Search

Staphylococcus aureusremains one of the leading causes of infections worldwide and a common cause of bacteremia. However, studies documenting the epidemiology ofS. aureusin South America (SA) using genomics are scarce. We hereby report on the largest to date genomic epidemiology study of both methicillin-resistantS. aureus(MRSA) and methicillin-susceptibleS. aureus(MSSA) in SA, conducted by the StaphNET-SA network. We characterised 404 genomes recovered from a prospective observational study ofS. aureusbacteremia in 58 hospitals from Argentina, Bolivia, Brazil, Paraguay and Uruguay between April and October 2019.We show that a minority ofS. aureusisolates are phenotypically multi-drug resistant (5.2%), but more than a quarter are resistant to macrolide-lincosamide-streptogramin B (MLSb). MSSA were more genetically diverse than MRSA. Lower rates of associated antimicrobial resistance in CA-MRSA vs HA-MRSA were found in association with threeS. aureusgenotypes dominating the MRSA population: CC30-MRSA-IVc-t019-lukS/F-PV+, CC5-MRSA-IV-t002-lukS/F-PV-, and CC8-MRSA-IVc-t008-lukS/F-PV+-COMER+. These are historically from a CA origin, carry on average less AMR determinants, and often lack key virulence genes.Surprisingly, CC398-MSSA-t1451-lukS/F-PV-related to the CC398 human-associated lineage is widely disseminated throughout the region, and is described here for the first time as the most prevalent MSSA lineage in SA. Moreover, CC398 strains carryingermTandsh_fabI(related to triclosan resistance) were recovered from both CA and HA origin, and are largely responsible for the MLSb rates of MSSA strains (inducible iMLSb phenotype).The frequency of MRSA and MSSA lineages differed between countries but the most prevalentS. aureusgenotypes are high-risk clones widespread in the South American region without clear country-specific phylogeographic structure. Therefore our findings underscore the need for continuous genomic surveillance by regional networks such as StaphNET-SA.Impact statementS. aureusis a common cause of bacteremia, a serious life threatening disease, and the second leading pathogen for deaths associated with resistance in 2019. However, genomic surveillance ofS. aureuscausing invasive infections in South America is limited. Previous surveillance studies have focused on the dissemination of MRSA with increasing AMR and/or virulence, but have not characterised MSSA in detail.Here, we show the results of a prospective observational study of genomic surveillance ofS. aureuscausing bacteremia conducted in South America during 2019 by the StaphNET-SA network.Our study reveals that in 2019 most bloodstream infections were caused by successful MRSA lineages of community origin, generally not MDR, and lacking key virulence genes in some cases. Importantly, we also describe here for the first time CC398-MSSA-t1451as the most prevalent and widely disseminated MSSA clone causing bacteraemia in the region during 2019. This human adapted clone, present both in the community and hospital environment, carries a gene conferring resistance against an antiseptic widely used in our region, and is largely responsible for the increasing resistance rates to erythromycin and clindamycin observed in MSSA.We also show evidence of readily transmission of the most prevalent MRSA and MSSA high-risk clones across country borders, which highlights the need for continuous genomic surveillance by regional networks such as StaphNET-SA.Data SummaryAll supporting data, code and protocols have been provided within the article or through supplementary data files. Five supplementary figures and five supplementary tables are available with the online version of this article.Sequence read files for all samples used in this study have been deposited in the European Nucleotide Archive under the project accession number PRJEB37318. Individual accession numbers for each sample are also detailed in microreact_project:https://microreact.org/project/staphnet-sa-1st-survey. Genome assemblies are available via Pathogenwatchhttps://pathogen.watch/collection/jz7rcy1zv0sk-staphnet-sa-first-survey.

Staphylococcus aureus clonal complex 30 (CC30) has given rise to epidemics worldwide and is one of the most prevalent lineages in Argentina, represented by sequence type 30 methicillin-resistant S. aureus SCCmec type IV (ST30-MRSA-IV). ST30-MRSA-IV has displaced previous prevalent clones in the country and demonstrated increased virulence. Despite the burden of infections caused by ST30-MRSA-IV both in hospitals and in communities in Argentina, no detailed genome-based characterization of this clone is available to date. In this study, we used whole-genome sequencing (WGS) to evaluate the genetic diversity, population structure, and genomic characteristics of 190 CC30-MRSA strains circulating in Argentina between 2004 and 2015. Phylogenetic analysis revealed the existence of 4 major clades: ARG-1 (CC30-MRSA-IVc-spa t012), ARG-2 (ST30-MRSA-IVc-spa t021 related), ARG-3 (ST30-MRSA-IVh/j-spa t021 and related), and ARG-4 (CC30-MRSA-IVc-spa t019 and related). The clades were characterized by different distributions of antimicrobial resistance determinants, virulence genes, and mobile genetic elements (MGEs). While ARG-1 and ARG-4 were related to global epidemic MRSA-16 (EMRSA-16) and South West Pacific (SWP) clones, respectively, ARG-3 was phylogenetically distinct from previously defined CC30 epidemic clones. ARG-4, the most prevalent and geographically disseminated in the collection (N = 164), was characterized by specific MGEs and chromosomal mutations that might have contributed to its virulence and success. To our knowledge, this is the first genomic epidemiology study of CC30-MRSA in Argentina, which will serve as baseline genomic data going forward to inform public health measures for infection prevention and control. IMPORTANCE The rise in prevalence of community-associated methicillin-resistant Staphylococcus aureus (CA-MRSA) is of public health concern. In Argentina, several studies documented a shift in the epidemiology of CA-MRSA since 2009, with clonal complex 30 (CC30) and, in particular, sequence type 30 MRSA SCCmec type IV (ST30-MRSA-IV) replacing other clones both in communities and in hospitals and possibly displaying increased virulence. By sequencing the whole genomes of 190 CC30 MRSA isolates recovered from Argentina between 2005 and 2015, we showed that they represented a diverse population composed of 4 major clades. The predominant clade evolved from the South West Pacific clone but has acquired a distinct repertoire of mobile genetic elements, virulence genes, and chromosomal mutations that might play a role in its success. Our work is the first extensive genomic study of CC30 S. aureus in Argentina and will contribute not only to the development of genomic surveillance in the region but also to our understanding of the global epidemiology of this pathogen.