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Strain-Dependent Adsorption of Pseudomonas Aeruginosa- Derived Adhesin-Like Peptides at Abiotic Surfaces

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Strain-Dependent Adsorption of Pseudomonas Aeruginosa- Derived Adhesin-Like Peptides at Abiotic Surfaces micro Article Strain-Dependent Adsorption of Pseudomonas aeruginosa- Derived Adhesin-Like Peptides at Abiotic Surfaces Yu Yang, Sabrina Schwiderek, Guido Grundmeier and Adrian Keller * Technical and Macromolecular Chemistry, Paderborn University, Warburger Str. 100, 33098 Paderborn, Germany; [email protected] (Y.Y.); [email protected] (S.S.); [email protected] (G.G.) * Correspondence: [email protected] Abstract: Implant-associated infections are an increasingly severe burden on healthcare systems worldwide and many research activities currently focus on inhibiting microbial colonization of biomedically relevant surfaces. To obtain molecular-level understanding of the involved processes and interactions, we investigate the adsorption of synthetic adhesin-like peptide sequences derived from the type IV pili of the Pseudomonas aeruginosa strains PAK and PAO at abiotic model surfaces, i.e., Au, SiO2, and oxidized Ti. These peptides correspond to the sequences of the receptor-binding domain 128–144 of the major pilin protein, which is known to facilitate P. aeruginosa adhesion at biotic and abiotic surfaces. Using quartz crystal microbalance with dissipation monitoring (QCM-D), we find that peptide adsorption is material- as well as strain-dependent. At the Au surface, PAO(128–144) shows drastically stronger adsorption than PAK(128–144), whereas adsorption of both peptides is markedly reduced at the oxide surfaces with less drastic differences between the two sequences. These observations suggest that peptide adsorption is influenced by not only the peptide sequence, Citation: Yang, Y.; Schwiderek, S.; but also peptide conformation. Our results furthermore highlight the importance of molecular-level Grundmeier, G.; Keller, A. investigations to understand and ultimately control microbial colonization of surfaces. Strain-Dependent Adsorption of Pseudomonas aeruginosa-Derived Keywords: adsorption; peptide; microbial adhesion; biofilm; quartz crystal microbalance Adhesin-Like Peptides at Abiotic Surfaces. Micro 2021, 1, 129–139. https://doi.org/10.3390/ micro1010010 1. Introduction Academic Editor: Giulia Ronchi The past century has seen a continuous increase in the number of surgical procedures aimed at the restoration of body functions via the implantation of artificial biomaterials. Received: 15 June 2021 While tremendous advances in the fields of reconstructive medicine and biomaterials Accepted: 27 July 2021 science and engineering have resulted in highly efficient implants with low probability Published: 31 July 2021 of rejection by the body, implant-associated infections have developed into a serious problem over the last two decades [1]. All implants from heart valves and prosthetic Publisher’s Note: MDPI stays neutral joints to vascular prostheses and dental implants attract microorganisms and thus exhibit with regard to jurisdictional claims in a certain risk of deep infection [2]. Due to the rapid spreading of antimicrobial-resistant published maps and institutional affil- pathogens [3–5], implant-associated infections represent an increasingly severe burden on iations. healthcare systems worldwide. For the US alone, it was estimated that the total number of infected total hip and total knee arthroplasties will increase from 8326 in 2010 to 37,059 in 2030, corresponding to additional costs resulting only from these two procedures of up to US$ 5 billion [6]. Suppressing implant-associated infections via the rational engineering Copyright: © 2021 by the authors. of implant surfaces to render them resistant to microbial colonization has thus become a Licensee MDPI, Basel, Switzerland. very important goal in the field of biomedical materials research [7]. For such engineering This article is an open access article strategies to succeed, however, a detailed understanding of the molecular mechanisms that distributed under the terms and govern microbial colonization of abiotic surfaces is required. conditions of the Creative Commons One of the most common nosocomial pathogens encountered in healthcare settings Attribution (CC BY) license (https:// all over the world is the Gram-negative bacterium Pseudomonas aeruginosa. P. aeruginosa creativecommons.org/licenses/by/ infections are particularly hard to treat and associated with exceptionally high mortality 4.0/). Micro 2021, 1, 129–139. https://doi.org/10.3390/micro1010010 https://www.mdpi.com/journal/micro Micro 2021, 1, FOR PEER REVIEW 2 Micro 2021, 1 130 infections are particularly hard to treat and associated with exceptionally high mortality ratesrates [8]. [8]. This This is isbecause because of ofthe the intrinsic intrinsic high high resistance resistance of P. of aeruginosaP. aeruginosa to manyto many antimi- an- crobialstimicrobials and its and remarkable its remarkable ability ability to acquire to acquire additional additional mechanisms mechanisms of resistance of resistance to mul- to tiplemultiple groups groups of antimicrobials of antimicrobials [9]. Pandrug-resistant [9]. Pandrug-resistant strains strains that do that not do respond not respond to any to availableany available antimicrobial antimicrobial are an are increasing an increasing problem problem worldwide worldwide [8,9]. Consequently, [8,9]. Consequently, in 2017, in carbapenem-resistant2017, carbapenem-resistant P. aeruginosaP. aeruginosa was rankedwas ranked second secondon the WHO on the priority WHOpriority list of antimi- list of crobial-resistantantimicrobial-resistant bacteria bacteria [10]. [10]. WhenWhen colonizing colonizing surfaces, surfaces, P. aeruginosa relies predominantlypredominantly onon dynamicdynamic proteinprotein fila-fil- amentsments called called type type IVIV pilipili (see(see FigureFigure1 1a)a) that that facilitate facilitate initial initial adhesionadhesion asas wellwell asas migrationmigration andand motility motility of of the the adhering bacteria bacteria [11–13]. [11–13]. Each Each of of these these filaments filaments is is anchored anchored in in the innerinner membrane membrane and and consists consists of of several several thousand thousand copies copies of of a a single single protein protein subunit subunit called called pilinpilin (see (see Figure Figure 1b).1b). These These type type IV IV pilins pilins are are structurally structurally highly highly conserved conserved in indifferent different P. aeruginosaP. aeruginosa strainsstrains and and also also other other bacteria bacteria [12–15]. [12–15 Of]. particular Of particular medical medical importance importance is the is C-terminalthe C-terminal D-region, D-region, which which contains contains a loop a loopstructure structure defined defined by a bydisulfide a disulfide bridge bridge (see Figure(see Figure 1b) and1b) andfacilitates facilitates adherence adherence to host-cell to host-cell epithelia epithelia [12,13]. [ 12 However,,13]. However, Giltner Giltner et al. demonstratedet al. demonstrated that this that receptor-binding this receptor-binding domain domain between between residues residues 128 and128 144 andis also 144 in- is volvedalso involved in P. aeruginosa in P. aeruginosa adhesionadhesion to abiotic to abiotic surfaces surfaces and in andparticular in particular stainless stainless steel, poly- steel, styrene,polystyrene, and polyvinylchloride and polyvinylchloride [14]. Therefore, [14]. Therefore, in this work, in this we work, investigate we investigate the adsorption the ad- ofsorption synthetic of syntheticpeptide sequences peptide sequences correspond correspondinging to the receptor-binding to the receptor-binding domains of domains P. aeru- ginosaof P. aeruginosa pilins at abioticpilins atmodel abiotic surfaces, model i.e., surfaces, Au, SiO i.e.,2, Au,and SiOoxidized2, and Ti oxidized (TiOx/Ti). Ti While (TiOx/Ti). Au isWhile used Au as isa well-defined, used as a well-defined, inert reference inert referencesurface, SiO surface,2 and SiOTiO2x/Tiand films TiO xserve/Ti films as model serve surfacesas model for surfaces implants for based implants on bioactive based on glasses bioactive [16] and glasses titanium [16] and alloys titanium [17], respectively. alloys [17], Sincerespectively. the receptor-binding Since the receptor-binding domain shows domain considerable shows sequence considerable variability sequence between variability dif- ferentbetween P. aeruginosa different P.strains, aeruginosa we arestrains, comparing we are the comparing adsorption the of adsorption two peptides of derived two peptides from twoderived different from strains, two different i.e., PAK strains, and PAO i.e., PAK (see andFigure PAO 1c). (see Using Figure quartz1c). crystal Using quartzmicrobalance crystal withmicrobalance dissipation with monitoring dissipation (QCM-D), monitoring we (QCM-D),find that peptide we find adsorption that peptide is not adsorption only sur- is face-dependent,not only surface-dependent, but also strain-dependent. but also strain-dependent. In particular, In particular,PAO(128–144) PAO(128–144) shows stronger shows adsorptionstronger adsorption at Au surfaces at Au than surfaces PAK(128–144), than PAK(128–144), whereas whereasat the oxide at the surfaces, oxide surfaces, adsorption ad- ofsorption both peptides of both is peptides markedly is markedly reduced and reduced almost and negligible. almost negligible. Our results Our suggest results that suggest pep- tidethat adsorption peptide adsorption at these surfaces at these is surfaces influenc ised influenced not only notby the only peptide by the sequence, peptide sequence, but
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