Changes in the Protein Profile in Staphylococcal Strains from Patients Infected with the SARS-CoV-2 Virus

JARZEMBOWSKI, TOMASZ; PIECHOWICZ, LIDIA; BRONK, MAREK; PAŁUBICKA, ANNA; NAUMIUK, ŁUKASZ

doi:10.33073/pjm-2023-001

Abstract

Staphylococcus aureus strains are particularly often isolated from patients with SARS-CoV-2 infection. The aim of the current research was to determine whether the SARS-CoV-2 virus infection affects the protein profile of S. aureus. Bacteria were isolated from the forty swabs collected from the patients in the hospitals of the Pomeranian region. MALDI-TOF MS spectra were obtained using a Microflex LT instrument. Twenty-nine peaks were identified. The peak (2,430) is described here for the first time and was unique for the isolates from patients infected with the SARS-CoV-2 virus. These results support the hypothesis of bacterial adaptation to the conditions caused by viral infection.

References

Bernardo K, Pakulat N, Macht M, Krut O, Seifert H, Fleer S, Hünger F, Krönke M. Identification and discrimination of Staphylococcus aureus strains using matrix-assisted laser desorption/ ionization-time of flight mass spectrometry. Proteomics. 2002 Jun; 2(6):747–753. https://doi.org/10.1002/1615-9861(200206)2:6<747::AID-PROT747>3.0.CO;2-V
Search in Google Scholar Back to article
Böhme K, Morandi S, Cremonesi P, Fernández No IC, Barros-Velázquez J, Castiglioni B, Brasca M, Cañas B, Calo-Mata P. Characterization of Staphylococcus aureus strains isolated from Italian dairy products by MALDI-TOF mass fingerprinting. Electrophoresis. 2012 Aug;33(15):2355–2364. https://doi.org/10.1002/elps.201100480
Search in Google Scholar Back to article
Bonnet I, Millon B, Meugnier H, Vandenesch F, Maurin M, Pavese P, Boisset S. High prevalence of spa type t571 among methicillin-susceptible Staphylococcus aureus from bacteremic patients in a French University Hospital. PLoS One. 2018 Oct;13(10):e0204977. https://doi.org/10.1371/journal.pone.0204977
Search in Google Scholar Back to article
Clancy CJ, Nguyen MH. Coronavirus disease 2019, superinfections, and antimicrobial development: What can we expect? Clin Infect Dis. 2020 Dec;71(10):2736–2743. https://doi.org/10.1093/cid/ciaa524
Search in Google Scholar Back to article
Clark AE, Kaleta EJ, Arora A, Wolk DM. Matrix-assisted laser desorption ionization-time of flight mass spectrometry: a fundamental shift in the routine practice of clinical microbiology. Clin Microbiol Rev. 2013 Jul;26(3):547–603. https://doi.org/10.1128/CMR.00072-12
Search in Google Scholar Back to article
Deasy EC, Brennan GI, Tecklenborg SC, Umeh C, Coleman DC, Shore AC. A molecular epidemiological investigation of methicillin-susceptible Staphylococcus aureus causing bloodstream infections in Ireland, 2006–2017. Eur J Clin Microbiol Infect Dis. 2019 May; 38(5):927–936. https://doi.org/10.1007/s10096-019-03523-0
Search in Google Scholar Back to article
Fetsch A, Contzen M, Hartelt K, Kleiser A, Maassen S, Rau J, Kraushaar B, Layer F, Strommenger B. Staphylococcus aureus food-poisoning outbreak associated with the consumption of ice-cream. Int J Food Microbiol. 2014 Sep;187:1–6. https://doi.org/10.1016/j.ijfoodmicro.2014.06.017
Search in Google Scholar Back to article
Franco A, Hasman H, Iurescia M, Lorenzetti R, Stegger M, Pantosti A, Feltrin F, Ianzano A, Porrero MC, Liapi M, et al. Molecular characterization of spa type t127, sequence type 1 methicillin-resistant Staphylococcus aureus from pigs. J Antimicrob Chemother. 2011 Jun;66(6):1231–1235. https://doi.org/10.1093/jac/dkr115
Search in Google Scholar Back to article
Frénay HM, Bunschoten AE, Schouls LM, van Leeuwen WJ, Vandenbroucke-Grauls CM, Verhoef J, Mooi FR. Molecular typing of methicillin-resistant Staphylococcus aureus on the basis of protein A gene polymorphism. Eur J Clin Microbiol Infect Dis. 1996 Jan;15(1):60–64. https://doi.org/10.1007/BF01586186
Search in Google Scholar Back to article
Ghasemzadeh-Moghaddam H, Ghaznavi-Rad E, Sekawi Z, Yun-Khoon L, Aziz MN, Hamat RA, Melles DC, van Belkum A, Shamsudin MN, Neela V. Methicillin-susceptible Staphylococcus aureus from clinical and community sources are genetically diverse. Int J Med Microbiol. 2011 Apr;301(4):347–353. https://doi.org/10.1016/j.ijmm.2010.10.004
Search in Google Scholar Back to article
Grundmann H, Aanensen DM, van den Wijngaard CC, Spratt BG, Harmsen D, Friedrich AW; European Staphylococcal Reference Laboratory Working Group. Geographic distribution of Staphylococcus aureus causing invasive infections in Europe: a molecular-epidemiological analysis. PLoS Med. 2010 Jan;7(1):e1000215. https://doi.org/10.1371/journal.pmed.1000215
Search in Google Scholar Back to article
Hallin M, Friedrich AW, Struelens MJ. spa typing for epidemiological surveillance of Staphylococcus aureus. Methods Mol Biol. 2009; 551:189–202. https://doi.org/10.1007/978-1-60327-999-4_15
Search in Google Scholar Back to article
Harmsen D, Claus H, Witte W, Rothgänger J, Claus H, Turnwald D, Vogel U. Typing of methicillin-resistant Staphylococcus aureus in a university hospital setting by using novel software for spa repeat determination and database management. J Clin Microbiol. 2003 Dec;41(12):5442–5448. https://doi.org/10.1128/JCM.41.12.5442-5448.2003
Search in Google Scholar Back to article
Hasman H, Moodley A, Guardabassi L, Stegger M, Skov RL, Aarestrup FM. spa type distribution in Staphylococcus aureus originating from pigs, cattle and poultry. Vet Microbiol. 2010 Mar;141 (3–4):326–331. https://doi.org/10.1016/j.vetmic.2009.09.025
Search in Google Scholar Back to article
Hoque MN, Akter S, Mishu ID, Islam MR, Rahman MS, Akhter M, Islam I, Hasan MM, Rahaman MM, Sultana M, et al. Microbial co-infections in COVID-19: associated microbiota and underlying mechanisms of pathogenesis. Microb Pathog. 2021 Jul;156:104941. https://doi.org/10.1016/j.micpath.2021.104941
Search in Google Scholar Back to article
Jackson KA, Edwards-Jones V, Sutton CW, Fox AJ. Optimisation of intact cell MALDI method for fingerprinting of methicillin-resistant Staphylococcus aureus. J Microbiol Methods. 2005 Sep;62(3):273–284. https://doi.org/10.1016/j.mimet.2005.04.015
Search in Google Scholar Back to article
Jarzembowski T, Daca A, Witkowski J, Rutkowski B, Gołębiewska J, Dębska-Ślizień A. Does CMV infection impact the virulence of Enterococcus faecalis? Virulence. 2013 Oct;4(7):641–645. https://doi.org/10.4161/viru.26315
Search in Google Scholar Back to article
Josten M, Reif M, Szekat C, Al-Sabti N, Roemer T, Sparbier K, Kostrzewa M, Rohde H, Sahl HG, Bierbaum G. Analysis of the matrix-assisted laser desorption ionization-time of flight mass spectrum of Staphylococcus aureus identifies mutations that allow differentiation of the main clonal lineages. J Clin Microbiol. 2013 Jun; 51(6):1809–1817. https://doi.org/10.1128/JCM.00518-13
Search in Google Scholar Back to article
Kwapisz E, Garbacz K, Kosecka-Strojek M, Schubert J, Bania J, Międzobrodzki J. Presence of egc-positive major clones ST 45, 30 and 22 among methicillin-resistant and methicillin-susceptible oral Staphylococcus aureus strains. Sci Rep. 2020 Nov;10(1):18889. https://doi.org/10.1038/s41598-020-76009-1
Search in Google Scholar Back to article
Lai CC, Liu YH, Wang CY, Wang YH, Hsueh SC, Yen MY, Ko WC, Hsueh PR. Asymptomatic carrier state, acute respiratory disease, and pneumonia due to severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2): facts and myths. J Microbiol Immunol Infect. 2020 Jun;53(3):404–412. https://doi.org/10.1016/j.jmii.2020.02.012
Search in Google Scholar Back to article
Lasch P, Fleige C, Stämmler M, Layer F, Nübel U, Witte W, Werner G. Insufficient discriminatory power of MALDI-TOF mass spectrometry for typing of Enterococcus faecium and Staphylococcus aureus isolates. J Microbiol Methods. 2014 May;100:58–69. https://doi.org/10.1016/j.mimet.2014.02.015
Search in Google Scholar Back to article
Lowy FD. Staphylococcus aureus infections. N Engl J Med. 1998 Aug 20;339(8):520–532. https://doi.org/10.1056/NEJM199808203390806
Search in Google Scholar Back to article
Mirzaei R, Goodarzi P, Asadi M, Soltani A, Aljanabi HAA, Jeda AS, Dashtbin S, Jalalifar S, Mohammadzadeh R, Teimoori A, et al. Bacterial co-infections with SARS-CoV-2. IUBMB Life. 2020 Oct;72(10):2097–2111. https://doi.org/10.1002/iub.2356
Search in Google Scholar Back to article
Morens DM, Taubenberger JK, Fauci AS. Predominant role of bacterial pneumonia as a cause of death in pandemic influenza: implications for pandemic influenza preparedness. J Infect Dis. 2008 Oct;198(7):962–970. https://doi.org/10.1086/591708
Search in Google Scholar Back to article
Østergaard C, Møller JK. Subdivision of MRSA CC398 isolates using MALDI-TOF MS. Int J Med Microbiol. 2018 Jun;308(4):476–485. https://doi.org/10.1016/j.ijmm.2018.04.001
Search in Google Scholar Back to article
Roe C, Stegger M, Lilje B, Johannesen TB, Ng KL, Sieber RN, Driebe E, Engelthaler DM, Andersen PS. Genomic analyses of Staphylococcus aureus clonal complex 45 isolates does not distinguish nasal carriage from bacteraemia. Microb Genom. 2020 Aug; 6(8): mgen000403. https://doi.org/10.1099/mgen.0.000403
Search in Google Scholar Back to article
Sauget M, Valot B, Bertrand X, Hocquet D. Can MALDI-TOF mass spectrometry reasonably type bacteria? Trends Microbiol. 2017 Jun;25(6):447–455. https://doi.org/10.1016/j.tim.2016.12.006
Search in Google Scholar Back to article
Shittu AO, Okon K, Adesida S, Oyedara O, Witte W, Strommenger B, Layer F, Nübel U. Antibiotic resistance and molecular epidemiology of Staphylococcus aureus in Nigeria. BMC Microbiol. 2011 May;11:92. https://doi.org/10.1186/1471-2180-11-92
Search in Google Scholar Back to article
Shopsin B, Gomez M, Montgomery SO, Smith DH, Waddington M, Dodge DE, Bost DA, Riehman M, Naidich S, Kreiswirth BN. Evaluation of protein A gene polymorphic region DNA sequencing for typing of Staphylococcus aureus strains. J Clin Microbiol. 1999 Nov;37(11):3556–3563. https://doi.org/10.1128/JCM.37.11.3556-3563.1999
Search in Google Scholar Back to article
Strohalm M, Hassman M, Kosata B, Kodícek M. mMass data miner: an open source alternative for mass spectrometric data analysis. Rapid Commun Mass Spectrom. 2008;22(6):905–908. https://doi.org/10.1002/rcm.3444
Search in Google Scholar Back to article
van Belkum A, Melles DC, Nouwen J, van Leeuwen WB, van Wamel W, Vos MC, Wertheim HF, Verbrugh HA. Co-evolutionary aspects of human colonisation and infection by Staphylococcus aureus. Infect Genet Evol. 2009 Jan;9(1):32–47. https://doi.org/10.1016/j.meegid.2008.09.012
Search in Google Scholar Back to article
Wiese-Posselt M, Heuck D, Draeger A, Mielke M, Witte W, Ammon A, Hamouda O. Successful termination of a furunculosis outbreak due to lukS-lukF-positive, methicillin-susceptible Staphylococcus aureus in a German village by stringent decolonization, 2002–2005. Clin Infect Dis. 2007 Jun;44(11):e88–e95. https://doi.org/10.1086/517503
Search in Google Scholar Back to article
Wiśniewska K, Piórkowska A, Kasprzyk J, Bronk M, Świeć K. Clonal distribution of bone sialoprotein-binding protein gene among Staphylococcus aureus isolates associated with bloodstream infections. Folia Microbiol (Praha). 2014 Nov;59(6):465–471. https://doi.org/10.1007/s12223-014-0321-7
Search in Google Scholar Back to article
Wolters M, Rohde H, Maier T, Belmar-Campos C, Franke G, Scherpe S, Aepfelbacher M, Christner M. MALDI-TOF MS fingerprinting allows for discrimination of major methicillin-resistant Staphylococcus aureus lineages. Int J Med Microbiol. 2011 Jan; 301(1):64–68. https://doi.org/10.1016/j.ijmm.2010.06.002
Search in Google Scholar Back to article

Changes in the Protein Profile in Staphylococcal Strains from Patients Infected with the SARS-CoV-2 Virus

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