Frontiers in Microbiology (Jun 2021)

Staphylococcus saprophyticus From Clinical and Environmental Origins Have Distinct Biofilm Composition

  • Opeyemi U. Lawal,
  • Opeyemi U. Lawal,
  • Marta Barata,
  • Maria J. Fraqueza,
  • Peder Worning,
  • Mette D. Bartels,
  • Luisa Goncalves,
  • Paulo Paixão,
  • Elsa Goncalves,
  • Cristina Toscano,
  • Joanna Empel,
  • Malgorzata Urbaś,
  • Maria A. Domiìnguez,
  • Henrik Westh,
  • Henrik Westh,
  • Hermínia de Lencastre,
  • Hermínia de Lencastre,
  • Maria Miragaia

DOI
https://doi.org/10.3389/fmicb.2021.663768
Journal volume & issue
Vol. 12

Abstract

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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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