Biofilm formation and inflammatory potential of Staphylococcus saccharolyticus: A possible cause of orthopedic implant-associated infections
Staphylococcus saccharolyticus, a coagulase-negative staphylococcal species, has some unusual characteristics for human-associated staphylococci, such as slow growth and its preference for anoxic culture conditions. This species is a relatively abundant member of the human skin microbiota, but its m...
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| Format: | Article |
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Frontiers Media S.A.
2022-11-01
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| Series: | Frontiers in Microbiology |
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| Online Access: | https://www.frontiersin.org/articles/10.3389/fmicb.2022.1070201/full |
| _version_ | 1828279879594934272 |
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| author | Mastaneh Afshar Andreas Møllebjerg Gabriel Antonio Minero Jacqueline Hollensteiner Anja Poehlein Axel Himmelbach Jeppe Lange Jeppe Lange Rikke Louise Meyer Rikke Louise Meyer Holger Brüggemann |
| author_facet | Mastaneh Afshar Andreas Møllebjerg Gabriel Antonio Minero Jacqueline Hollensteiner Anja Poehlein Axel Himmelbach Jeppe Lange Jeppe Lange Rikke Louise Meyer Rikke Louise Meyer Holger Brüggemann |
| author_sort | Mastaneh Afshar |
| collection | DOAJ |
| description | Staphylococcus saccharolyticus, a coagulase-negative staphylococcal species, has some unusual characteristics for human-associated staphylococci, such as slow growth and its preference for anoxic culture conditions. This species is a relatively abundant member of the human skin microbiota, but its microbiological properties, as well as the pathogenic potential, have scarcely been investigated so far, despite being occasionally isolated from different types of infections including orthopedic implant-associated infections. Here, we investigated the growth and biofilm properties of clinical isolates of S. saccharolyticus and determined host cell responses. Growth assessments in anoxic and oxic conditions revealed strain-dependent outcomes, as some strains can also grow aerobically. All tested strains of S. saccharolyticus were able to form biofilm in a microtiter plate assay. Strain-dependent differences were determined by optical coherence tomography, revealing that medium supplementation with glucose and sodium chloride enhanced biofilm formation. Visualization of the biofilm by confocal laser scanning microscopy revealed the role of extracellular DNA in the biofilm structure. In addition to attached biofilms, S. saccharolyticus also formed bacterial aggregates at an early stage of growth. Transcriptome analysis of biofilm-grown versus planktonic cells revealed a set of upregulated genes in biofilm-embedded cells, including factors involved in adhesion, colonization, and competition such as epidermin, type I toxin-antitoxin system, and phenol-soluble modulins (beta and epsilon). To investigate consequences for the host after encountering S. saccharolyticus, cytokine profiling and host cell viability were assessed by infection experiments with differentiated THP-1 cells. The microorganism strongly triggered the secretion of the tested pro-inflammatory cyto- and chemokines IL-6, IL-8, and TNF-alpha, determined at 24 h post-infection. S. saccharolyticus was less cytotoxic than Staphylococcus aureus. Taken together, the results indicate that S. saccharolyticus has substantial pathogenic potential. Thus, it can be a potential cause of orthopedic implant-associated infections and other types of deep-seated infections. |
| first_indexed | 2024-04-13T07:50:14Z |
| format | Article |
| id | doaj.art-43041ea25c3d400fb1f0f528924d827f |
| institution | Directory Open Access Journal |
| issn | 1664-302X |
| language | English |
| last_indexed | 2024-04-13T07:50:14Z |
| publishDate | 2022-11-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Microbiology |
| spelling | doaj.art-43041ea25c3d400fb1f0f528924d827f2022-12-22T02:55:33ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2022-11-011310.3389/fmicb.2022.10702011070201Biofilm formation and inflammatory potential of Staphylococcus saccharolyticus: A possible cause of orthopedic implant-associated infectionsMastaneh Afshar0Andreas Møllebjerg1Gabriel Antonio Minero2Jacqueline Hollensteiner3Anja Poehlein4Axel Himmelbach5Jeppe Lange6Jeppe Lange7Rikke Louise Meyer8Rikke Louise Meyer9Holger Brüggemann10Department of Biomedicine, Aarhus University, Aarhus, DenmarkInterdisciplinary Nanoscience Center (iNANO), Aarhus University, Aarhus, DenmarkInterdisciplinary Nanoscience Center (iNANO), Aarhus University, Aarhus, DenmarkDepartment of Genomic and Applied Microbiology, Institute of Microbiology and Genetics, University of Göttingen, Göttingen, GermanyDepartment of Genomic and Applied Microbiology, Institute of Microbiology and Genetics, University of Göttingen, Göttingen, GermanyLeibniz Institute of Plant Genetics and Crop Plant Research (IPK), Gatersleben, GermanyDepartment of Clinical Medicine, Aarhus University, Aarhus, DenmarkDepartment of Orthopedic Surgery Horsens Regional Hospital, Horsens, DenmarkInterdisciplinary Nanoscience Center (iNANO), Aarhus University, Aarhus, DenmarkDepartment of Biology, Aarhus University, Aarhus, DenmarkDepartment of Biomedicine, Aarhus University, Aarhus, DenmarkStaphylococcus saccharolyticus, a coagulase-negative staphylococcal species, has some unusual characteristics for human-associated staphylococci, such as slow growth and its preference for anoxic culture conditions. This species is a relatively abundant member of the human skin microbiota, but its microbiological properties, as well as the pathogenic potential, have scarcely been investigated so far, despite being occasionally isolated from different types of infections including orthopedic implant-associated infections. Here, we investigated the growth and biofilm properties of clinical isolates of S. saccharolyticus and determined host cell responses. Growth assessments in anoxic and oxic conditions revealed strain-dependent outcomes, as some strains can also grow aerobically. All tested strains of S. saccharolyticus were able to form biofilm in a microtiter plate assay. Strain-dependent differences were determined by optical coherence tomography, revealing that medium supplementation with glucose and sodium chloride enhanced biofilm formation. Visualization of the biofilm by confocal laser scanning microscopy revealed the role of extracellular DNA in the biofilm structure. In addition to attached biofilms, S. saccharolyticus also formed bacterial aggregates at an early stage of growth. Transcriptome analysis of biofilm-grown versus planktonic cells revealed a set of upregulated genes in biofilm-embedded cells, including factors involved in adhesion, colonization, and competition such as epidermin, type I toxin-antitoxin system, and phenol-soluble modulins (beta and epsilon). To investigate consequences for the host after encountering S. saccharolyticus, cytokine profiling and host cell viability were assessed by infection experiments with differentiated THP-1 cells. The microorganism strongly triggered the secretion of the tested pro-inflammatory cyto- and chemokines IL-6, IL-8, and TNF-alpha, determined at 24 h post-infection. S. saccharolyticus was less cytotoxic than Staphylococcus aureus. Taken together, the results indicate that S. saccharolyticus has substantial pathogenic potential. Thus, it can be a potential cause of orthopedic implant-associated infections and other types of deep-seated infections.https://www.frontiersin.org/articles/10.3389/fmicb.2022.1070201/fullStaphylococcus saccharolyticuscoagulase-negative staphylococcianaerobesbiofilmtranscriptomeinflammation |
| spellingShingle | Mastaneh Afshar Andreas Møllebjerg Gabriel Antonio Minero Jacqueline Hollensteiner Anja Poehlein Axel Himmelbach Jeppe Lange Jeppe Lange Rikke Louise Meyer Rikke Louise Meyer Holger Brüggemann Biofilm formation and inflammatory potential of Staphylococcus saccharolyticus: A possible cause of orthopedic implant-associated infections Frontiers in Microbiology Staphylococcus saccharolyticus coagulase-negative staphylococci anaerobes biofilm transcriptome inflammation |
| title | Biofilm formation and inflammatory potential of Staphylococcus saccharolyticus: A possible cause of orthopedic implant-associated infections |
| title_full | Biofilm formation and inflammatory potential of Staphylococcus saccharolyticus: A possible cause of orthopedic implant-associated infections |
| title_fullStr | Biofilm formation and inflammatory potential of Staphylococcus saccharolyticus: A possible cause of orthopedic implant-associated infections |
| title_full_unstemmed | Biofilm formation and inflammatory potential of Staphylococcus saccharolyticus: A possible cause of orthopedic implant-associated infections |
| title_short | Biofilm formation and inflammatory potential of Staphylococcus saccharolyticus: A possible cause of orthopedic implant-associated infections |
| title_sort | biofilm formation and inflammatory potential of staphylococcus saccharolyticus a possible cause of orthopedic implant associated infections |
| topic | Staphylococcus saccharolyticus coagulase-negative staphylococci anaerobes biofilm transcriptome inflammation |
| url | https://www.frontiersin.org/articles/10.3389/fmicb.2022.1070201/full |
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