An important function in protein folding is the formation of disulfide bonds. In different compartments of bacteria specific oxido reductases are responsible for this function. Thanks to the identification of all genes from various model organisms the understanding of the function of the various members of this family has increased dramatically. 

Zie: Summary

Dorenbos, Ronald,

An important function in protein folding is the formation of disulfide bonds. In different compartments of bacteria specific oxido reductases are responsible for this function. Thanks to the identification of all genes from various model organisms the understanding of the function of the various members of this family has increased dramatically. Zie: Summar

Dorenbos, Ronald

ARTS repository - University of Groningen

   University of GroningenThiol-disulfide oxidoreductases in Bacillus subtilisDorenbos, RonaldIMPORTANT NOTE: You are advised to consult the publisher's version (publisher's PDF) if you wish to cite fromit. Please check the document version below.Document VersionPublisher's PDF, also known as Version of recordPublication date:2004Link to publication in University of Groningen/UMCG research databaseCitation for published version (APA):Dorenbos, R. (2004). Thiol-disulfide oxidoreductases in Bacillus subtilis. s.n.CopyrightOther than for strictly personal use, it is not permitted to download or to forward/distribute the text or part of it without the consent of theauthor(s) and/or copyright holder(s), unless the work is under an open content license (like Creative Commons).The publication may also be distributed here under the terms of Article 25fa of the Dutch Copyright Act, indicated by the “Taverne” license.More information can be found on the University of Groningen website: https://www.rug.nl/library/open-access/self-archiving-pure/taverne-amendment.Take-down policyIf you believe that this document breaches copyright please contact us providing details, and we will remove access to the work immediatelyand investigate your claim.Downloaded from the University of Groningen/UMCG research database (Pure): http://www.rug.nl/research/portal. For technical reasons thenumber of authors shown on this cover page is limited to 10 maximum.Download date: 16-07-2023 Thiol-disulfide Oxidoreductases in Bacillus subtilisRonald Dorenbos    RIJKSUNIVERSITEIT GRONINGEN     Thiol-disulfide Oxidoreductases in Bacillus subtilis    Proefschrift   ter verkrijging van het doctoraat in de Wiskunde en Natuurwetenschappen aan de Rijksuniversiteit Groningen op gezag van Rector Magnificus, dr. F. Zwarts, in het openbaar te verdedigen op dinsdag 21 december 2004 om 13.15 uur   door   Ronald Dorenbos    geboren op 8 mei 1972 te Winschoten   Promotores:   Prof. Dr. W.J. Quax     Prof. Dr. J.M. van Dijl    Beoordelingscommissie:  Prof. Dr. O.P. Kuipers Prof. Dr. B. Oudega Prof. Dr. M. Sarvas                                 Only those who will risk going too far  can possibly find out how far one can go.   Thomas Stearns Eliot (1888-1965)     Paranimfen:   Joost Folgering  Mattijs Julsing                               Voor mijn ouders,   Jaap & Wiesje Dorenbos                    This research was performed at the Department of Pharmaceutical Biology of the University of Groningen, the Netherlands. Funding for the work described in this thesis, was provided by the Commission of the European Union Projects BIO4-CT98-0250, QLK3-CT-1999-00413, and QLK3-CT-1999-00917.   Publication of this thesis has been made possible by financial support from the Groningen University Institute for Drug Exploration (GUIDE), Novozymes A/S (Denmark), and Genencor International Inc. (Palo Alto, California). Their contributions are greatly acknowledged.   ISBN: 90-9018901-7   Copyright © 2004 R. Dorenbos. All rights reserved. This book, or any parts thereof, may not be reproduced or transmitted by any means or in any form, without permission from the author.   Cover design by Ronald Dorenbos. Electron microscopic pictures used for the cover, the bookmark, and the chapter heads were made by Ietse Stokroos.            Contents  1 Introduction  Thiol-disulfide Oxidoreductases ........................................ 16 1.1 Protein production ........................................................................... 16 1.2 Thiol-disulfide Oxidoreductases in E. coli ...................................... 19 1.2.1 DsbA........................................................................................ 21 1.2.2 DsbB........................................................................................ 24 1.2.3 DsbC........................................................................................ 27 1.2.4 DsbD........................................................................................ 29 1.2.5 DsbE ........................................................................................ 32 1.2.6 DsbG........................................................................................ 34 1.2.7 Other E. coli proteins implicated in disulfide bond formation. 35 1.3 Thiol-disulfide Oxidoreductases in B. subtilis................................. 36 1.3.1 Bacillus subtilis........................................................................ 36 1.3.2 The cytoplasm of B. subtilis .................................................... 37 1.3.3 Identification of thiol-disulfide oxidoreductases in Bacillus ... 40 1.3.4 BdbA and BdbB....................................................................... 41 1.3.5 BdbC and BdbD....................................................................... 44 1.3.6 Other B. subtilis proteins implicated in disulfide bond formation 46 1.3.7 Thiol-disulfide Oxidoreductases in Other Organisms ............. 51 1.4 Scope of this thesis .......................................................................... 53 2 The bdbDC operon of Bacillus subtilis encodes thiol-disulfide oxidoreductases required for competence development .................................. 56 2.1 Summary.......................................................................................... 56 2.2 Introduction ..................................................................................... 57 2.3 Experimental Procedures ................................................................. 59 2.4 Results ............................................................................................. 64 2.5 Discussion........................................................................................ 78 2.6 Acknowledgements ......................................................................... 80 3 A specific stress response in Bacillus subtilis triggered by secretion of a disulfide bond-containing protein.................................................................... 82 3.1 Summary.......................................................................................... 82 3.2 Introduction ..................................................................................... 83 3.3 Experimental procedures ................................................................. 85 3.4 Results ............................................................................................. 92 3.5 Discussion...................................................................................... 102 3.6 Acknowledgements ....................................................................... 107 4 Four thiol-disulfide oxidoreductases involved in swarming motility of Bacillus subtilis ............................................................................................. 110 4.1 Summary........................................................................................ 110 4.2 Introduction ................................................................................... 111 4.3 Experimental Procedures ............................................................... 114 4.4 Results ........................................................................................... 118   4.5 Discussion...................................................................................... 123 4.6 Acknowledgements ....................................................................... 126 5 Thiol-disulfide oxidoreductases are essential for the production of the lantibiotic sublancin 168................................................................................ 128 5.1 Summary........................................................................................ 128 5.2 Introduction ................................................................................... 129 5.3 Experimental procedures ............................................................... 132 5.4 Results ........................................................................................... 137 5.5 Discussion...................................................................................... 144 5.6 Acknowledgements ....................................................................... 148 6 YolJ, a CxxS protein required for sublancin 168 production by Bacillus subtilis ........................................................................................................... 150 6.1 Summary........................................................................................ 150 6.2 Introduction ................................................................................... 151 6.3 Experimental procedures ............................................................... 153 6.4 Results ........................................................................................... 160 6.5 Discussion...................................................................................... 170 6.6 Acknowledgements ....................................................................... 174 7 Thiol-disulfide Oxidoreductases of Bacillus subtilis ............................. 176 7.1 Summary........................................................................................ 176 7.2 Introduction ................................................................................... 177 7.3 Experimental Procedures ............................................................... 179 7.4 Results ........................................................................................... 184 7.5 Discussion...................................................................................... 189 7.6 Acknowledgements ....................................................................... 192 8 Discussion & Future Perspectives ......................................................... 194 8.1 Thiol-disulfide Oxidoreductase-like proteins of B. subtilis........... 194 8.2 Thiol-disulfide oxidoreductases and improved production of heterologous proteins................................................................................. 199 8.3 Wider application potential of thiol-disulfide oxidoreductases ..... 202 8.4 Pathogenicity and thiol-disulfide oxidoreductases ........................ 204 8.5 Concluding Remarks ..................................................................... 207 9 Reference List........................................................................................ 210 10 Summary & Samenvatting................................................................. 234 10.1 Summary........................................................................................ 234 10.2 Samenvatting ................................................................................. 238 11 Dankwoord ........................................................................................ 244 12 Curriculum Vitae & Publications ...................................................... 254 12.1 Curriculum Vitae ........................................................................... 254 12.2 Publications ................................................................................... 255            

English

Thiol-disulfide oxidoreductases in Bacillus subtilis

University of Groningen Digital Archive

University of Groningen

University of Groningen Research Database

  
 University of Groningen
Thiol-disulfide oxidoreductases in Bacillus subtilis
Dorenbos, Ronald
IMPORTANT NOTE: You are advised to consult the publisher's version (publisher's PDF) if you wish to cite from
it. Please check the document version below.
Document Version
Publisher's PDF, also known as Version of record
Publication date:
2004
Link to publication in University of Groningen/UMCG research database
Citation for published version (APA):
Dorenbos, R. (2004). Thiol-disulfide oxidoreductases in Bacillus subtilis Groningen: s.n.
Copyright
Other than for strictly personal use, it is not permitted to download or to forward/distribute the text or part of it without the consent of the
author(s) and/or copyright holder(s), unless the work is under an open content license (like Creative Commons).
Take-down policy
If you believe that this document breaches copyright please contact us providing details, and we will remove access to the work immediately
and investigate your claim.
Downloaded from the University of Groningen/UMCG research database (Pure): http://www.rug.nl/research/portal. For technical reasons the
number of authors shown on this cover page is limited to 10 maximum.
Download date: 10-02-2018
 Thiol-disulfide Oxidoreductases in
 Bacillus subtilis
Ronald Dorenbos
 
 
  
RIJKSUNIVERSITEIT GRONINGEN 
 
 
 
 
Thiol-disulfide Oxidoreductases 
in Bacillus subtilis 
 
 
 
Proefschrift 
 
 
ter verkrijging van het doctoraat in de 
Wiskunde en Natuurwetenschappen 
aan de Rijksuniversiteit Groningen 
op gezag van 
Rector Magnificus, dr. F. Zwarts, 
in het openbaar te verdedigen op 
dinsdag 21 december 2004 
om 13.15 uur 
 
 
door 
 
 
Ronald Dorenbos 
 
 
 
geboren op 8 mei 1972 
te Winschoten 
 
 Promotores:   Prof. Dr. W.J. Quax 
    Prof. Dr. J.M. van Dijl 
 
 
 
Beoordelingscommissie:  Prof. Dr. O.P. Kuipers 
Prof. Dr. B. Oudega 
Prof. Dr. M. Sarvas 
  
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
Only those who will risk going too far 
 can possibly find out how far one can go.  
 
Thomas Stearns Eliot (1888-1965) 
 
 
 
 Paranimfen:   Joost Folgering 
 
Mattijs Julsing
  
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
Voor mijn ouders,  
 
Jaap & Wiesje Dorenbos 
 
 
  
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
This research was performed at the Department of Pharmaceutical 
Biology of the University of Groningen, the Netherlands. Funding for 
the work described in this thesis, was provided by the Commission of 
the European Union Projects BIO4-CT98-0250, QLK3-CT-1999-
00413, and QLK3-CT-1999-00917. 
 
 
Publication of this thesis has been made possible by financial support 
from the Groningen University Institute for Drug Exploration (GUIDE), 
Novozymes A/S (Denmark), and Genencor International Inc. (Palo 
Alto, California). Their contributions are greatly acknowledged. 
 
 
ISBN: 90-9018901-7 
 
 
Copyright © 2004 R. Dorenbos. All rights reserved. This book, or any 
parts thereof, may not be reproduced or transmitted by any means or in 
any form, without permission from the author. 
 
 
Cover design by Ronald Dorenbos. Electron microscopic pictures used 
for the cover, the bookmark, and the chapter heads were made by Ietse 
Stokroos. 
  
 
 
 
 
 
 
 
  
Contents 
 
1 Introduction  Thiol-disulfide Oxidoreductases ........................................ 16 
1.1 Protein production ........................................................................... 16 
1.2 Thiol-disulfide Oxidoreductases in E. coli ...................................... 19 
1.2.1 DsbA........................................................................................ 21 
1.2.2 DsbB........................................................................................ 24 
1.2.3 DsbC........................................................................................ 27 
1.2.4 DsbD........................................................................................ 29 
1.2.5 DsbE ........................................................................................ 32 
1.2.6 DsbG........................................................................................ 34 
1.2.7 Other E. coli proteins implicated in disulfide bond formation. 35 
1.3 Thiol-disulfide Oxidoreductases in B. subtilis................................. 36 
1.3.1 Bacillus subtilis........................................................................ 36 
1.3.2 The cytoplasm of B. subtilis .................................................... 37 
1.3.3 Identification of thiol-disulfide oxidoreductases in Bacillus ... 40 
1.3.4 BdbA and BdbB....................................................................... 41 
1.3.5 BdbC and BdbD....................................................................... 44 
1.3.6 Other B. subtilis proteins implicated in disulfide bond formation
 46 
1.3.7 Thiol-disulfide Oxidoreductases in Other Organisms ............. 51 
1.4 Scope of this thesis .......................................................................... 53 
2 The bdbDC operon of Bacillus subtilis encodes thiol-disulfide 
oxidoreductases required for competence development .................................. 56 
2.1 Summary.......................................................................................... 56 
2.2 Introduction ..................................................................................... 57 
2.3 Experimental Procedures ................................................................. 59 
2.4 Results ............................................................................................. 64 
2.5 Discussion........................................................................................ 78 
2.6 Acknowledgements ......................................................................... 80 
3 A specific stress response in Bacillus subtilis triggered by secretion of a 
disulfide bond-containing protein.................................................................... 82 
3.1 Summary.......................................................................................... 82 
3.2 Introduction ..................................................................................... 83 
3.3 Experimental procedures ................................................................. 85 
3.4 Results ............................................................................................. 92 
3.5 Discussion...................................................................................... 102 
3.6 Acknowledgements ....................................................................... 107 
4 Four thiol-disulfide oxidoreductases involved in swarming motility of 
Bacillus subtilis ............................................................................................. 110 
4.1 Summary........................................................................................ 110 
4.2 Introduction ................................................................................... 111 
4.3 Experimental Procedures ............................................................... 114 
4.4 Results ........................................................................................... 118 
 
 4.5 Discussion...................................................................................... 123 
4.6 Acknowledgements ....................................................................... 126 
5 Thiol-disulfide oxidoreductases are essential for the production of the 
lantibiotic sublancin 168................................................................................ 128 
5.1 Summary........................................................................................ 128 
5.2 Introduction ................................................................................... 129 
5.3 Experimental procedures ............................................................... 132 
5.4 Results ........................................................................................... 137 
5.5 Discussion...................................................................................... 144 
5.6 Acknowledgements ....................................................................... 148 
6 YolJ, a CxxS protein required for sublancin 168 production by Bacillus 
subtilis ........................................................................................................... 150 
6.1 Summary........................................................................................ 150 
6.2 Introduction ................................................................................... 151 
6.3 Experimental procedures ............................................................... 153 
6.4 Results ........................................................................................... 160 
6.5 Discussion...................................................................................... 170 
6.6 Acknowledgements ....................................................................... 174 
7 Thiol-disulfide Oxidoreductases of Bacillus subtilis ............................. 176 
7.1 Summary........................................................................................ 176 
7.2 Introduction ................................................................................... 177 
7.3 Experimental Procedures ............................................................... 179 
7.4 Results ........................................................................................... 184 
7.5 Discussion...................................................................................... 189 
7.6 Acknowledgements ....................................................................... 192 
8 Discussion & Future Perspectives ......................................................... 194 
8.1 Thiol-disulfide Oxidoreductase-like proteins of B. subtilis........... 194 
8.2 Thiol-disulfide oxidoreductases and improved production of 
heterologous proteins................................................................................. 199 
8.3 Wider application potential of thiol-disulfide oxidoreductases ..... 202 
8.4 Pathogenicity and thiol-disulfide oxidoreductases ........................ 204 
8.5 Concluding Remarks ..................................................................... 207 
9 Reference List........................................................................................ 210 
10 Summary & Samenvatting................................................................. 234 
10.1 Summary........................................................................................ 234 
10.2 Samenvatting ................................................................................. 238 
11 Dankwoord ........................................................................................ 244 
12 Curriculum Vitae & Publications ...................................................... 254 
12.1 Curriculum Vitae ........................................................................... 254 
12.2 Publications ................................................................................... 255 
 
  
 
 
  
 
 
 
 


NARCIS 

   University of GroningenThiol-disulfide oxidoreductases in Bacillus subtilisDorenbos, RonaldIMPORTANT NOTE: You are advised to consult the publisher's version (publisher's PDF) if you wish to cite fromit. Please check the document version below.Document VersionPublisher's PDF, also known as Version of recordPublication date:2004Link to publication in University of Groningen/UMCG research databaseCitation for published version (APA):Dorenbos, R. (2004). Thiol-disulfide oxidoreductases in Bacillus subtilis. s.n.CopyrightOther than for strictly personal use, it is not permitted to download or to forward/distribute the text or part of it without the consent of theauthor(s) and/or copyright holder(s), unless the work is under an open content license (like Creative Commons).The publication may also be distributed here under the terms of Article 25fa of the Dutch Copyright Act, indicated by the “Taverne” license.More information can be found on the University of Groningen website: https://www.rug.nl/library/open-access/self-archiving-pure/taverne-amendment.Take-down policyIf you believe that this document breaches copyright please contact us providing details, and we will remove access to the work immediatelyand investigate your claim.Downloaded from the University of Groningen/UMCG research database (Pure): http://www.rug.nl/research/portal. For technical reasons thenumber of authors shown on this cover page is limited to 10 maximum.Download date: 06-06-2022 Thiol-disulfide Oxidoreductases in Bacillus subtilisRonald Dorenbos    RIJKSUNIVERSITEIT GRONINGEN     Thiol-disulfide Oxidoreductases in Bacillus subtilis    Proefschrift   ter verkrijging van het doctoraat in de Wiskunde en Natuurwetenschappen aan de Rijksuniversiteit Groningen op gezag van Rector Magnificus, dr. F. Zwarts, in het openbaar te verdedigen op dinsdag 21 december 2004 om 13.15 uur   door   Ronald Dorenbos    geboren op 8 mei 1972 te Winschoten   Promotores:   Prof. Dr. W.J. Quax     Prof. Dr. J.M. van Dijl    Beoordelingscommissie:  Prof. Dr. O.P. Kuipers Prof. Dr. B. Oudega Prof. Dr. M. Sarvas                                 Only those who will risk going too far  can possibly find out how far one can go.   Thomas Stearns Eliot (1888-1965)     Paranimfen:   Joost Folgering  Mattijs Julsing                               Voor mijn ouders,   Jaap & Wiesje Dorenbos                    This research was performed at the Department of Pharmaceutical Biology of the University of Groningen, the Netherlands. Funding for the work described in this thesis, was provided by the Commission of the European Union Projects BIO4-CT98-0250, QLK3-CT-1999-00413, and QLK3-CT-1999-00917.   Publication of this thesis has been made possible by financial support from the Groningen University Institute for Drug Exploration (GUIDE), Novozymes A/S (Denmark), and Genencor International Inc. (Palo Alto, California). Their contributions are greatly acknowledged.   ISBN: 90-9018901-7   Copyright © 2004 R. Dorenbos. All rights reserved. This book, or any parts thereof, may not be reproduced or transmitted by any means or in any form, without permission from the author.   Cover design by Ronald Dorenbos. Electron microscopic pictures used for the cover, the bookmark, and the chapter heads were made by Ietse Stokroos.            Contents  1 Introduction  Thiol-disulfide Oxidoreductases ........................................ 16 1.1 Protein production ........................................................................... 16 1.2 Thiol-disulfide Oxidoreductases in E. coli ...................................... 19 1.2.1 DsbA........................................................................................ 21 1.2.2 DsbB........................................................................................ 24 1.2.3 DsbC........................................................................................ 27 1.2.4 DsbD........................................................................................ 29 1.2.5 DsbE ........................................................................................ 32 1.2.6 DsbG........................................................................................ 34 1.2.7 Other E. coli proteins implicated in disulfide bond formation. 35 1.3 Thiol-disulfide Oxidoreductases in B. subtilis................................. 36 1.3.1 Bacillus subtilis........................................................................ 36 1.3.2 The cytoplasm of B. subtilis .................................................... 37 1.3.3 Identification of thiol-disulfide oxidoreductases in Bacillus ... 40 1.3.4 BdbA and BdbB....................................................................... 41 1.3.5 BdbC and BdbD....................................................................... 44 1.3.6 Other B. subtilis proteins implicated in disulfide bond formation 46 1.3.7 Thiol-disulfide Oxidoreductases in Other Organisms ............. 51 1.4 Scope of this thesis .......................................................................... 53 2 The bdbDC operon of Bacillus subtilis encodes thiol-disulfide oxidoreductases required for competence development .................................. 56 2.1 Summary.......................................................................................... 56 2.2 Introduction ..................................................................................... 57 2.3 Experimental Procedures ................................................................. 59 2.4 Results ............................................................................................. 64 2.5 Discussion........................................................................................ 78 2.6 Acknowledgements ......................................................................... 80 3 A specific stress response in Bacillus subtilis triggered by secretion of a disulfide bond-containing protein.................................................................... 82 3.1 Summary.......................................................................................... 82 3.2 Introduction ..................................................................................... 83 3.3 Experimental procedures ................................................................. 85 3.4 Results ............................................................................................. 92 3.5 Discussion...................................................................................... 102 3.6 Acknowledgements ....................................................................... 107 4 Four thiol-disulfide oxidoreductases involved in swarming motility of Bacillus subtilis ............................................................................................. 110 4.1 Summary........................................................................................ 110 4.2 Introduction ................................................................................... 111 4.3 Experimental Procedures ............................................................... 114 4.4 Results ........................................................................................... 118   4.5 Discussion...................................................................................... 123 4.6 Acknowledgements ....................................................................... 126 5 Thiol-disulfide oxidoreductases are essential for the production of the lantibiotic sublancin 168................................................................................ 128 5.1 Summary........................................................................................ 128 5.2 Introduction ................................................................................... 129 5.3 Experimental procedures ............................................................... 132 5.4 Results ........................................................................................... 137 5.5 Discussion...................................................................................... 144 5.6 Acknowledgements ....................................................................... 148 6 YolJ, a CxxS protein required for sublancin 168 production by Bacillus subtilis ........................................................................................................... 150 6.1 Summary........................................................................................ 150 6.2 Introduction ................................................................................... 151 6.3 Experimental procedures ............................................................... 153 6.4 Results ........................................................................................... 160 6.5 Discussion...................................................................................... 170 6.6 Acknowledgements ....................................................................... 174 7 Thiol-disulfide Oxidoreductases of Bacillus subtilis ............................. 176 7.1 Summary........................................................................................ 176 7.2 Introduction ................................................................................... 177 7.3 Experimental Procedures ............................................................... 179 7.4 Results ........................................................................................... 184 7.5 Discussion...................................................................................... 189 7.6 Acknowledgements ....................................................................... 192 8 Discussion & Future Perspectives ......................................................... 194 8.1 Thiol-disulfide Oxidoreductase-like proteins of B. subtilis........... 194 8.2 Thiol-disulfide oxidoreductases and improved production of heterologous proteins................................................................................. 199 8.3 Wider application potential of thiol-disulfide oxidoreductases ..... 202 8.4 Pathogenicity and thiol-disulfide oxidoreductases ........................ 204 8.5 Concluding Remarks ..................................................................... 207 9 Reference List........................................................................................ 210 10 Summary & Samenvatting................................................................. 234 10.1 Summary........................................................................................ 234 10.2 Samenvatting ................................................................................. 238 11 Dankwoord ........................................................................................ 244 12 Curriculum Vitae & Publications ...................................................... 254 12.1 Curriculum Vitae ........................................................................... 254 12.2 Publications ................................................................................... 255            

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Thiol-disulfide oxidoreductases in Bacillus subtilis

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