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Serrapeptase impairs biofilm, wall, and phospho-homeostasis of resistant and susceptible Staphylococcus aureus
ABSTRACT: Staphylococcus aureus biofilms are implicated in hospital infections due to elevated antibiotic and host immune system resistance. Molecular components of cell wall including amyloid proteins, peptidoglycans (PGs), and lipoteichoic acid (LTA) are crucial for biofilm formation and tolerance...
Autores principales: | , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
Springer Berlin Heidelberg
2023
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9898353/ https://www.ncbi.nlm.nih.gov/pubmed/36635396 http://dx.doi.org/10.1007/s00253-022-12356-5 |
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author | Katsipis, Georgios Pantazaki, Anastasia A. |
author_facet | Katsipis, Georgios Pantazaki, Anastasia A. |
author_sort | Katsipis, Georgios |
collection | PubMed |
description | ABSTRACT: Staphylococcus aureus biofilms are implicated in hospital infections due to elevated antibiotic and host immune system resistance. Molecular components of cell wall including amyloid proteins, peptidoglycans (PGs), and lipoteichoic acid (LTA) are crucial for biofilm formation and tolerance of methicillin-resistant S. aureus (MRSA). Significance of alkaline phosphatases (ALPs) for biofilm formation has been recorded. Serrapeptase (SPT), a protease of Serratia marcescens, possesses antimicrobial properties similar or superior to those of many antibiotics. In the present study, SPT anti-biofilm activity was demonstrated against S. aureus (ATCC 25923, methicillin-susceptible strain, methicillin-susceptible S. aureus (MSSA)) and MRSA (ST80), with IC(50) values of 0.67 μg/mL and 7.70 μg/mL, respectively. SPT affected bacterial viability, causing a maximum inhibition of − 46% and − 27%, respectively. Decreased PGs content at [SPT] ≥ 0.5 μg/mL and ≥ 8 μg/mL was verified for MSSA and MRSA, respectively. In MSSA, LTA levels decreased significantly (up to − 40%) at lower SPT doses but increased at the highest dose of 2 μg/mL, a counter to spectacularly increased cellular and secreted LTA levels in MRSA. SPT also reduced amyloids of both strains. Additionally, intracellular ALP activity decreased in both MSSA and MRSA (up to − 85% and − 89%, respectively), while extracellular activity increased up to + 482% in MSSA and + 267% in MRSA. Altered levels of DING proteins, which are involved in phosphate metabolism, in SPT-treated bacteria, were also demonstrated here, implying impaired phosphorus homeostasis. The differential alterations in the studied molecular aspects underline the differences between MSSA and MRSA and offer new insights in the treatment of resistant bacterial biofilms. KEY POINTS: • SPT inhibits biofilm formation in methicillin-resistant and methicillin-susceptible S. aureus. • SPT treatment decreases bacterial viability, ALP activity, and cell wall composition. • SPT-treated bacteria present altered levels of phosphate-related DING proteins. GRAPHICAL ABSTRACT: [Image: see text] SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1007/s00253-022-12356-5. |
format | Online Article Text |
id | pubmed-9898353 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2023 |
publisher | Springer Berlin Heidelberg |
record_format | MEDLINE/PubMed |
spelling | pubmed-98983532023-02-05 Serrapeptase impairs biofilm, wall, and phospho-homeostasis of resistant and susceptible Staphylococcus aureus Katsipis, Georgios Pantazaki, Anastasia A. Appl Microbiol Biotechnol Applied Microbial and Cell Physiology ABSTRACT: Staphylococcus aureus biofilms are implicated in hospital infections due to elevated antibiotic and host immune system resistance. Molecular components of cell wall including amyloid proteins, peptidoglycans (PGs), and lipoteichoic acid (LTA) are crucial for biofilm formation and tolerance of methicillin-resistant S. aureus (MRSA). Significance of alkaline phosphatases (ALPs) for biofilm formation has been recorded. Serrapeptase (SPT), a protease of Serratia marcescens, possesses antimicrobial properties similar or superior to those of many antibiotics. In the present study, SPT anti-biofilm activity was demonstrated against S. aureus (ATCC 25923, methicillin-susceptible strain, methicillin-susceptible S. aureus (MSSA)) and MRSA (ST80), with IC(50) values of 0.67 μg/mL and 7.70 μg/mL, respectively. SPT affected bacterial viability, causing a maximum inhibition of − 46% and − 27%, respectively. Decreased PGs content at [SPT] ≥ 0.5 μg/mL and ≥ 8 μg/mL was verified for MSSA and MRSA, respectively. In MSSA, LTA levels decreased significantly (up to − 40%) at lower SPT doses but increased at the highest dose of 2 μg/mL, a counter to spectacularly increased cellular and secreted LTA levels in MRSA. SPT also reduced amyloids of both strains. Additionally, intracellular ALP activity decreased in both MSSA and MRSA (up to − 85% and − 89%, respectively), while extracellular activity increased up to + 482% in MSSA and + 267% in MRSA. Altered levels of DING proteins, which are involved in phosphate metabolism, in SPT-treated bacteria, were also demonstrated here, implying impaired phosphorus homeostasis. The differential alterations in the studied molecular aspects underline the differences between MSSA and MRSA and offer new insights in the treatment of resistant bacterial biofilms. KEY POINTS: • SPT inhibits biofilm formation in methicillin-resistant and methicillin-susceptible S. aureus. • SPT treatment decreases bacterial viability, ALP activity, and cell wall composition. • SPT-treated bacteria present altered levels of phosphate-related DING proteins. GRAPHICAL ABSTRACT: [Image: see text] SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1007/s00253-022-12356-5. Springer Berlin Heidelberg 2023-01-13 2023 /pmc/articles/PMC9898353/ /pubmed/36635396 http://dx.doi.org/10.1007/s00253-022-12356-5 Text en © The Author(s) 2023 https://creativecommons.org/licenses/by/4.0/Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . |
spellingShingle | Applied Microbial and Cell Physiology Katsipis, Georgios Pantazaki, Anastasia A. Serrapeptase impairs biofilm, wall, and phospho-homeostasis of resistant and susceptible Staphylococcus aureus |
title | Serrapeptase impairs biofilm, wall, and phospho-homeostasis of resistant and susceptible Staphylococcus aureus |
title_full | Serrapeptase impairs biofilm, wall, and phospho-homeostasis of resistant and susceptible Staphylococcus aureus |
title_fullStr | Serrapeptase impairs biofilm, wall, and phospho-homeostasis of resistant and susceptible Staphylococcus aureus |
title_full_unstemmed | Serrapeptase impairs biofilm, wall, and phospho-homeostasis of resistant and susceptible Staphylococcus aureus |
title_short | Serrapeptase impairs biofilm, wall, and phospho-homeostasis of resistant and susceptible Staphylococcus aureus |
title_sort | serrapeptase impairs biofilm, wall, and phospho-homeostasis of resistant and susceptible staphylococcus aureus |
topic | Applied Microbial and Cell Physiology |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9898353/ https://www.ncbi.nlm.nih.gov/pubmed/36635396 http://dx.doi.org/10.1007/s00253-022-12356-5 |
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