Staphylococcus aureus biofilm matrix under bone environment influence

2020 ◽  
Author(s):  
Fabien Lamret ◽  
Jennifer Varin-Simon ◽  
Sophie Gangloff ◽  
Fany Reffuveille
Keyword(s):  
Staphylococcus Aureus ◽  
Bacterial Adhesion ◽  
Biofilm Formation ◽  
Matrix Composition ◽  
Magnesium Concentration ◽  
Bone Microenvironment ◽  
Low Oxygen ◽  
The Matrix ◽  
Main Components ◽  
Biofilm Matrix

<p>Bone and joint infections linked to implanted materials are mostly due to Staphylococcus aureus. Deciphering the biofilm structure appears to be a promising strategy to develop antibiofilm molecules in order to curb infection occurrence and the bacterial recurrence. Indeed, the characterization of biofilm architecture and physiology could help to find new therapeutic targets through notable quantification of the matrix main components. Our hypothesis is that the very complex and interconnected bone microenvironment influences the bacterial adhesion and biofilm maturation and so its composition.</p> <p>To identify the main factors influencing biofilm formation in the bone microenvironment, we determined biofilm biomass and the number of live adhered bacteria in a static model, completed with microscopy approaches to support our results. Different factors of bone microenvironment were tested: starvation, low oxygen rate, excess of magnesium, and presence of bone cell products. Our first results showed that MSSA or MRSA strains did not have the same behaviors under the tested conditions. However, for both types of strains, excess of magnesium combined to paucity of amino acids and oxygen increased the most the proportion of adhered Staphylococcus aureus (a 6 to 43 fold-increase, p = < 0.01). But biofilm biomass quantification and bacterial adhesion results showed divergent profiles leading us to think that matrix could be involved in such contrasts. Scanning electron microscopy highlighted several structures of matrix produced by these bacteria: well-known slime aspect, but also fibrous appearance, and no matrix production was revealed under some conditions. Indeed, all strains produced few matrix when cultured with control medium and oxygenated condition. Only CIP 53.154 strain built a strong slime-like matrix in response to oxygen depletion. However, both MSSA CIP 53.154 and SH1000 strains developed fibrous structures under anaerobic conditions associated with amino acid starvation, high magnesium concentration with or without glucose. MRSA USA300 strain did not seem to produce a matrix under our conditions, which is supported by the literature. Further investigations of the biofilm matrix are needed to conclude on the matrix nature, which surrounds bacteria under our conditions.</p> <p>The bone microenvironment is complex but our results show that the parameters that mimicked this specific environment influenced the bacterial adhesion and probably the biofilm matrix composition of several strains of Staphylococcus aureus. Further investigations will help to understand how the different factors influence biofilm formation through quantification of the matrix main components by fluorescence microscopy and enzyme digestion. Our final aim is to develop an in vitro model mimicking this specific microenvironment in order to screen different antimicrobial molecules, which could target the biofilm matrix.</p>

scholarly journals An Electrostatic Net Model for the Role of Extracellular DNA in Biofilm Formation by Staphylococcus aureus

2015 ◽  
Vol 197 (24) ◽  
pp. 3779-3787 ◽  
Author(s):  
Vanina Dengler ◽  
Lucy Foulston ◽  
Alicia S. DeFrancesco ◽  
Richard Losick
Keyword(s):  
Staphylococcus Aureus ◽  
Biofilm Formation ◽  
Extracellular Dna ◽  
Matrix Proteins ◽  
Exogenous Dna ◽  
Content Type ◽  
Cytoplasmic Proteins ◽  
The Matrix ◽  
Biofilm Matrix

ABSTRACTStaphylococcus aureusis an important human pathogen that can form biofilms on various surfaces. These cell communities are protected from the environment by a self-produced extracellular matrix composed of proteins, DNA, and polysaccharide. The exact compositions and roles of the different components are not fully understood. In this study, we investigated the role of extracellular DNA (eDNA) and its interaction with the recently identified cytoplasmic proteins that have a moonlighting role in the biofilm matrix. These matrix proteins associate with the cell surface upon the drop in pH that naturally occurs during biofilm formation, and we found here that this association is independent of eDNA. Conversely, the association of eDNA with the matrix was dependent on matrix proteins. Both proteinase and DNase treatments severely reduced clumping of resuspended biofilms; highlighting the importance of both proteins and eDNA in connecting cells together. By adding an excess of exogenous DNA to DNase-treated biofilm, clumping was partially restored, confirming the crucial role of eDNA in the interconnection of cells. On the basis of our results, we propose that eDNA acts as an electrostatic net, interconnecting cells surrounded by positively charged matrix proteins at a low pH.IMPORTANCEExtracellular DNA (eDNA) is an important component of the biofilm matrix of diverse bacteria, but its role in biofilm formation is not well understood. Here we report that inStaphylococcus aureus, eDNA associates with cells in a manner that depends on matrix proteins and that eDNA is required to link cells together in the biofilm. These results confirm previous studies that showed that eDNA is an important component of theS. aureusbiofilm matrix and also suggest that eDNA acts as an electrostatic net that tethers cells together via the proteinaceous layer of the biofilm matrix.

scholarly journals Conserved Role for Biofilm Matrix Polysaccharides in Candida auris Drug Resistance

mSphere ◽  
2019 ◽  
Vol 4 (1) ◽  
Author(s):  
E. G. Dominguez ◽  
R. Zarnowski ◽  
H. L. Choy ◽  
M. Zhao ◽  
H. Sanchez ◽  
...  
Keyword(s):  
Drug Resistance ◽  
Biofilm Formation ◽  
Resistance Mechanism ◽  
Matrix Composition ◽  
Candida Auris ◽  
Biofilm Growth ◽  
Content Type ◽  
The Matrix ◽  
And Function ◽  
Biofilm Matrix

ABSTRACT Candida auris has emerged as an outbreak pathogen associated with high mortality. Biofilm formation and linked drug resistance are common among Candida species. Drug sequestration by the biofilm matrix accounts for much of the antifungal tolerance. In this study, we examine the biofilm matrix composition and function for a diverse set of C. auris isolates. We show that matrix sequesters nearly 70% of the available triazole antifungal. Like the biofilms formed by other Candida spp., we find that the matrix of C. auris is rich in mannan-glucan polysaccharides and demonstrate that their hydrolysis reduces drug tolerance. This biofilm matrix resistance mechanism appears conserved among Candida species, including C. auris. IMPORTANCE Candida auris is an emerging fungal threat linked to poor patient outcomes. The factors responsible for this apparent increase in pathogenicity remain largely unknown. Biofilm formation has been suggested as an important factor for persistence of this organism in patients and the environment. Our findings reveal one mechanism utilized by C. auris to evade the effect of triazole antifungal therapy during biofilm growth. The conservation of the protective biofilm matrix among Candida spp. suggests that is a promising pan-fungal Candida biofilm drug target.

scholarly journals Enzymes Catalyzing the TCA- and Urea Cycle Influence the Matrix Composition of Biofilms Formed by Methicillin-Resistant Staphylococcus aureus USA300

2018 ◽  
Vol 6 (4) ◽  
pp. 113 ◽  
Author(s):  
Sarah De Backer ◽  
Julia Sabirova ◽  
Ines De Pauw ◽  
Henri De Greve ◽  
Jean-Pierre Hernalsteens ◽  
...  
Keyword(s):  
Staphylococcus Aureus ◽  
Urea Cycle ◽  
Citrate Synthase ◽  
Fumarate Hydratase ◽  
Tca Cycle ◽  
Matrix Composition ◽  
Methicillin Resistant ◽  
The Tca Cycle ◽  
The Matrix ◽  
Biofilm Matrix

In methicillin-sensitive Staphylococcus aureus (MSSA), the tricarboxylic acid (TCA) cycle is known to negatively regulate production of the major biofilm-matrix exopolysaccharide, PIA/PNAG. However, methicillin-resistant S. aureus (MRSA) produce a primarily proteinaceous biofilm matrix, and contribution of the TCA-cycle therein remains unclear. Utilizing USA300-JE2 Tn-mutants (NARSA) in genes encoding TCA- and urea cycle enzymes for transduction into a prolific biofilm-forming USA300 strain (UAS391-Erys), we studied the contribution of the TCA- and urea cycle and of proteins, eDNA and PIA/PNAG, to the matrix. Genes targeted in the urea cycle encoded argininosuccinate lyase and arginase (argH::Tn and rocF::Tn), and in the TCA-cycle encoded succinyl-CoA synthetase, succinate dehydrogenase, aconitase, isocitrate dehydrogenase, fumarate hydratase class II, and citrate synthase II (sucC::Tn, sdhA/B::Tn, acnA::Tn, icd::Tn, fumC::Tn and gltA::Tn). Biofilm formation was significantly decreased under no flow and flow conditions by argH::Tn, fumC::Tn, and sdhA/B::Tn (range OD492 0.374−0.667; integrated densities 2.065−4.875) compared to UAS391-EryS (OD492 0.814; integrated density 10.676) (p ≤ 0.008). Cellular and matrix stains, enzymatic treatment (Proteinase K, DNase I), and reverse-transcriptase PCR-based gene-expression analysis of fibronectin-binding proteins (fnbA/B) and the staphylococcal accessory regulator (sarA) on pre-formed UAS391-Erys and Tn-mutant biofilms showed: (i) < 1% PIA/PNAG in the proteinaceous/eDNA matrix; (ii) increased proteins under no flow and flow in the matrix of Tn mutant biofilms (on average 50 and 51 (±11)%) compared to UAS391-Erys (on average 22 and 25 (±4)%) (p < 0.001); and (iii) down- and up-regulation of fnbA/B and sarA, respectively, in Tn-mutants compared to UAS391-EryS (0.62-, 0.57-, and 2.23-fold on average). In conclusion, we show that the biofilm matrix of MRSA-USA300 and the corresponding Tn mutants is PIA/PNAG-independent and are mainly composed of proteins and eDNA. The primary impact of TCA-cycle inactivation was on the protein component of the biofilm matrix of MRSA-USA300.

scholarly journals Protein A-Mediated Multicellular Behavior in Staphylococcus aureus

2008 ◽  
Vol 191 (3) ◽  
pp. 832-843 ◽  
Author(s):  
Nekane Merino ◽  
Alejandro Toledo-Arana ◽  
Marta Vergara-Irigaray ◽  
Jaione Valle ◽  
Cristina Solano ◽  
...  
Keyword(s):  
Staphylococcus Aureus ◽  
Biofilm Formation ◽  
Protein A ◽  
Surface Proteins ◽  
Growth Media ◽  
Dependent Manner ◽  
Chronic Infections ◽  
The Matrix ◽  
Implanted Medical Devices ◽  
Biofilm Development

ABSTRACT The capacity of Staphylococcus aureus to form biofilms on host tissues and implanted medical devices is one of the major virulence traits underlying persistent and chronic infections. The matrix in which S. aureus cells are encased in a biofilm often consists of the polysaccharide intercellular adhesin (PIA) or poly-N-acetyl glucosamine (PNAG). However, surface proteins capable of promoting biofilm development in the absence of PIA/PNAG exopolysaccharide have been described. Here, we used two-dimensional nano-liquid chromatography and mass spectrometry to investigate the composition of a proteinaceous biofilm matrix and identified protein A (spa) as an essential component of the biofilm; protein A induced bacterial aggregation in liquid medium and biofilm formation under standing and flow conditions. Exogenous addition of synthetic protein A or supernatants containing secreted protein A to growth media induced biofilm development, indicating that protein A can promote biofilm development without being covalently anchored to the cell wall. Protein A-mediated biofilm formation was completely inhibited in a dose-dependent manner by addition of serum, purified immunoglobulin G, or anti-protein A-specific antibodies. A murine model of subcutaneous catheter infection unveiled a significant role for protein A in the development of biofilm-associated infections, as the amount of protein A-deficient bacteria recovered from the catheter was significantly lower than that of wild-type bacteria when both strains were used to coinfect the implanted medical device. Our results suggest a novel role for protein A complementary to its known capacity to interact with multiple immunologically important eukaryotic receptors.

scholarly journals Galactose Metabolism Plays a Crucial Role in Biofilm Formation by Bacillus subtilis

mBio ◽  
2012 ◽  
Vol 3 (4) ◽  
Author(s):  
Yunrong Chai ◽  
Pascale B. Beauregard ◽  
Hera Vlamakis ◽  
Richard Losick ◽  
Roberto Kolter
Keyword(s):  
Bacillus Subtilis ◽  
Biofilm Formation ◽  
Carbon Sources ◽  
Galactose Metabolism ◽  
Content Type ◽  
Leloir Pathway ◽  
The Matrix ◽  
Living Organisms ◽  
Galactose Metabolites ◽  
Biofilm Matrix

ABSTRACTGalactose is a common monosaccharide that can be utilized by all living organisms via the activities of three main enzymes that make up the Leloir pathway: GalK, GalT, and GalE. InBacillus subtilis, the absence of GalE causes sensitivity to exogenous galactose, leading to rapid cell lysis. This effect can be attributed to the accumulation of toxic galactose metabolites, since thegalEmutant is blocked in the final step of galactose catabolism. In a screen for suppressor mutants restoring viability to agalEnull mutant in the presence of galactose, we identified mutations insinR, which is the major biofilm repressor gene. These mutations caused an increase in the production of the exopolysaccharide (EPS) component of the biofilm matrix. We propose that UDP-galactose is the toxic galactose metabolite and that it is used in the synthesis of EPS. Thus, EPS production can function as a shunt mechanism for this toxic molecule. Additionally, we demonstrated that galactose metabolism genes play an essential role inB. subtilisbiofilm formation and that the expressions of both thegalandepsgenes are interrelated. Finally, we propose thatB. subtilisand other members of theBacillusgenus may have evolved to utilize naturally occurring polymers of galactose, such as galactan, as carbon sources.IMPORTANCEBacteria switch from unicellular to multicellular states by producing extracellular matrices that contain exopolysaccharides. In such aggregates, known as biofilms, bacteria are more resistant to antibiotics. This makes biofilms a serious problem in clinical settings. The resilience of biofilms makes them very useful in industrial settings. Thus, understanding the production of biofilm matrices is an important problem in microbiology. In studying the synthesis of the biofilm matrix ofBacillus subtilis, we provide further understanding of a long-standing microbiological observation that certain mutants defective in the utilization of galactose became sensitive to it. In this work, we show that the toxicity observed before was because cells were grown under conditions that were not propitious to produce the exopolysaccharide component of the matrix. When cells are grown under conditions that favor matrix production, the toxicity of galactose is relieved. This allowed us to demonstrate that galactose metabolism is essential for the synthesis of the extracellular matrix.

Decrypting the matrix: how interspecies interactions influence matrix in multispecies biofilm?

2020 ◽  
Author(s):  
Cristina Amador ◽  
Henriette L. Røder ◽  
Ute Kuhlicke ◽  
Thomas Neu ◽  
Mette Burmølle
Keyword(s):  
Single Species ◽  
Matrix Composition ◽  
Emergent Properties ◽  
Interspecies Interactions ◽  
Matrix Encoding ◽  
The Matrix ◽  
Static Conditions ◽  
Encoding Genes ◽  
Multispecies Biofilms ◽  
Biofilm Matrix

&lt;p&gt;The biofilm matrix contributes to the establishment of microbial cells on very diverse surfaces, stabilizing biofilms and providing cells with protection against multiple hostile conditions. Moreover, the biofilm matrix can also retain nutrients, enzymes or quorum sensing molecules, favoring the establishment of social interactions among biofilm cells. Functional bacterial amyloids are part of the biofilm structural components of various species, and they were previously proven to bind QS molecules and strengthen the matrix. Multiple studies have been conducted to characterize matrix determinants and their regulation in single species biofilms, while these remain scarcely understood in multispecies biofilms. We have previously isolated and characterized a soil-derived consortium composed of Xanthomonas retroflexus, Stenotrophomonas rhizophila, Microbacterium oxydans and Paenibacillus amylolyticus showing enhanced biofilm biomass and differential gene/protein expression specific of the four-species biofilm.&lt;/p&gt; &lt;p&gt;This study aimed at exploring the effect of interspecies interactions on biofilm matrix production in the four-species biofilm. We hypothesize that interspecies interactions may result in differential expression of matrix-encoding genes responsible for biofilm emergent properties.&lt;/p&gt; &lt;p&gt;We searched for matrix determinant homologues in X.retroflexus and combined different techniques for characterizing the matrix identity and expression in mono-, dual- and multispecies biofilms.&lt;/p&gt; &lt;p&gt;The fap amyloid operon, described in Pseudomonas as a biofilm-scaffold contributing element, was deleted in X. retroflexus, replaced in the four-species model and compared to the parental community for biofilm structure and adhesion capability. The fap mutant displayed poor substrate colonization in flow cells in both mono- and multispecies biofilms with relative filamentous structure compared to the parental strain/ consortium. However, adhesion did not significantly change under static conditions. To characterize matrix composition, we tested 78 different lectins in multispecies biofilms and identified five that bound to our samples. Interestingly, some matrix glycoconjugates were only produced in the consortium.&lt;/p&gt; &lt;p&gt;Our data suggest that loss of matrix components, such as the Fap amyloid, and the presence of other species, influences synergistic biofilm properties in the four-species consortium. Ongoing approaches involving localized expression of matrix-encoding genes and matrix proteomes will aid in identifying the mechanisms underlying emergent properties in the four-species biofilm.&lt;/p&gt; &lt;p&gt;&amp;#160;&lt;/p&gt;

scholarly journals Biofilm Production of Leptospira spp. Strains

2018 ◽  
Vol 46 (1) ◽  
pp. 5
Author(s):  
Dayane Olímpia Gomes ◽  
Laura Gonçalves da Silva Chagas ◽  
Gabriela Bim Ramos ◽  
Andreia Zago Ciuffa ◽  
Laís Miguel Rezende ◽  
...  
Keyword(s):  
Confocal Microscopy ◽  
Propidium Iodide ◽  
Biofilm Formation ◽  
Matrix Composition ◽  
Leptospira Interrogans ◽  
Biofilm Production ◽  
Leptospira Spp ◽  
The Matrix ◽  
Polypropylene Material ◽  
Pooled Sample

Background: Leptospirosis is a zoonosis that affects many species of mammals and occurs endemically in Brazil. The biofilm matrix provides structure and protection to the biofilm cells working as a physical barrier to antibiotic agents, which are attached or consumed by the matrix components. However, this attribute varies according to the matrix, antimicrobial agent and biofilm age. Leptospira may change morphologically according to environmental conditions, including cell aggregation and biofilm formation. Leptospira can colonize the ducts of kidney from hosts for a long time, forming a biofilm, which is believed to be an important factor for their maintenance in animals and in the environment. Thus, the objective of this research was to determine the biofilm formation capacity of four strains of Leptospira interrogans.Materials, Methods & Results: The strains were typified by WHO/FAO/OIE and National Collaborating Center for Reference and Research on Leptospirosis (Kit Biomedical Research, Amsterdam, Netherlands). Leptospira interrogans strains, two isolated from cattle and two isolated from dogs were biofilms tested for adhesion on polystyrene plates, extracellular matrix composition and confocal microscopy. In the plating adhesion test, the suspension was inoculated into 96-well sterile polystyrene microplates with flat bottom at a ratio of 1:200 in EMJH medium, followed by 24 h incubation at 28°C, with medium renewal after 12 h. After this period the wells were washed three times with sterile PBS and following incubation; the plates were dried in the oven at 60°C for 30 min and added 200 μL of 1% violet crystal for five min. Subsequently, the plates were washed with distilled water, after complete removal, 200 μL of acetic acid 33% was added and the readings were performed at 570 nm in the ELISA reader. The proteins and polysaccharides were quantified in a scraped pooled sample diluted in 0.85% sterile saline solution to achieve an optimal amount for testing used reagents of the BCA kit. The polysaccharide content was determined by adding into a tube, an aliquot of 0.5 mL from the pooled sample, 0.5 mL of phenol and then immediately 2.5 mL of sulfuric acid. The solution was homogenized and left to react for 15 min at room temperature. The reading was performed at 490 nm in ELISA reader. The strains were compared regarding polysaccharides and protein matrices using analysis of variance (ANOVA) and Tukey test. At confocal microscopy the strains were incubated with the tested polypropylene material for 24 h. The materials were washed with sterile phosphate buffer and stained with propidium iodide. The reading was performed using a Laser Scanning Confocal Microscope (Zeiss 710) with laser excitation (488 nm) and 580-680 nm emission filters for propidium iodide (red marking). All strains displayed strong adherence on microplate and the amount of polysaccharides in biofilm was not statistically different among the studied strains, but the amount of protein was significantly different in strain 4 (P > 0.5). The confocal microscopy showed the adherence of the Leptospira spp. strains to polypropylene material after washing.Discussion: Biofilm production plays an important role in the maintenance of a chronic infection by Leptospira interrogans with renal colonization. The exopolysaccharide (EPS) has various functions, such as checking insolubility in water; giving the three-dimensional conformation of the biofilm; protecting cells from physical (mechanical action, irradiation and temperature variations), chemical.

scholarly journals The Use of Zwitterionic Methylmethacrylat Coated Silicone Inhibits Bacterial Adhesion and Biofilm Formation of Staphylococcus aureus

2021 ◽  
Vol 9 ◽  
Author(s):  
Franziska Woitschach ◽  
Marlen Kloss ◽  
Karsten Schlodder ◽  
Anne Rabes ◽  
Caroline Mörke ◽  
...  
Keyword(s):  
Staphylococcus Aureus ◽  
Bacterial Adhesion ◽  
Biofilm Formation ◽  
Bacterial Colonization ◽  
Thermoplastic Polyurethane ◽  
Opportunistic Pathogens ◽  
Bacterial Strains ◽  
Liquid Silicone Rubber ◽  
Liquid Silicone ◽  
Biofilm Bacteria

In recent decades, biofilm-associated infections have become a major problem in many medical fields, leading to a high burden on patients and enormous costs for the healthcare system. Microbial infestations are caused by opportunistic pathogens which often enter the incision already during implantation. In the subsequently formed biofilm bacteria are protected from the hosts immune system and antibiotic action. Therefore, the development of modified, anti-microbial implant materials displays an indispensable task. Thermoplastic polyurethane (TPU) represents the state-of-the-art material in implant manufacturing. Due to the constantly growing areas of application and the associated necessary adjustments, the optimization of these materials is essential. In the present study, modified liquid silicone rubber (LSR) surfaces were compared with two of the most commonly used TPUs in terms of bacterial colonization and biofilm formation. The tests were conducted with the clinically relevant bacterial strains Staphylococcus aureus and Staphylococcus epidermidis. Crystal violet staining and scanning electron microscopy showed reduced adhesion of bacteria and thus biofilm formation on these new materials, suggesting that the investigated materials are promising candidates for implant manufacturing.

scholarly journals Hyaluronan Modulation Impacts Staphylococcus aureus Biofilm Infection

2016 ◽  
Vol 84 (6) ◽  
pp. 1917-1929 ◽  
Author(s):  
Carolyn B. Ibberson ◽  
Corey P. Parlet ◽  
Jakub Kwiecinski ◽  
Heidi A. Crosby ◽  
David K. Meyerholz ◽  
...  
Keyword(s):  
Staphylococcus Aureus ◽  
Biofilm Formation ◽  
Infection Model ◽  
Wild Type ◽  
Content Type ◽  
Joint Infections ◽  
The Impact ◽  
Biofilm Infection ◽  
Biofilm Matrix

Staphylococcus aureusis a leading cause of chronic biofilm infections. Hyaluronic acid (HA) is a large glycosaminoglycan abundant in mammalian tissues that has been shown to enhance biofilm formation in multiple Gram-positive pathogens. We observed that HA accumulated in anS. aureusbiofilm infection using a murine implant-associated infection model and that HA levels increased in a mutant strain lacking hyaluronidase (HysA).S. aureussecretes HysA in order to cleave HA during infection. Throughin vitrobiofilm studies with HA, thehysAmutant was found to accumulate increased biofilm biomass compared to the wild type, and confocal microscopy showed that HA is incorporated into the biofilm matrix. Exogenous addition of purified HysA enzyme dispersed HA-containing biofilms, while catalytically inactive enzyme had no impact. Additionally, induction ofhysAexpression prevented biofilm formation and also dispersed an established biofilm in the presence of HA. These observations were corroborated in the implant model, where there was decreased dissemination from anhysAmutant biofilm infection compared to theS. aureuswild type. Histopathology demonstrated that infection with anhysAmutant caused significantly reduced distribution of tissue inflammation compared to wild-type infection. To extend these studies, the impact of HA andS. aureusHysA on biofilm-like aggregates found in joint infections was examined. We found that HA contributes to the formation of synovial fluid aggregates, and HysA can disrupt aggregate formation. Taken together, these studies demonstrate that HA is a relevant component of theS. aureusbiofilm matrix and HysA is important for dissemination from a biofilm infection.

scholarly journals Staphylococcus saprophyticus From Clinical and Environmental Origins Have Distinct Biofilm Composition

2021 ◽  
Vol 12 ◽  
Author(s):  
Opeyemi U. Lawal ◽  
Marta Barata ◽  
Maria J. Fraqueza ◽  
Peder Worning ◽  
Mette D. Bartels ◽  
...  
Keyword(s):  
Biofilm Formation ◽  
Extracellular Dna ◽  
Matrix Composition ◽  
Comparative Genomic ◽  
Coagulase Negative Staphylococci ◽  
Structure Variation ◽  
Staphylococcus Saprophyticus ◽  
Biofilm Production ◽  
Tract Infections ◽  
Biofilm Matrix

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 &lt; 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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