High-throughput functional analysis provides novel insight into type VII secretion in Staphylococcus aureus

Successful colonization by the opportunistic pathogen Staphylococcus aureus depends on its ability to interact with other microorganisms. Staphylococcus aureus strains harbour a T7b subtype of type VII secretion system (T7SSb), a protein secretion system found in a wide variety of Bacillota, which f...

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Main Authors: Yaping Yang, Aaron A. Scott, Holger Kneuper, Felicity Alcock, Tracy Palmer
Format: Article
Language:English
Published: The Royal Society 2024-08-01
Series:Open Biology
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Online Access:https://royalsocietypublishing.org/doi/10.1098/rsob.240060
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author Yaping Yang
Aaron A. Scott
Holger Kneuper
Felicity Alcock
Tracy Palmer
author_facet Yaping Yang
Aaron A. Scott
Holger Kneuper
Felicity Alcock
Tracy Palmer
author_sort Yaping Yang
collection DOAJ
description Successful colonization by the opportunistic pathogen Staphylococcus aureus depends on its ability to interact with other microorganisms. Staphylococcus aureus strains harbour a T7b subtype of type VII secretion system (T7SSb), a protein secretion system found in a wide variety of Bacillota, which functions in bacterial antagonism and virulence. Assessment of T7SSb activity in S. aureus has been hampered by low secretion activity under laboratory conditions and the lack of a sensitive assay to measure secretion. Here, we have utilized NanoLuc binary technology to develop a simple assay to monitor protein secretion via detection of bioluminescence. Fusion of the 11 amino acid NanoLuc fragment to the conserved substrate EsxA permits its extracellular detection upon supplementation with the large NanoLuc fragment and luciferase substrate. Following miniaturization of the assay to 384-well format, we use high-throughput analysis to demonstrate that T7SSb-dependent protein secretion differs across strains and growth temperature. We further show that the same assay can be used to monitor secretion of the surface-associated toxin substrate TspA. Using this approach, we identify three conserved accessory proteins required to mediate TspA secretion. Co-purification experiments confirm that all three proteins form a complex with TspA.
format Article
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publishDate 2024-08-01
publisher The Royal Society
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spelling doaj-art-e7e60f5eb285483daf48771a66a32a2c2025-08-20T02:14:49ZengThe Royal SocietyOpen Biology2046-24412024-08-0114810.1098/rsob.240060High-throughput functional analysis provides novel insight into type VII secretion in Staphylococcus aureusYaping Yang0Aaron A. Scott1Holger Kneuper2Felicity Alcock3Tracy Palmer4Newcastle University Biosciences Institute, Newcastle University , Newcastle upon Tyne NE2 4HH, UKNewcastle University Biosciences Institute, Newcastle University , Newcastle upon Tyne NE2 4HH, UKNewcastle University Biosciences Institute, Newcastle University , Newcastle upon Tyne NE2 4HH, UKNewcastle University Biosciences Institute, Newcastle University , Newcastle upon Tyne NE2 4HH, UKNewcastle University Biosciences Institute, Newcastle University , Newcastle upon Tyne NE2 4HH, UKSuccessful colonization by the opportunistic pathogen Staphylococcus aureus depends on its ability to interact with other microorganisms. Staphylococcus aureus strains harbour a T7b subtype of type VII secretion system (T7SSb), a protein secretion system found in a wide variety of Bacillota, which functions in bacterial antagonism and virulence. Assessment of T7SSb activity in S. aureus has been hampered by low secretion activity under laboratory conditions and the lack of a sensitive assay to measure secretion. Here, we have utilized NanoLuc binary technology to develop a simple assay to monitor protein secretion via detection of bioluminescence. Fusion of the 11 amino acid NanoLuc fragment to the conserved substrate EsxA permits its extracellular detection upon supplementation with the large NanoLuc fragment and luciferase substrate. Following miniaturization of the assay to 384-well format, we use high-throughput analysis to demonstrate that T7SSb-dependent protein secretion differs across strains and growth temperature. We further show that the same assay can be used to monitor secretion of the surface-associated toxin substrate TspA. Using this approach, we identify three conserved accessory proteins required to mediate TspA secretion. Co-purification experiments confirm that all three proteins form a complex with TspA.https://royalsocietypublishing.org/doi/10.1098/rsob.240060type VII secretion systemStaphylococcus aureusbioluminescenceNanoBittoxinaccessory factors
spellingShingle Yaping Yang
Aaron A. Scott
Holger Kneuper
Felicity Alcock
Tracy Palmer
High-throughput functional analysis provides novel insight into type VII secretion in Staphylococcus aureus
Open Biology
type VII secretion system
Staphylococcus aureus
bioluminescence
NanoBit
toxin
accessory factors
title High-throughput functional analysis provides novel insight into type VII secretion in Staphylococcus aureus
title_full High-throughput functional analysis provides novel insight into type VII secretion in Staphylococcus aureus
title_fullStr High-throughput functional analysis provides novel insight into type VII secretion in Staphylococcus aureus
title_full_unstemmed High-throughput functional analysis provides novel insight into type VII secretion in Staphylococcus aureus
title_short High-throughput functional analysis provides novel insight into type VII secretion in Staphylococcus aureus
title_sort high throughput functional analysis provides novel insight into type vii secretion in staphylococcus aureus
topic type VII secretion system
Staphylococcus aureus
bioluminescence
NanoBit
toxin
accessory factors
url https://royalsocietypublishing.org/doi/10.1098/rsob.240060
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