one ST1945 MRSA strain from a human sample (Harrison et al, 2017); it is worth noting that all these IEC-positive isolates were of type-E (carrying the scn and sak genes)
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