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Staphylococcal Biofilm on the Surface of Catheters: Electron Microscopy

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Staphylococcal Biofilm on the Surface of Catheters: Electron Microscopy antibiotics Article Staphylococcal Biofilm on the Surface of Catheters: Electron Microscopy Evaluation of the Inhibition of Biofilm Growth by RNAIII Inhibiting Peptide Adilson de Oliveira 1, Luiza Pinheiro-Hubinger 2,* , Valéria Cataneli Pereira 1 , Danilo Flávio Moraes Riboli 1, Katheryne Benini Martins 1 , Letícia Calixto Romero 1 and Maria de Lourdes Ribeiro de Souza da Cunha 1 1 Department of Chemical and Biological Sciences, Biosciences Institute, UNESP—Universidade Estadual Paulista, Botucatu 18618-691, Brazil; [email protected] (A.d.O.); [email protected] (V.C.P.); [email protected] (D.F.M.R.); [email protected] (K.B.M.); [email protected] (L.C.R.); [email protected] (M.d.L.R.d.S.d.C.) 2 Department of Anatomic Pathology, Lauro de Souza Lima Institute, Bauru 17034-971, Brazil * Correspondence: [email protected]; Tel.: +55-(0)14-38800428 Abstract: Staphylococcus aureus and coagulase-negative staphylococci (CoNS) have become the main causative agents of medical device-related infections due to their biofilm-forming capability, which protects them from the host’s immune system and from the action of antimicrobials. This Citation: de Oliveira, A.; study evaluated the ability of RNA III inhibiting peptide (RIP) to inhibit biofilm formation in Pinheiro-Hubinger, L.; Pereira, V.C.; 10 strains isolated from clinical materials, including one S. aureus strain, two S. epidermidis, two Riboli, D.F.M.; Martins, K.B.; Romero, S. haemolyticus, two S. lugdunensis, and one isolate each of the following species: S. warneri, S. hominis, L.C.; Cunha, M.d.L.R.d.S.d. and S. saprophyticus. The isolates were selected from a total of 200 strains evaluated regarding Staphylococcal Biofilm on the Surface phenotypic biofilm production and the presence and expression of the ica operon. The isolates were of Catheters: Electron Microscopy cultured in trypticase soy broth with 2% glucose in 96-well polystyrene plates containing catheter Evaluation of the Inhibition of Biofilm segments in the presence and absence of RIP. The catheter segments were observed by scanning Growth by RNAIII Inhibiting Peptide. electron microscopy. The results showed inhibition of biofilm formation in the presence of RIP in all Antibiotics 2021, 10, 879. https:// CoNS isolates; however, RIP did not interfere with biofilm formation by S. aureus. RIP is a promising doi.org/10.3390/antibiotics10070879 tool that might be used in the future for the prevention of biofilm-related infections caused by CoNS. Academic Editors: Débora Keywords: Staphylococcus aureus; coagulase-negative staphylococci; biofilm structure; quorum sens- C. Coraça-Huber, Eliana Aparecida de Rezende Duek and Marina ing; catheter; RIP; biofilm inhibition; scanning electron microscopy Angélica Marciano da Silva Received: 25 March 2021 Accepted: 11 May 2021 1. Introduction Published: 20 July 2021 Medical device-related infections are associated with the capability of bacteria to ad- here and attach to surfaces and to subsequently form a biofilm [1,2]. Biofilms are composed Publisher’s Note: MDPI stays neutral of communities of microorganisms enveloped by an extracellular matrix consisting of with regard to jurisdictional claims in polysaccharides or proteins produced by the bacteria themselves, which remain adhered to published maps and institutional affil- abiotic or biotic surfaces [3,4]. The bacteria present inside the biofilm may have a different iations. virulence and resistance phenotype in terms of gene transcription and growth rate [5]. Biofilms are considered one of the most important virulence factors in S. aureus and are the most important virulence factor in the majority of coagulase-negative staphylococci (CoNS), especially S. epidermidis, protecting them from the host’s immune system and from Copyright: © 2021 by the authors. the action of antibiotics [5,6]. The composition of the biofilm matrix varies among staphy- Licensee MDPI, Basel, Switzerland. lococcal strains; however, the main class of exopolysaccharides in staphylococcal biofilms This article is an open access article is polysaccharide intercellular adhesin (PIA), which is synthesized by four proteins, IcaA, distributed under the terms and IcaD, IcaB, and IcaC, encoded by the icaADBC operon [7–9]. conditions of the Creative Commons Biofilm formation depends on the combination and expression of a variety of genes, Attribution (CC BY) license (https:// whose expression is influenced by environmental factors such as growth conditions, car- creativecommons.org/licenses/by/ bohydrate supplementation, sub-inhibitory concentrations of antimicrobials, and high 4.0/). Antibiotics 2021, 10, 879. https://doi.org/10.3390/antibiotics10070879 https://www.mdpi.com/journal/antibiotics Antibiotics 2021, 10, x FOR PEER REVIEW 2 of 14 Biofilm formation depends on the combination and expression of a variety of genes, whose expression is influenced by environmental factors such as growth conditions, Antibiotics 2021, 10, 879 2 of 13 carbohydrate supplementation, sub-inhibitory concentrations of antimicrobials, and high osmolarity. The bacteria use a cellular communication system called quorum sensing (QS) for this regulation, which works as a population density sensor [10,11]. This osmolarity.communication The bacteriais mediated use aby cellular signaling communication molecules called system autoinducers called quorum that sensingregulate (QS) the forbehavior this regulation, of bacteria which in response works to as populati a populationon density. density When sensor a smal [10,l11 number]. This of communi- bacteria cationreleases is autoinducers mediated by signalinginto the environment, molecules called their autoinducersconcentration that is too regulate low to the be behaviordetected. ofHowever, bacteria when in response the population to population density density. is high When, the concentration a small number of autoinducers of bacteria releases reaches autoinducersa threshold that into induces the environment, cells to respond their concentration to stimuli, activating is too low or torepr beessing detected. target However, genes. whenThis system the population thus allows density the is high,bacteria the concentrationto coordinate of their autoinducers behavior reaches according a threshold to the thatenvironmental induces cells conditions, to respond as to well stimuli, as activatingthe expression or repressing of virulence target genes.factors, This biofilm sys- temformation, thus allows and others the bacteria [12]. to coordinate their behavior according to the environmental conditions,Balaban as et well al. [13], as the studying expression a peptide of virulence (YSPWTNF-NH2) factors, biofilm known formation, as RNAIII and others inhibiting [12]. peptideBalaban (RIP), et found al. [13 that], studying it can inhibit a peptide RNA (YSPWTNF-NH2)III activity by hindering known asthe RNAIII phosphorylation inhibiting peptideof TRAP, (RIP), interrupting found that the it canexpression inhibit RNAIIIof virulence activity factors, by hindering including the biofilm phosphorylation formation of(Figure TRAP, 1). interrupting Studies conducted the expression on catheter of virulenceimplanted factors, animals including in order biofilmto observe formation biofilm (Figureformation1). Studieshave shown conducted that the on injection catheter of implanted RIP resulted animals in low in orderbiofilm to production observe biofilm and a formationlow frequency have of shown infections that the[14]. injection Other studies of RIP resulteddemonstrated in low that, biofilm in productionaddition to andbeing a lowvery frequency effective ofin infectionspreventing [14 ].device-related Other studies Staphylococcus demonstrated that,infections, in addition RIP toalso being reduces very effectivebacterial inload preventing and can be device-related useful for theStaphylococcus treatment of infectedinfections, wounds RIP also [15]. reduces Thus, RIP bacterial might loadbe in andthe future can be an useful interesting for the alternative treatment ofto conventional infected wounds antibiotics. [15]. Thus, However, RIP might according be in theto some future authors, an interesting the TRAP alternative system does to conventional not participate antibiotics. in the activation However, of the according agr system to someand hence authors, plays the no TRAP role systemin the path doesogenesis not participate of diseases in the caused activation by Staphylococcus of the agr system [16,17]. and hence plays no role in the pathogenesis of diseases caused by Staphylococcus [16,17]. Figure 1. Schematic representation of agr control in staphylococci. As the bacteria multiply, RAP reachesFigure 1. a Schematic concentration representation threshold, inducingof agr control the phosphorylation in staphylococci. of As TRAP the bacteria that triggers multiply, a poorly RAP reaches a concentration threshold, inducing the phosphorylation of TRAP that triggers a poorly known mechanism for the synthesis of QSII, which consists of the products of the agr system. The known mechanism for the synthesis of QSII, which consists of the products of the agr system. The agr system is composed of two divergent transcripts, RNAII and RNAIII. RNAII encodes AgrA, agr system is composed of two divergent transcripts, RNAII and RNAIII. RNAII encodes AgrA, AgrC, AgrD, andand AgrB.AgrB. AgrDAgrD producesproduces autoinducingautoinducing peptide (AIP) that isis processedprocessed byby AgrBAgrB maturation and export. At a certai certainn threshold concentration,concentration, AIP induces
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