Species-Specific Recognition of <italic toggle="yes">Sulfolobales</italic> Mediated by UV-Inducible Pili and S-Layer Glycosylation Patterns

ABSTRACT The UV-inducible pili system of Sulfolobales (Ups) mediates the formation of species-specific cellular aggregates. Within these aggregates, cells exchange DNA to repair DNA double-strand breaks via homologous recombination. Substitution of the Sulfolobus acidocaldarius pilin subunits UpsA a...

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Autores principales: Marleen van Wolferen, Asif Shajahan, Kristina Heinrich, Susanne Brenzinger, Ian M. Black, Alexander Wagner, Ariane Briegel, Parastoo Azadi, Sonja-Verena Albers
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Publicado: American Society for Microbiology 2020
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spelling oai:doaj.org-article:85b42167652c4126972a5439f180f1d72021-11-15T15:57:02ZSpecies-Specific Recognition of <italic toggle="yes">Sulfolobales</italic> Mediated by UV-Inducible Pili and S-Layer Glycosylation Patterns10.1128/mBio.03014-192150-7511https://doaj.org/article/85b42167652c4126972a5439f180f1d72020-04-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.03014-19https://doaj.org/toc/2150-7511ABSTRACT The UV-inducible pili system of Sulfolobales (Ups) mediates the formation of species-specific cellular aggregates. Within these aggregates, cells exchange DNA to repair DNA double-strand breaks via homologous recombination. Substitution of the Sulfolobus acidocaldarius pilin subunits UpsA and UpsB with their homologs from Sulfolobus tokodaii showed that these subunits facilitate species-specific aggregation. A region of low conservation within the UpsA homologs is primarily important for this specificity. Aggregation assays in the presence of different sugars showed the importance of N-glycosylation in the recognition process. In addition, the N-glycan decorating the S-layer of S. tokodaii is different from the one of S. acidocaldarius. Therefore, each Sulfolobus species seems to have developed a unique UpsA binding pocket and unique N-glycan composition to ensure aggregation and, consequently, also DNA exchange with cells from only the same species, which is essential for DNA repair by homologous recombination. IMPORTANCE Type IV pili can be found on the cell surface of many archaea and bacteria where they play important roles in different processes. The UV-inducible pili system of Sulfolobales (Ups) pili from the crenarchaeal Sulfolobales species are essential in establishing species-specific mating partners, thereby assisting in genome stability. With this work, we show that different Sulfolobus species have specific regions in their Ups pili subunits, which allow them to interact only with cells from the same species. Additionally, different Sulfolobus species have unique surface-layer N-glycosylation patterns. We propose that the unique features of each species allow the recognition of specific mating partners. This knowledge for the first time gives insights into the molecular basis of archaeal self-recognition.Marleen van WolferenAsif ShajahanKristina HeinrichSusanne BrenzingerIan M. BlackAlexander WagnerAriane BriegelParastoo AzadiSonja-Verena AlbersAmerican Society for Microbiologyarticletype IV piliarchaeaSulfolobusDNA exchangeglycosylationspecies-specific recognitionMicrobiologyQR1-502ENmBio, Vol 11, Iss 2 (2020)
institution DOAJ
collection DOAJ
language EN
topic type IV pili
archaea
Sulfolobus
DNA exchange
glycosylation
species-specific recognition
Microbiology
QR1-502
spellingShingle type IV pili
archaea
Sulfolobus
DNA exchange
glycosylation
species-specific recognition
Microbiology
QR1-502
Marleen van Wolferen
Asif Shajahan
Kristina Heinrich
Susanne Brenzinger
Ian M. Black
Alexander Wagner
Ariane Briegel
Parastoo Azadi
Sonja-Verena Albers
Species-Specific Recognition of <italic toggle="yes">Sulfolobales</italic> Mediated by UV-Inducible Pili and S-Layer Glycosylation Patterns
description ABSTRACT The UV-inducible pili system of Sulfolobales (Ups) mediates the formation of species-specific cellular aggregates. Within these aggregates, cells exchange DNA to repair DNA double-strand breaks via homologous recombination. Substitution of the Sulfolobus acidocaldarius pilin subunits UpsA and UpsB with their homologs from Sulfolobus tokodaii showed that these subunits facilitate species-specific aggregation. A region of low conservation within the UpsA homologs is primarily important for this specificity. Aggregation assays in the presence of different sugars showed the importance of N-glycosylation in the recognition process. In addition, the N-glycan decorating the S-layer of S. tokodaii is different from the one of S. acidocaldarius. Therefore, each Sulfolobus species seems to have developed a unique UpsA binding pocket and unique N-glycan composition to ensure aggregation and, consequently, also DNA exchange with cells from only the same species, which is essential for DNA repair by homologous recombination. IMPORTANCE Type IV pili can be found on the cell surface of many archaea and bacteria where they play important roles in different processes. The UV-inducible pili system of Sulfolobales (Ups) pili from the crenarchaeal Sulfolobales species are essential in establishing species-specific mating partners, thereby assisting in genome stability. With this work, we show that different Sulfolobus species have specific regions in their Ups pili subunits, which allow them to interact only with cells from the same species. Additionally, different Sulfolobus species have unique surface-layer N-glycosylation patterns. We propose that the unique features of each species allow the recognition of specific mating partners. This knowledge for the first time gives insights into the molecular basis of archaeal self-recognition.
format article
author Marleen van Wolferen
Asif Shajahan
Kristina Heinrich
Susanne Brenzinger
Ian M. Black
Alexander Wagner
Ariane Briegel
Parastoo Azadi
Sonja-Verena Albers
author_facet Marleen van Wolferen
Asif Shajahan
Kristina Heinrich
Susanne Brenzinger
Ian M. Black
Alexander Wagner
Ariane Briegel
Parastoo Azadi
Sonja-Verena Albers
author_sort Marleen van Wolferen
title Species-Specific Recognition of <italic toggle="yes">Sulfolobales</italic> Mediated by UV-Inducible Pili and S-Layer Glycosylation Patterns
title_short Species-Specific Recognition of <italic toggle="yes">Sulfolobales</italic> Mediated by UV-Inducible Pili and S-Layer Glycosylation Patterns
title_full Species-Specific Recognition of <italic toggle="yes">Sulfolobales</italic> Mediated by UV-Inducible Pili and S-Layer Glycosylation Patterns
title_fullStr Species-Specific Recognition of <italic toggle="yes">Sulfolobales</italic> Mediated by UV-Inducible Pili and S-Layer Glycosylation Patterns
title_full_unstemmed Species-Specific Recognition of <italic toggle="yes">Sulfolobales</italic> Mediated by UV-Inducible Pili and S-Layer Glycosylation Patterns
title_sort species-specific recognition of <italic toggle="yes">sulfolobales</italic> mediated by uv-inducible pili and s-layer glycosylation patterns
publisher American Society for Microbiology
publishDate 2020
url https://doaj.org/article/85b42167652c4126972a5439f180f1d7
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