Detection and expression of SapS, a class C nonspecific acid phosphatase with O-phospho-Ltyrosine- phosphatase activity, in Staphylococcus aureus isolates from patients with chronic osteomyelitis

Carlos Martínez-Canseco, Rebecca E. Franco-Bourland, Norma González-Huerta, Marco Antonio Paredes-Espinosa, Silvia Giono-Cerezo, Laura Sánchez-Chapul, Rogelio Paniagua-Pérez, René Valdez-Mijares, C Hernández-Flores, .

Keywords: Staphylococcus aureus, virulence factors, osteomyelitis

Abstract

Introduction. The identity of Staphylococcus aureus virulence factors involved in chronic osteomyelitis remains unresolved. SapS is a class C non-specific acid phosphatase and a well-known virulence factor that has been identified in S. aureus strain 154 but in protein extracts from rotting vegetables.
Objective. To identify the SapS gene and characterize the activity of SapS from S. aureus strains: 12 isolates from bone infected samples of patients treated for chronic osteomyelitis and 49 from a database with in silico analysis of complete bacterial genomes.
Materials and methods. The SapS gene was isolated and sequenced from 12 S. aureus clinical isolates and two reference strains; 49 S. aureus strains and 11 coagulase-negative staphylococci were tested using in silico PCR. Culture media semi-purified protein extracts from the clinical strains were assayed for phosphatase activity with p-nitro-phenylphosphate, O-phospho-L-tyrosine, O-phospho-L-serine, and OphosphoL-threonine in conjunction with various phosphatase inhibitors.
Results. SapS was detected in the clinical and in-silico S. aureus strains, but not in the in silico coagulase-negative staphylococci strains. Sec-type I lipoprotein-type N-terminal signal peptide sequences; secreted proteins, and aspartate bipartite catalytic domains coding sequences were found in the SapS nucleotide and amino acid sequence analysis. SapS dephosphorylated with p-nitro-phenyl-phosphate and ophosphoLtyrosine were selectively resistant to tartrate and fluoride, but sensitive to vanadate and molybdate.
Conclusion. SapS gene was found in the genome of the clinical isolates and the in silico Staphylococcus aureus strains. SapS shares biochemical similarities with known virulent bacterial, such as protein tyrosine phosphatases, suggesting it may be a virulence factor in chronic osteomyelitis.

Downloads

Download data is not yet available.
  • Carlos Martínez-Canseco Servicio de Bioquímica, Instituto Nacional de Rehabilitación “Luis Guillermo Ibarra Ibarra”, Ciudad de México, México https://orcid.org/0000-0002-3889-608X
  • Rebecca E. Franco-Bourland Servicio de Bioquímica, Instituto Nacional de Rehabilitación “Luis Guillermo Ibarra Ibarra”, Ciudad de México, México https://orcid.org/0000-0001-6385-7106
  • Norma González-Huerta Servicio de Medicina Genómica, Instituto Nacional de Rehabilitación “Luis Guillermo Ibarra Ibarra”, Ciudad de México, México
  • Marco Antonio Paredes-Espinosa Servicio de Bioterio y Cirugía Experimental, Instituto Nacional de Rehabilitación “Luis Guillermo Ibarra Ibarra”, Ciudad de México, México https://orcid.org/0000-0002-5915-9716
  • Silvia Giono-Cerezo Laboratorio de Bacteriología Médica, Escuela Nacional de Ciencias Biológicas, Instituto Politécnico Nacional, Ciudad de México, México https://orcid.org/0000-0003-1835-6788
  • Laura Sánchez-Chapul Laboratorio de Enfermedades Neuromusculares, Instituto Nacional de Rehabilitación “Luis Guillermo Ibarra Ibarra”, Ciudad de México, México https://orcid.org/0000-0002-4268-2279
  • Rogelio Paniagua-Pérez Servicio de Bioquímica, Instituto Nacional de Rehabilitación “Luis Guillermo Ibarra Ibarra”, Ciudad de México, México https://orcid.org/0000-0003-3274-2941
  • René Valdez-Mijares Servicio de Bioquímica, Instituto Nacional de Rehabilitación “Luis Guillermo Ibarra Ibarra”, Ciudad de México, México https://orcid.org/0000-0001-7920-9015
  • C Hernández-Flores Servicio de Bioquímica, Instituto Nacional de Rehabilitación “Luis Guillermo Ibarra Ibarra”, Ciudad de México, México https://orcid.org/0000-0001-6115-3287

References

Barakat A, Schilling WHK, Sharma S, Guryel E, Freeman R. Chronic osteomyelitis: a review on current concepts and trends in treatment. Orthop Trauma. 2019;33:181-7. https://doi.org/10.1016/j.mporth.2019.03.005

Lew DP, Waldvogel FA. Osteomyelitis. Lancet. 2004;364:369-79. https://doi.org/10.1016/s0140-6736(04)16727-5

Tong SYC, Davis JS, Eichenberger E, Holland TL, Fowler VG Jr. Staphylococcus aureus infections: epidemiology, pathophysiology, clinical manifestations, and management. Clin Microbiol Rev. 2015;28:603-61. https://doi.org/10.1128/CMR.00134-14

Ziebandt AK, Kusch H, Degner M, Jaglitz S, Sibbald MJJB, Arends JP, et al. Proteomics uncovers extreme heterogeneity in the Staphylococcus aureus exoproteome due to genomic plasticity and variant gene regulation. Proteomics. 2010;10:1634-44. https://doi.org/10.1002/pmic.200900313

Jin T, Zhu YL, Li J, Shi J, He XQ, Ding J, et al. Staphylococcal protein A, panton-valentin leukocidin and coagulase aggravate the bone loss and bone destruction in osteomyelitis. Cell Physiol Biochem. 2013;32:322-33. https://doi.org/10.1159/000354440

Rossolini GM, Schippa S, Riccio ML, Berlutti F, Macaskie LE, Thaller MC. Bacterial non-specific acid phosphohydrolases: physiology, evolution and use as tools in microbial biotechnology. Cell Mol Life Sci. 1998;54:833-50. https://doi.org/10.1007/s000180050212

Gandhi NU, Chandra SB. A comparative analysis of three classes of bacterial non-specific acid phosphatases and archaeal phosphoesterases: evolutionary perspective. Acta Inform Med. 2012;20:167-73. https://doi.org/10.5455/aim.2012.20.167-73

Du Plessis EM, Theron J, Joubert L, Lotter T, Watson TG. Characterization of a phosphatase secreted by Staphylococcus aureus strain 154, a new member of the bacterial class C family of non-specific acid phosphatases. Syst Appl Microbiol. 2002;25:21-30. https://doi.org/10.1078/0723-2020-00098

Novick RP. Genetic systems in Staphylococci. Meth Enzymol. 1991;204:587636. https://doi.org/10.1016/0076-6879(91)04029-N

Bikandi J, San Millán R, Rementeria A, Garaizar J. In silico analysis of complete bacterial genomes: PCR, AFLP-PCR and endonuclease restriction. Bioinformatics. 2004;20:798-9. https://doi.org/10.1093/bioinformatics/btg491

Madeira F, Park YM, Lee J, Buso N, Gur T, Madhusoodanan N, et al. The EMBL EBI search and sequence analysis tools. APIs in 2019. Nucleic Acids Res. 2019;47: W636-41. https://doi.org/10.1093/nar/gkz268

Almagro-Armenteros JJ, Tsirigos KD, Sønderby CK, Petersen TN, Winther O, Brunak B, et al. SignalP 5.0 improves signal peptide predictions using deep neural networks. Nat Biotechnol. 2019;37:420-3. https://doi.org/10.1038/s41587-019-0036-z

Shen HB, Chou KC. Gpos-mPLoc: A top-down approach to improve the quality of predicting subcellular localization of gram-positive bacterial proteins. Protein Pept Lett. 2009;16:1478-84. https://doi.org/10.2174/092986609789839322

NCBI Resource Coordinators. Database resources of the National Center for Biotechnology Information. Nucleic Acids Res. 2018;46:D8-13. https://doi.org/10.1093/nar/gkx1095

Golovan S, Wang G, Zhang J, Forsberg CW. Characterization and overproduction of the Escherichia coli appA encoded bifunctional enzyme that exhibits both phytase and acid phosphatase activities. Can J Microbiol. 2000;46:59-71. https://doi.org/10.1139/cjm-46-1-59

Hamilton A, Harrington D, Sutcliffe IC. Characterization of acid phosphatase activities in the equine pathogen Streptococcus equi. Syst Appl Microbiol. 2000;23:325-9. https://doi.org/10.1016/S0723-2020(00)80060-0

Zlotnick GW, Gottlieb M. A sensitive staining technique for the detection of phosphohydrolase activities after polyacrylamide gel electrophoresis. Anal Biochem. 1986;153:121-5. https://doi.org/10.1016/0003-2697(86)90069-2

Thaller MC, Schippa S, Rossolini GM. Conserved sequence motifs among bacterial, eukaryotic, and archaeal phosphatases that define a new phosphohydrolase superfamily. Protein Sci. 1998;7:1647-52. https://doi.org/10.1002/pro.5560070722

Kusch H, Engelmann S. Secrets of the secretome in Staphylococcus aureus. Int J Med Microbiol. 2014;304:133–41. https://doi.org/10.1016/j.ijmm.2013.11.005

Bosi E, Monk JM, Aziz RK, Fondi M, Nizet V, Palsson BØ. Comparative genome-scale modelling of Staphylococcus aureus strains identifies strain-specific metabolic capabilities linked to pathogenicity. Proc Natl Acad Sci USA. 2016;113:E38019. https://doi.org/10.1073/pnas.1523199113

Feil EJ, Cooper JE, Grundmann H, Robinson DA, Enright MC, Berendt T, et al. How clonal is Staphylococcus aureus? J Bacteriol. 2003;185:3307-16. https://doi.org/10.1128/jb.185.11.3307-3316.2003

Sibbald MJ, Ziebandt AK, Engelmann S, Hecker M, de Jong A, Harmsen HJ, et al. Mapping the pathways to staphylococcal pathogenesis by comparative secretomics. Microbiol Mol Biol Rev. 2006;70:755-88. https://doi.org/10.1128/MMBR.00008-06

Caselli A, Paoli P, Santi A, Mugnaioni C, Toti A, Camici G, et al. Low molecular weight protein tyrosine phosphatase: Multifaceted functions of an evolutionarily conserved enzyme. Biochim Biophys Acta. 2016;1864:1339-55. https://doi.org/10.1016/j.bbapap.2016.07.001

Reilly TJ, Chance DL, Calcutt MJ, Tanner JJ, Felts RL, Waller SC, et al. Characterization of a unique class C acid phosphatase from Clostridium perfringens. Appl Environ Microbiol. 2009;75:3745-54. https://doi.org/10.1128/AEM.01599-08

Saleh MT, Belisle JT. Secretion of an acid phosphatase (SapM) by Mycobacterium tuberculosis that is similar to eukaryotic acid phosphatases. J Bacteriol. 2000;182:6850-3. https://doi.org/10.1128/JB.182.23.6850-6853.2000

Muthukrishnan G, Masters EA, Daiss JL, Schwarz EM. Mechanisms of immune evasion and bone tissue colonization that make Staphylococcus aureus the primary pathogen in osteomyelitis. Curr Osteoporos Rep. 2019;17:395-404. https://doi.org/10.1007/s11914-019-00548-4

Neal AL, Blackwell M, Akkari E, Guyomar C, Clark I, Hirsch PR. Phylogenetic distribution, biogeography and the effects of land management upon bacterial non-specific Acid phosphatase Gene diversity and abundance. Plant Soil. 2018;427:175-89. https://doi.org/10.1007/s11104-017-3301-2

Kelliher JL, Radin JN, Grim KP, Párraga-Solórzano PK, Degnan PH, Kehl-Fie TE. Acquisition of the phosphate transporter NptA enhances Staphylococcus aureus pathogenesis by improving phosphate uptake in divergent environments. Infect Immun. 2018;86. https://doi.org/10.1128/iai.00631-17

Kelliher JL, Leder-Macek AJ, Grudzinski KM, Radin JN, Kehl-Fie TE. Staphylococcus aureus preferentially liberates inorganic phosphate from organophosphates in environments where this nutrient is limiting. J Bacteriol. 2020;202. https://doi.org/10.1128/JB.00264-20

How to Cite
1.
Martínez-Canseco C, Franco-Bourland RE, González-Huerta N, Paredes-Espinosa MA, Giono-Cerezo S, Sánchez-Chapul L, et al. Detection and expression of SapS, a class C nonspecific acid phosphatase with O-phospho-Ltyrosine- phosphatase activity, in Staphylococcus aureus isolates from patients with chronic osteomyelitis. biomedica [Internet]. 2023 Jun. 30 [cited 2024 May 19];43(2):200-12. Available from: https://revistabiomedica.org/index.php/biomedica/article/view/6604

Some similar items:

Published
2023-06-30
Section
Original articles

Altmetric

Article metrics
Abstract views
Galley vies
PDF Views
HTML views
Other views
Crossref Cited-by logo
QR Code