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

TITLE=Staphylococcus saprophyticus From Clinical and Environmental Origins Have Distinct Biofilm Composition

JOURNAL=Frontiers in Microbiology

VOLUME=12

YEAR=2021

URL=https://www.frontiersin.org/journals/microbiology/articles/10.3389/fmicb.2021.663768

DOI=10.3389/fmicb.2021.663768

ISSN=1664-302X

ABSTRACT=<p>Biofilm formation has been shown to be critical to the success of uropathogens. Although <italic>Staphylococcus saprophyticus</italic> 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 <italic>S. saprophyticus</italic> (<italic>n</italic> = 422). Biofilm matrix composition was assessed in representative strains (<italic>n</italic> = 63) belonging to two main <italic>S. saprophyticus</italic> 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%; <italic>n</italic> = 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 (<italic>p</italic> &lt; 0.05). Putative biofilm-associated genes, namely, <italic>aas</italic>, <italic>atl</italic>, <italic>ebpS</italic>, <italic>uafA</italic>, <italic>sasF</italic>, <italic>sasD</italic>, <italic>sdrH</italic>, <italic>splE</italic>, <italic>sdrE</italic>, <italic>sdrC</italic>, <italic>sraP</italic>, and <italic>ica</italic> genes, were found with different frequencies (3–100%), but there was no correlation between their presence and biofilm production or matrix types. Notably, <italic>icaC_1</italic> was ubiquitous in the collection, while <italic>icaR</italic> was lineage G-associated, and only four strains carried a complete <italic>ica</italic> gene cluster (<italic>icaADBCR</italic>) except one that was without <italic>icaR</italic>. We provided evidence, using a comparative genomic approach, that the complete <italic>icaADBCR</italic> cluster was acquired multiple times by <italic>S. saprophyticus</italic> and originated from other coagulase-negative staphylococci. Overall, the composition of <italic>S. saprophyticus</italic> 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 <italic>S. saprophyticus</italic> is <italic>ica</italic>-independent, and the complete <italic>icaADBCR</italic> was acquired from other staphylococci.</p>