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Subtilase Sprp Exerts Pleiotropic Effects in Pseudomonas Aeruginosa

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Subtilase Sprp Exerts Pleiotropic Effects in Pseudomonas Aeruginosa ORIGINAL RESEARCH Subtilase SprP exerts pleiotropic effects in Pseudomonas aeruginosa Alexander Pelzer1, Tino Polen2, Horst Funken1, Frank Rosenau3, Susanne Wilhelm1, Michael Bott2 & Karl-Erich Jaeger1 1Institute of Molecular Enzyme Technology, Research Centre Juelich, Heinrich-Heine-University Duesseldorf, D-52426 Juelich, Germany 2Institut of Bio- und Geosciences IBG-1: Biotechnology, Research Centre Juelich, D-52426 Juelich, Germany 3Institute of Pharmaceutical Biotechnology, Ulm-University, Albert-Einstein-Allee 11, D-89069 Ulm, Germany Keywords Abstract Biofilm, microarray, motility, orf PA1242, protease, Pseudomonas aeruginosa, The open reading frame PA1242 in the genome of Pseudomonas aeruginosa Pyoverdine. PAO1 encodes a putative protease belonging to the peptidase S8 family of sub- tilases. The respective enzyme termed SprP consists of an N-terminal signal Correspondence peptide and a so-called S8 domain linked by a domain of unknown function Karl-Erich Jaeger, Institute of Molecular (DUF). Presumably, this DUF domain defines a discrete class of Pseudomonas Enzyme Technology, Heinrich-Heine- proteins as homologous domains can be identified almost exclusively in pro- University Duesseldorf, Research Centre Juelich, D-52426 Juelich, Germany. teins of the genus Pseudomonas. The sprP gene was expressed in Escherichia coli Δ Tel: (+49)-2461-61-3716; Fax: (+49)-2461-61- and proteolytic activity was demonstrated. A P. aeruginosa sprP mutant was 2490; E-mail: [email protected] constructed and its gene expression pattern compared to the wild-type strain by genome microarray analysis revealing altered expression levels of 218 genes. Funding Information Apparently, SprP is involved in regulation of a variety of different cellular pro- 2021 As a member of the CLIB -Graduate cesses in P. aeruginosa including pyoverdine synthesis, denitrification, the Cluster for Industrial Biotechnology Alexander formation of cell aggregates, and of biofilms. Pelzer received a scholarship financed by the Ministry of Innovation, Science and Research (MIWF) of North Rhine-Westphalia and the Heinrich-Heine-University of Duesseldorf. Received: 12 July 2013; Revised: 7 November 2013; Accepted: 20 November 2013 MicrobiologyOpen 2014; 3(1): 89–103 doi: 10.1002/mbo3.150 Introduction rate (Chastre and Fagon 2002). Epidemic increases in bacterial multidrug resistance and the occurrence of truly Pseudomonas aeruginosa is an opportunistic aerobic Gram- pan-resistant Gram-negative pathogens (e.g., P. aeruginosa, negative bacterium regarded as the major cause of death in Acinetobacter baumannii, Klebsiella pneumonia) are major cystic fibrosis patients (Murray et al. 2007). It causes both concerns in clinical microbiology, and thus, novel antibiot- community- and hospital-acquired infections including ics are urgently needed (Payne 2008; Rasko and Sperandio ulcerative keratitis, skin and soft tissue infections, pneumo- 2010). However, the identification of potential drug targets nia, and infection after burn injuries (Zegans et al. 2002; and the success of novel antimicrobial agents proves to be Fujitani et al. 2011; Rezaei et al. 2011; Wu et al. 2011) and difficult (Maeda et al. 2012). Part of the P. aeruginosa path- is the leading cause of respiratory tract infections in ogenic potential is an impressive arsenal of virulence fac- patients intubated during surgery, with a high mortality tors, like flagella and type IV pili, exopolysaccharides, ª 2013 The Authors. MicrobiologyOpen published by John Wiley & Sons Ltd. This is an open access article under the terms of 89 the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited. P. aeruginosa Protease SprP A. Pelzer et al. lipopolysaccharides, and several secreted factors (Ramphal 1997; Bergeron et al. 2000; Antao and Malcata 2005; and Pier 1985; Nicas and Iglewski 1986; Drake and Montie Poole et al. 2007). The majority of subtilases is secreted 1988; Sato et al. 1988; Gupta et al. 1994). All these viru- but several members are localized intracellularly (Siezen lence factors are regulated by several complex regulatory and Leunissen 1997). In general, subtilases play a key role systems including the quorum sensing (QS) system (Pesci in protein maturation processes and precursor processing et al. 1999; Venturi 2006). The yellow–green siderophore (Siezen et al. 2007). Subtilases typically show a multi- pyoverdine is also required for pathogenicity of P. aerugin- domain structure containing a signal sequence for translo- osa as it is part of the major iron uptake system which is cation, a pro-domain for maturation, and a protease controlled by the iron starvation (IS) sigma factor PvdS domain (Siezen and Leunissen 1997). The N-terminal (Ochsner et al. 2002; Tiburzi et al. 2008). Several other propeptide of subtilases usually acts as an intramolecular virulence factors including the proteases PrpL and AprA, chaperone (Shinde and Inouye 1993) that ensures correct are also regulated by PvdS (Shigematsu et al. 2001; Wilder- folding of the enzyme, inhibits premature proteolytic man et al. 2001; Lamont et al. 2002). Two different surface activity (Kojima et al. 1997), and is autocatalytically organelles, namely a single polar flagellum and polar type cleaved off during enzyme maturation (Gallagher et al. IV pili, are responsible for P. aeruginosa motility. In liquid 1995; Yabuta et al. 2001). environments, P. aeruginosa can swim using flagella, We have identified in the genome sequence of P. aeru- whereas the type IV pili enable twitching motility on solid ginosa PAO1 (Stover et al. 2000), the open reading frame surfaces (Henrichsen 1972; Mattick 2002). On semisolid sprP (PA1242) encoding a so far hypothetical protein with surfaces, P. aeruginosa moves by swarming via flagella and homology to enzymes of the subtilisin-like peptidase fam- type IV pili (Kohler€ et al. 2000). These cell surface struc- ily S8. The predicted protein SprP contains a signal tures are also involved in biofilm formation (O’Toole and sequence and a peptidase S8 domain. We have demon- Kolter 1998; Klausen et al. 2003). P. aeruginosa biofilms strated that SprP exhibits protease activity and further pose a significant problem in both industrial and medical report on the role of SprP for various important cellular settings. Biofilms can form on medical devices like intrave- functions in P. aeruginosa including growth, cellular motil- nous catheters and contact lenses and they are causative for ity, biofilm formation, and pyoverdine production. the high resistance of P. aeruginosa against many antibiotics as well as the host immune system (Zegans et al. 2002). Experimental Procedures Biofilms exist in a complex extracellular matrix consisting of DNA, polysaccharides, and proteins. Their formation is Bacterial strains, plasmids, media, and a highly regulated process depending, among other factors, culture conditions on cell motility and complex QS systems stabilizing such biofilms (Harmsen et al. 2010; Ghafoor et al. 2011; Mikkel- The strains and plasmids used in this study are listed in sen et al. 2011). Table 1. Escherichia coli DH5a was used as host for cloning Proteases represent a very diverse group of hydrolases and expression; E. coli S17-1 was used for conjugal transfer. which are found in all kingdoms of life (Rawlings and All strains were grown in lysogeny broth (LB) medium Barrett 1994). In bacteria, they are often involved in (10 g/L tryptone, 5 g/L yeast extract, 10 g/L NaCl). For essential regulatory processes, for example, via degrada- anaerobic growth conditions, 50 mmol/L KNO3 was added tion of abnormally folded proteins or by controlling the to the medium. Cultures grown for 16 h at 37°CinLB intracellular amounts of sigma factors and chaperones medium (volume: 10 mL) in Erlenmeyer flasks were used (Gottesman 1996). They catalyze the cleavage of peptide to inoculate main cultures (volume: 25 mL) to an initial bonds in proteins and either show high specificity for optical density of OD580nm = 0.1. Cultures were grown at defined amino acid (aa) sequences, or unspecifically 37°C in a rotating shaker at 150 rpm until they reached an hydrolyze proteins to yield oligopeptides or aa. Serine optical density of OD580nm = 2.5. Sodium nitroprusside proteases contain serine as the active site residue and are (SNP) was added to LB-medium at a concentration of grouped into 13 clans in the MEROPS database (Rawlings 2 mmol/L. For E. coli, chloramphenicol (50 lg/mL) was et al. 2012). Among them, family S8 of peptidases, also used and for P. aeruginosa, chloramphenicol (300 lg/mL), known as “subtilisin-like” or “subtilase” family, harbors and gentamycin (30 lg/mL) was added. the serine endopeptidase subtilisin and related enzymes with a characteristic Asp/His/Ser catalytic triad and repre- Recombinant DNA techniques, gene cloning, sents the second largest family of serine proteases (Siezen and mutant construction and Leunissen 1997; Siezen et al. 2007; Rawlings et al. 2012). Subtilases are found in archaea, bacteria, viruses, Recombinant DNA techniques were performed fungi, yeast, and higher eukaryotes (Siezen and Leunissen essentially as described by Sambrook et al. (1989). DNA 90 ª 2013 The Authors. MicrobiologyOpen published by John Wiley & Sons Ltd. A. Pelzer et al. P. aeruginosa Protease SprP Table 1. Strains, plasmids, and primers used in this study. Strain or plasmid Genotype/Phenotype Reference or source Strains Pseudomonas aeruginosa PAO1 Wild type Holloway et
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