Distinct Requirements for Tail-Anchored Membrane Protein Biogenesis in <named-content content-type="genus-species">Escherichia coli</named-content>

ABSTRACT Tail-anchored membrane proteins (TAMPs) are a distinct subset of inner membrane proteins (IMPs) characterized by a single C-terminal transmembrane domain (TMD) that is responsible for both targeting and anchoring. Little is known about the routing of TAMPs in bacteria. Here, we have investi...

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Autores principales:	Markus Peschke, Mélanie Le Goff, Gregory M. Koningstein, Norbert O. Vischer, Abbi Abdel-Rehim, Stephen High, Peter van Ulsen, Joen Luirink
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2019
Materias:	Escherichia coli hydrophobicity membrane proteins membrane targeting tail-anchored Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/5a939ea9bcec43ba9f5d870883c209e8
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spelling	oai:doaj.org-article:5a939ea9bcec43ba9f5d870883c209e82021-11-15T15:59:41ZDistinct Requirements for Tail-Anchored Membrane Protein Biogenesis in <named-content content-type="genus-species">Escherichia coli</named-content>10.1128/mBio.01580-192150-7511https://doaj.org/article/5a939ea9bcec43ba9f5d870883c209e82019-10-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.01580-19https://doaj.org/toc/2150-7511ABSTRACT Tail-anchored membrane proteins (TAMPs) are a distinct subset of inner membrane proteins (IMPs) characterized by a single C-terminal transmembrane domain (TMD) that is responsible for both targeting and anchoring. Little is known about the routing of TAMPs in bacteria. Here, we have investigated the role of TMD hydrophobicity in tail-anchor function in Escherichia coli and its influence on the choice of targeting/insertion pathway. We created a set of synthetic, fluorescent TAMPs that vary in the hydrophobicity of their TMDs and corresponding control polypeptides that are extended at their C terminus to create regular type II IMPs. Surprisingly, we observed that TAMPs have a much lower TMD hydrophobicity threshold for efficient targeting and membrane insertion than their type II counterparts. Using strains conditional for the expression of known membrane-targeting and insertion factors, we show that TAMPs with strongly hydrophobic TMDs require the signal recognition particle (SRP) for targeting. Neither the SecYEG translocon nor YidC appears to be essential for the membrane insertion of any of the TAMPs studied. In contrast, corresponding type II IMPs with a TMD of sufficient hydrophobicity to promote membrane insertion followed an SRP- and SecYEG translocon-dependent pathway. Together, these data indicate that the capacity of a TMD to promote the biogenesis of E. coli IMPs is strongly dependent upon the polypeptide context in which it is presented. IMPORTANCE A subset of membrane proteins is targeted to and inserted into the membrane via a hydrophobic transmembrane domain (TMD) that is positioned at the very C terminus of the protein. The biogenesis of these so-called tail-anchored proteins (TAMPs) has been studied in detail in eukaryotic cells. Various partly redundant pathways were identified, the choice for which depends in part on the hydrophobicity of the TMD. Much less is known about bacterial TAMPs. The significance of our research is in identifying the role of TMD hydrophobicity in the routing of E. coli TAMPs. Our data suggest that both the nature of the TMD and its role in routing can be very different for TAMPs versus “regular” membrane proteins. Elucidating these position-specific effects of TMDs will increase our understanding of how prokaryotic cells face the challenge of producing a wide variety of membrane proteins.Markus PeschkeMélanie Le GoffGregory M. KoningsteinNorbert O. VischerAbbi Abdel-RehimStephen HighPeter van UlsenJoen LuirinkAmerican Society for MicrobiologyarticleEscherichia colihydrophobicitymembrane proteinsmembrane targetingtail-anchoredMicrobiologyQR1-502ENmBio, Vol 10, Iss 5 (2019)
institution	DOAJ
collection	DOAJ
language	EN
topic	Escherichia coli hydrophobicity membrane proteins membrane targeting tail-anchored Microbiology QR1-502
spellingShingle	Escherichia coli hydrophobicity membrane proteins membrane targeting tail-anchored Microbiology QR1-502 Markus Peschke Mélanie Le Goff Gregory M. Koningstein Norbert O. Vischer Abbi Abdel-Rehim Stephen High Peter van Ulsen Joen Luirink Distinct Requirements for Tail-Anchored Membrane Protein Biogenesis in <named-content content-type="genus-species">Escherichia coli</named-content>
description	ABSTRACT Tail-anchored membrane proteins (TAMPs) are a distinct subset of inner membrane proteins (IMPs) characterized by a single C-terminal transmembrane domain (TMD) that is responsible for both targeting and anchoring. Little is known about the routing of TAMPs in bacteria. Here, we have investigated the role of TMD hydrophobicity in tail-anchor function in Escherichia coli and its influence on the choice of targeting/insertion pathway. We created a set of synthetic, fluorescent TAMPs that vary in the hydrophobicity of their TMDs and corresponding control polypeptides that are extended at their C terminus to create regular type II IMPs. Surprisingly, we observed that TAMPs have a much lower TMD hydrophobicity threshold for efficient targeting and membrane insertion than their type II counterparts. Using strains conditional for the expression of known membrane-targeting and insertion factors, we show that TAMPs with strongly hydrophobic TMDs require the signal recognition particle (SRP) for targeting. Neither the SecYEG translocon nor YidC appears to be essential for the membrane insertion of any of the TAMPs studied. In contrast, corresponding type II IMPs with a TMD of sufficient hydrophobicity to promote membrane insertion followed an SRP- and SecYEG translocon-dependent pathway. Together, these data indicate that the capacity of a TMD to promote the biogenesis of E. coli IMPs is strongly dependent upon the polypeptide context in which it is presented. IMPORTANCE A subset of membrane proteins is targeted to and inserted into the membrane via a hydrophobic transmembrane domain (TMD) that is positioned at the very C terminus of the protein. The biogenesis of these so-called tail-anchored proteins (TAMPs) has been studied in detail in eukaryotic cells. Various partly redundant pathways were identified, the choice for which depends in part on the hydrophobicity of the TMD. Much less is known about bacterial TAMPs. The significance of our research is in identifying the role of TMD hydrophobicity in the routing of E. coli TAMPs. Our data suggest that both the nature of the TMD and its role in routing can be very different for TAMPs versus “regular” membrane proteins. Elucidating these position-specific effects of TMDs will increase our understanding of how prokaryotic cells face the challenge of producing a wide variety of membrane proteins.
format	article
author	Markus Peschke Mélanie Le Goff Gregory M. Koningstein Norbert O. Vischer Abbi Abdel-Rehim Stephen High Peter van Ulsen Joen Luirink
author_facet	Markus Peschke Mélanie Le Goff Gregory M. Koningstein Norbert O. Vischer Abbi Abdel-Rehim Stephen High Peter van Ulsen Joen Luirink
author_sort	Markus Peschke
title	Distinct Requirements for Tail-Anchored Membrane Protein Biogenesis in <named-content content-type="genus-species">Escherichia coli</named-content>
title_short	Distinct Requirements for Tail-Anchored Membrane Protein Biogenesis in <named-content content-type="genus-species">Escherichia coli</named-content>
title_full	Distinct Requirements for Tail-Anchored Membrane Protein Biogenesis in <named-content content-type="genus-species">Escherichia coli</named-content>
title_fullStr	Distinct Requirements for Tail-Anchored Membrane Protein Biogenesis in <named-content content-type="genus-species">Escherichia coli</named-content>
title_full_unstemmed	Distinct Requirements for Tail-Anchored Membrane Protein Biogenesis in <named-content content-type="genus-species">Escherichia coli</named-content>
title_sort	distinct requirements for tail-anchored membrane protein biogenesis in <named-content content-type="genus-species">escherichia coli</named-content>
publisher	American Society for Microbiology
publishDate	2019
url	https://doaj.org/article/5a939ea9bcec43ba9f5d870883c209e8
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Distinct Requirements for Tail-Anchored Membrane Protein Biogenesis in <named-content content-type="genus-species">Escherichia coli</named-content>

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