Foodborne Origin and Local and Global Spread of <i>Staphylococcus saprophyticus</i> Causing Human Urinary Tract Infections

Lawal, Opeyemi U; Fraqueza, Maria João; Bouchami, Ons; Worning, Peder; Bartels, Mette Damkjær; Gonçalves, Maria Luísa; Paixão, Paulo; Gonçalves, Elsa; Toscano, Cristina; Empel, Joanna; Urbaś, Małgorzata; Domínguez, M. Ángeles; Westh, Henrik; Lencastre, Hermı́nia de; Miragaia, Maria

doi:10.3201/eid2703.200852

Cited by 30 publications

(36 citation statements)

References 48 publications

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“…We assembled a large collection of 422 Staphylococcus saprophyticus isolates recovered in seven countries from human infection and colonization as well as food-related environment between 1997 and 2017 ( Supplementary Table 1 ). Out of a total number of biofilm producers ( n = 384), we selected 63 strains with high biofilm production representing the different phylogenetic clusters identified when isolates were studied by single-nucleotide polymorphism (SNP) analysis ( Lawal et al, 2021a ). The selected isolates comprised isolates from both clonal lineages G ( n = 42) and S ( n = 21; Supplementary Figure 1 ).…”

Section: Methodsmentioning

confidence: 99%

“…Paired-end sequence reads produced on an Illumina MiSeq with an average coverage of 103 per genome reported in Lawal et al (2021a) with the accession number PRJNA604222 were retrieved from sequence read archives. Low Q-score ends (Q < 20) were trimmed of the Illumina reads using Trimmomatic v0.36 ( Bolger et al, 2014 ).…”

Section: Methodsmentioning

confidence: 99%

“…A recent study showed that S. saprophyticus causing UTI in humans belonged to two major clonal lineages (G and S) that originated in food/production animals and humans, respectively, ( Lawal et al, 2021a ). However, it is still unknown if the mechanisms of disease caused by the two lineages are related.…”

Section: Introductionmentioning

confidence: 99%

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Staphylococcus saprophyticus From Clinical and Environmental Origins Have Distinct Biofilm Composition

et al. 2021

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Biofilm formation has been shown to be critical to the success of uropathogens. Although Staphylococcus saprophyticus is a common cause of urinary tract infections, its biofilm production capacity, composition, genetic basis, and origin are poorly understood. We investigated biofilm formation in a large and diverse collection of S. saprophyticus (n = 422). Biofilm matrix composition was assessed in representative strains (n = 63) belonging to two main S. saprophyticus lineages (G and S) recovered from human infection, colonization, and food-related environment using biofilm detachment approach. To identify factors that could be associated with biofilm formation and structure variation, we used a pangenome-wide association study approach. Almost all the isolates (91%; n = 384/422) produced biofilm. Among the 63 representative strains, we identified eight biofilm matrix phenotypes, but the most common were composed of protein or protein–extracellular DNA (eDNA)–polysaccharides (38%, 24/63 each). Biofilms containing protein–eDNA–polysaccharides were linked to lineage G and environmental isolates, whereas protein-based biofilms were produced by lineage S and infection isolates (p < 0.05). Putative biofilm-associated genes, namely, aas, atl, ebpS, uafA, sasF, sasD, sdrH, splE, sdrE, sdrC, sraP, and ica genes, were found with different frequencies (3–100%), but there was no correlation between their presence and biofilm production or matrix types. Notably, icaC_1 was ubiquitous in the collection, while icaR was lineage G-associated, and only four strains carried a complete ica gene cluster (icaADBCR) except one that was without icaR. We provided evidence, using a comparative genomic approach, that the complete icaADBCR cluster was acquired multiple times by S. saprophyticus and originated from other coagulase-negative staphylococci. Overall, the composition of S. saprophyticus biofilms was distinct in environmental and clinical isolates, suggesting that modulation of biofilm structure could be a key step in the pathogenicity of these bacteria. Moreover, biofilm production in S. saprophyticus is ica-independent, and the complete icaADBCR was acquired from other staphylococci.

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Section: Methodsmentioning

confidence: 99%

Section: Methodsmentioning

confidence: 99%

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Staphylococcus saprophyticus From Clinical and Environmental Origins Have Distinct Biofilm Composition

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“…Staphylococcus epidermidis and Staphylococcus haemolyticus are most commonly associated with infections of indwelling or implanted foreign bodies ( Ahmed et al 2019 ; Both et al 2021 ). Staphylococcus saprophyticus is the common cause of urinary tract infections ( Widerström et al 2007 ; Lawal et al 2021 ), whereas Staphylococcus lugdunensis can cause infectious endocarditis ( Non and Santos 2017 ). Staphylococcus capitis has been implicated in sepsis in preterm infants in neonatal intensive care units ( Stenmark et al 2019 ; Wirth et al 2020 ).…”

Section: Introductionmentioning

confidence: 99%

Extensive Horizontal Gene Transfer within and between Species of Coagulase-Negative Staphylococcus

Smith

Andam

2021

Genome Biology and Evolution

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Members of the gram-positive bacterial genus Staphylococcus have historically been classified into coagulase-positive Staphylococcus (CoPS) and coagulase-negative Staphylococcus (CoNS) based on the diagnostic presentation of the coagulase protein. Previous studies have noted the importance of horizontal gene transfer (HGT) and recombination in the more well-known CoPS species Staphylococcus aureus, yet little is known of the contributions of these processes in CoNS evolution. In this study, we aimed to elucidate the phylogenetic relationships, genomic characteristics and frequencies of HGT in CoNS, which are now being recognized as major opportunistic pathogens of humans. We compiled a dataset of 1,876 publicly available named CoNS genomes. These can be delineated into 55 species based on allele differences in 462 core genes and variation in accessory gene content. CoNS species are a reservoir of transferrable genes associated with resistance to diverse classes of antimicrobials. We also identified nine types of the mobile genetic element SCCmec, which carries the methicillin resistance determinant mecA. Other frequently transferred genes included those associated with resistance to heavy metals, surface-associated proteins related to virulence and biofilm formation, type VII secretion system, iron capture, recombination and metabolic enzymes. The highest frequencies of receipt and donation of recombined DNA fragments were observed in Staphylococcus capitis, Staphylococcus caprae, Staphylococcus hominis, Staphylococcus haemolyticus and members of the Saprophyticus species group. The variable rates of recombination and biases in transfer partners imply that certain CoNS species function as hubs of gene flow and major reservoir of genetic diversity for the entire genus.

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“…We have previously defined the population structure of S. saprophyticus and identified two clonal lineages, lineages G and S, that were disseminated worldwide and had distinctive genetic features. We also provided evidence for a possible animal origin for lineage G and human origin for lineage S (26). In this study, the analysis of an S. saprophyticus collection of diverse origins by phenotypic and genomic tools allowed us to determine the MIC of S. saprophyticus to four heavy metals, assess the distribution of metal resistance determinants among the S. saprophyticus population, and identify previously unknown associations between specific genetic determinants, metal resistance, and pathogenicity in this bacterial species.…”

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confidence: 99%

Staphylococcus saprophyticus Causing Infections in Humans Is Associated with High Resistance to Heavy Metals

Lawal

Fraqueza

Worning

et al. 2021

Antimicrob Agents Chemother

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Staphylococcus saprophyticus is a common pathogen of the urinary tract, a heavy metal-rich environment, but information regarding its heavy metal resistance is unknown. We investigated 422 S. saprophyticus isolates from human infection and colonization/contamination, animals, and environmental sources for resistance to copper, zinc, arsenic and cadmium using agar dilution method. To identify the genes associated with metal resistance and assess possible links to pathogenicity, we accessed the whole-genome sequence of all isolates and used in-silico and pangenome-wide association approaches. The MIC values for copper and zinc were uniformly high (1,600 mg/L). Genes encoding copper efflux pumps (copA, copB, copZ, mco, and csoR) and zinc transporters (zinT, czrAB, znuBC, and zur) were abundant in the population (20-100%). Arsenic and cadmium showed various susceptibility levels. Genes encoding the ars operon (arsRDABC), an ABC transporter and a two-component permease were linked to resistance to arsenic (≥1,600 mg/L, 14%; 58/422, p<0.05). At least three cad-genes (cadA or cadC and cadD-cadX or czrC) and genes encoding multidrug efflux pumps and hyper-osmoregulation in acidified conditions were associated with resistance to cadmium (≥200 mg/L, 20% (85/422)) (p <0.05). These resistance genes were frequently carried by mobile genetic elements. Resistance to arsenic and cadmium were linked to human infection and to a clonal lineage originating in animals (p <0.05). Altogether, S. saprophyticus were highly resistant to heavy metals and accumulated multiple metal resistance determinants. The highest arsenic and cadmium resistance levels were associated with infection, suggesting resistance to these metals are relevant for S. saprophyticus pathogenicity.

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Foodborne Origin and Local and Global Spread of Staphylococcus saprophyticus Causing Human Urinary Tract Infections

Cited by 30 publications

References 48 publications

Staphylococcus saprophyticus From Clinical and Environmental Origins Have Distinct Biofilm Composition

Staphylococcus saprophyticus From Clinical and Environmental Origins Have Distinct Biofilm Composition

Extensive Horizontal Gene Transfer within and between Species of Coagulase-Negative Staphylococcus

Staphylococcus saprophyticus Causing Infections in Humans Is Associated with High Resistance to Heavy Metals

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