A highly active S1-P1 nuclease from the opportunistic pathogen Stenotrophomonas maltophilia cleaves c-di-GMP
Language English Country Great Britain, England Media print-electronic
Document type Journal Article, Research Support, Non-U.S. Gov't
- Keywords
- S1-P1 nuclease, Stenotrophomonas maltophilia, c-di-GMP, cyclic diguanylate, nosocomial infection,
- MeSH
- Endonucleases metabolism MeSH
- Cyclic GMP metabolism MeSH
- RNA metabolism MeSH
- Stenotrophomonas maltophilia * genetics metabolism MeSH
- Publication type
- Journal Article MeSH
- Research Support, Non-U.S. Gov't MeSH
- Names of Substances
- bis(3',5')-cyclic diguanylic acid MeSH Browser
- Endonucleases MeSH
- Cyclic GMP MeSH
- RNA MeSH
A number of multidrug-resistant bacterial pathogens code for S1-P1 nucleases with a poorly understood role. We have characterized a recombinant form of S1-P1 nuclease from Stenotrophomonas maltophilia, an opportunistic pathogen. S. maltophilia nuclease 1 (SmNuc1) acts predominantly as an RNase and is active in a wide range of temperatures and pH. It retains a notable level of activity towards RNA and ssDNA at pH 5 and 9 and about 10% of activity towards RNA at 10 °C. SmNuc1 with very high catalytic rates outperforms S1 nuclease from Aspergillus oryzae and other similar nucleases on all types of substrates. SmNuc1 degrades second messenger c-di-GMP, which has potential implications for its role in the pathogenicity of S. maltophilia.
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Brooke JS (2012) Stenotrophomonas maltophilia: an emerging global opportunistic pathogen. Clin Microbiol Rev 25, 2-41.
Adegoke AA, Stenström TA and Okoh AI (2017) Stenotrophomonas maltophilia as an emerging ubiquitous pathogen: looking beyond contemporary antibiotic therapy. Front Microbiol 8, 2276.
McCutcheon JG and Dennis JJ (2021) The potential of phage therapy against the emerging opportunistic pathogen Stenotrophomonas maltophilia. Viruses 13, 1057.
Sánchez MB (2015) Antibiotic resistance in the opportunistic pathogen Stenotrophomonas maltophilia. Front Microbiol 6, 658.
Gröschel MI, Meehan CJ, Barilar I, Diricks M, Gonzaga A, Steglich M, Conchillo-Solé O, Scherer IC, Mamat U, Luz CF et al. (2020) The phylogenetic landscape and nosocomial spread of the multidrug-resistant opportunist Stenotrophomonas maltophilia. Nat Commun 11, 2044.
Silbaq FS (2009) Viable ultramicrocells in drinking water. J Appl Microbiol 106, 106-117.
Trifonova A and Strateva T (2019) Stenotrophomonas maltophilia - a low-grade pathogen with numerous virulence factors. Infect Dis 51, 168-178.
Sharma P, Garg N, Sharma A, Capalash N and Singh R (2019) Nucleases of bacterial pathogens as virulence factors, therapeutic targets and diagnostic markers. Int J Med Microbiol 309, 151354.
Trundová M, Kovaľ T, Owens RJ, Fejfarová K, Dušková J, Kolenko P and Dohnálek J (2018) Highly stable single-strand-specific 3′-nuclease/nucleotidase from Legionella pneumophila. Int J Biol Macromol 114, 776-787.
Kovaľ T and Dohnálek J (2018) Characteristics and application of S1-P1 nucleases in biotechnology and medicine. Biotechnol Adv 36, 603-612.
Pimkin M, Miller CG, Blakesley L, Oleykowski CA, Kodali NS and Yeung AT (2006) Characterization of a periplasmic S1-like nuclease coded by the Mesorhizobium loti symbiosis Island. Biochem Biophys Res Commun 343, 77-84.
Jenal U, Reinders A and Lori C (2017) Cyclic di-GMP: second messenger extraordinaire. Nat Rev Microbiol 15, 271-284.
Hengge R (2009) Principles of c-di-GMP signalling in bacteria. Nat Rev Microbiol 7, 263-273.
Esposito A, Pompilio A, Bettua C, Crocetta V, Giacobazzi E, Fiscarelli E, Jousson O and Di Bonaventura G (2017) Evolution of Stenotrophomonas maltophilia in cystic fibrosis lung over chronic infection: a genomic and phenotypic population study. Front Microbiol 8, 1590-1515.
Clark K, Karsch-Mizrachi I, Lipman DJ, Ostell J and Sayers EW (2016) GenBank. Nucleic Acids Res 44, 67-72.
UniProt Consortium (2020) UniProt: the universal protein knowledgebase in 2021. Nucleic Acids Res 49, 480-489.
Fuhrmann M, Hausherr A, Ferbitz L, Schodl T, Heitzer M and Hegemann P (2004) Monitoring dynamic expression of nuclear genes in Chlamydomonas reinhardtii by using a synthetic luciferase reporter gene. Plant Mol Biol 55, 869-881.
Raab D, Graf M, Notka F, Schödl T and Wagner R (2010) The GeneOptimizer algorithm: using a sliding window approach to cope with the vast sequence space in multiparameter DNA sequence optimization. Syst Synth Biotechnol 4, 215-225.
Strohalm M, Kavan D, Novak P, Volny M and Havlicek V (2010) mMass 3: a cross-platform software environment for precise analysis of mass spectrometric data. Anal Chem 82, 4648-4651.
Stelitano V, Brandt A, Fernicola S, Franceschini S, Giardina G, Pica A, Rinaldo S, Sica F and Cutruzzolà F (2013) Probing the activity of diguanylate cyclases and c-di-GMP phosphodiesterases in real-time by CD spectroscopy. Nucleic Acids Res 41, e79.
Gasteiger E, Hoogland C, Gattiker A, Duvaud S, Wilkins MR, Appel RD and Bairoch A (2005) Protein Identification and Analysis Tools on the ExPASy Server. Humana, Totowa, NJ.
Kovaľ T, Lipovová P, Podzimek T, Matoušek J, Dušková J, Skálová T, Stěpánková A, Hašek J and Dohnálek J (2013) Plant multifunctional nuclease TBN1 with unexpected phospholipase activity: structural study and reaction-mechanism analysis. Acta Crystallogr D 69, 213-226.
Podzimek T, Přerovská T, Šantrůček J, Kovaľ T, Dohnálek J, Matoušek J and Lipovová P (2018) N-glycosylation of tomato nuclease TBN1 produced in N. benthamiana and its effect on the enzyme activity. Plant Sci 276, 152-161.
Kovaľ T, Østergaard LH, Lehmbeck J, Nørgaard A, Lipovová P, Dušková J, Skálová T, Trundová M, Kolenko P, Fejfarová K et al. (2016) Structural and catalytic properties of S1 nuclease from Aspergillus oryzae responsible for substrate recognition, cleavage, non-specificity, and inhibition. PLoS One 11, e0168832.
Adámková K, Koval' T, Østergaard LH, Dušková J, Malý M, Švecová L, Skálová T, Kolenko P and Dohnálek J (2022) Atomic resolution studies of S1 nuclease complexes reveal details of RNA interaction with the enzyme despite multiple lattice-translocation defects. Acta Crystallogr D 78, 1194-1209.
Podzimek T, Matoušek J, Lipovová P, Poučková P, Spiwok V and Šantrůček J (2011) Biochemical properties of three plant nucleases with anticancer potential. Plant Sci 180, 343-351.
Desai NA and Shankar V (2003) Single-strand-specific nucleases. FEMS Microbiol Rev 26, 457-491.
Paletta-Silva R, Vieira DP, Vieira-Bernardo R, Majerowicz D, Gondim KC, Vannier-Santos MA, Lopes AH and Meyer-Fernandes JR (2011) Leishmania amazonensis: characterization of an ecto-3′-nucleotidase activity and its possible role in virulence. Exp Parasitol 129, 277-283.
Freitas-Mesquita AL, Dick CF, Dos-Santos ALA, Nascimento MTC, Rochael NC, Saraiva EM and Meyer-Fernandes JR (2019) Cloning, expression and purification of 3′-nucleotidase/nuclease, an enzyme responsible for the Leishmania escape from neutrophil extracellular traps. Mol Biochem Parasitol 229, 6-14.
Shishido K and Noriyuki H (1986) Purification of S1 nuclease to homogeneity and its chemical, physical and catalytic properties. Biochim Biophys Acta Gen Subj 884, 215-218.
Ko C-Y, Lai Y-L, Liu W-Y, Lin C-H, Chen Y-T, Chen L-FO, Lin T-Y and Shaw J-F (2012) Arabidopsis ENDO2: its catalytic role and requirement of N-glycosylation for function. J Agric Food Chem 60, 5169-5179.
Touw DS, Patel DR and van den Berg B (2010) The crystal structure of OprG from Pseudomonas aeruginosa, a potential channel for transport of hydrophobic molecules across the outer membrane. PLoS One 5, e15016.
Sattler SA, Wang X, Lewis KM, DeHan PJ, Park CM, Xin Y, Liu H, Xian M, Xun L and Kang CH (2015) Characterizations of two bacterial persulfide dioxygenases of the metallo-β-lactamase superfamily. J Biol Chem 290, 18914-18923.
Teufel F, Almagro Armenteros JJ, Johansen AR, Gíslason MH, Pihl SI, Tsirigos KD, Winther O, Brunak S, von Heijne G and Nielsen H (2022) SignalP 6.0 predicts all five types of signal peptides using protein language models. Nat Biotechnol 40, 1023-1025.
Tsirigotaki A, De Geyter J, Šoštaric´ N, Economou A and Karamanou S (2017) Protein export through the bacterial Sec pathway. Nat Rev Microbiol 15, 21-36.
Menetrey Q, Sorlin P, Jumas-Bilak E, Chiron R, Dupont C and Marchandin H (2021) Achromobacter xylosoxidans and Stenotrophomonas maltophilia: emerging pathogens well-armed for life in the cystic fibrosis patients' lung. Genes 12, 610.
Christen M, Christen B, Folcher M, Schauerte A and Jenal U (2005) Identification and characterization of a cyclic di-GMP-specific phosphodiesterase and its allosteric control by GTP. J Biol Chem 280, 30829-30837.
Andrade WA, Firon A, Schmidt T, Hornung V, Fitzgerald KA, Kurt-Jones EA, Trieu-Cuot P, Golenbock DT and Kaminski PA (2016) Group B Streptococcus degrades cyclic-di-AMP to modulate STING-dependent type I interferon production. Cell Host Microbe 20, 49-59.
Rao F, Yang Y, Qi Y and Liang ZX (2008) Catalytic mechanism of cyclic di-GMP-specific phosphodiesterase: a study of the EAL domain-containing RocR from Pseudomonas aeruginosa. J Bacteriol 190, 3622-3631.
McWhirter SM, Barbalat R, Monroe KM, Fontana MF, Hyodo M, Joncker NT, Ishii KJ, Akira S, Colonna M, Chen ZJ et al. (2009) A host type I interferon response is induced by cytosolic sensing of the bacterial second messenger cyclic-di-GMP. J Exp Med 206, 1899-1911.
Yin Q, Tian Y, Kabaleeswaran V, Jiang X, Tu D, Eck MJ, Chen ZJ and Wu H (2012) Cyclic di-GMP sensing via the innate immune signaling protein STING. Mol Cell 46, 735-745.
