The production and utilization of GDP-glucose in the biosynthesis of trehalose-6-phosphate by Streptomyces venezuelae

Autores
Asención Diez, Matías Damián; Miah, Farzana; Stevenson, Clare E. M.; Lawson, David M.; Iglesias, Alberto Alvaro; Bornemann, Stephen
Año de publicación
2017
Idioma
inglés
Tipo de recurso
artículo
Estado
versión publicada
Descripción
Trehalose-6-phosphate synthase OtsA from streptomycetes is unusual in that it uses GDP-glucose as the donor substrate rather than the more commonly used UDP-glucose. We now confirm that OtsA from Streptomyces venezuelae has such a preference for GDP-glucose and can utilize ADP-glucose to some extent too. A crystal structure of the enzyme shows that it shares twin Rossmann-like domains with the UDP-glucose-specific OtsA from Escherichia coli. However, it is structurally more similar to Streptomyces hygroscopicus VldE, a GDP-valienol-dependent pseudoglycosyltransferase enzyme. Comparison of the donor binding sites reveals that the amino acids associated with the binding of diphosphoribose are almost all identical in these three enzymes. By contrast, the amino acids associated with binding guanine in VldE (Asn, Thr, and Val) are similar in S. venezuelae OtsA (Asp, Ser, and Phe, respectively) but not conserved in E. coli OtsA (His, Leu, and Asp, respectively), providing a rationale for the purine base specificity of S. venezuelae OtsA. To establish which donor is used in vivo, we generated an otsA null mutant in S. venezuelae. The mutant had a cell density-dependent growth phenotype and accumulated galactose 1-phosphate, glucose 1-phosphate, and GDP-glucose when grown on galactose. To determine how the GDP-glucose is generated, we characterized three candidate GDP-glucose pyrophosphorylases. SVEN_3027 is a UDP-glucose pyrophosphorylase, SVEN_3972 is an unusual ITP-mannose pyrophosphorylase, and SVEN_2781 is a pyrophosphorylase that is capable of generating GDP-glucose as well as GDP-mannose. We have therefore established how S. venezuelae can make and utilize GDP-glucose in the biosynthesis of trehalose 6-phosphate.
Fil: Asención Diez, Matías Damián. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Santa Fe. Instituto de Agrobiotecnología del Litoral. Universidad Nacional del Litoral. Instituto de Agrobiotecnología del Litoral; Argentina
Fil: Miah, Farzana. John Innes Institute; Reino Unido
Fil: Stevenson, Clare E. M.. John Innes Institute; Reino Unido
Fil: Lawson, David M.. John Innes Institute; Reino Unido
Fil: Iglesias, Alberto Alvaro. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Santa Fe. Instituto de Agrobiotecnología del Litoral. Universidad Nacional del Litoral. Instituto de Agrobiotecnología del Litoral; Argentina
Fil: Bornemann, Stephen. John Innes Institute; Reino Unido
Materia
Trehalose-6p
Actinobacteria
Glucosyltransferase
Gdp-Glucose
Nivel de accesibilidad
acceso abierto
Condiciones de uso
https://creativecommons.org/licenses/by-nc-sa/2.5/ar/
Repositorio
CONICET Digital (CONICET)
Institución
Consejo Nacional de Investigaciones Científicas y Técnicas
OAI Identificador
oai:ri.conicet.gov.ar:11336/45674
Acceder
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oai_identifier_str oai:ri.conicet.gov.ar:11336/45674
network_acronym_str CONICETDig
repository_id_str 3498
network_name_str CONICET Digital (CONICET)
spelling The production and utilization of GDP-glucose in the biosynthesis of trehalose-6-phosphate by Streptomyces venezuelaeAsención Diez, Matías DamiánMiah, FarzanaStevenson, Clare E. M.Lawson, David M.Iglesias, Alberto AlvaroBornemann, StephenTrehalose-6pActinobacteriaGlucosyltransferaseGdp-Glucosehttps://purl.org/becyt/ford/1.6https://purl.org/becyt/ford/1Trehalose-6-phosphate synthase OtsA from streptomycetes is unusual in that it uses GDP-glucose as the donor substrate rather than the more commonly used UDP-glucose. We now confirm that OtsA from Streptomyces venezuelae has such a preference for GDP-glucose and can utilize ADP-glucose to some extent too. A crystal structure of the enzyme shows that it shares twin Rossmann-like domains with the UDP-glucose-specific OtsA from Escherichia coli. However, it is structurally more similar to Streptomyces hygroscopicus VldE, a GDP-valienol-dependent pseudoglycosyltransferase enzyme. Comparison of the donor binding sites reveals that the amino acids associated with the binding of diphosphoribose are almost all identical in these three enzymes. By contrast, the amino acids associated with binding guanine in VldE (Asn, Thr, and Val) are similar in S. venezuelae OtsA (Asp, Ser, and Phe, respectively) but not conserved in E. coli OtsA (His, Leu, and Asp, respectively), providing a rationale for the purine base specificity of S. venezuelae OtsA. To establish which donor is used in vivo, we generated an otsA null mutant in S. venezuelae. The mutant had a cell density-dependent growth phenotype and accumulated galactose 1-phosphate, glucose 1-phosphate, and GDP-glucose when grown on galactose. To determine how the GDP-glucose is generated, we characterized three candidate GDP-glucose pyrophosphorylases. SVEN_3027 is a UDP-glucose pyrophosphorylase, SVEN_3972 is an unusual ITP-mannose pyrophosphorylase, and SVEN_2781 is a pyrophosphorylase that is capable of generating GDP-glucose as well as GDP-mannose. We have therefore established how S. venezuelae can make and utilize GDP-glucose in the biosynthesis of trehalose 6-phosphate.Fil: Asención Diez, Matías Damián. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Santa Fe. Instituto de Agrobiotecnología del Litoral. Universidad Nacional del Litoral. Instituto de Agrobiotecnología del Litoral; ArgentinaFil: Miah, Farzana. John Innes Institute; Reino UnidoFil: Stevenson, Clare E. M.. John Innes Institute; Reino UnidoFil: Lawson, David M.. John Innes Institute; Reino UnidoFil: Iglesias, Alberto Alvaro. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Santa Fe. Instituto de Agrobiotecnología del Litoral. Universidad Nacional del Litoral. Instituto de Agrobiotecnología del Litoral; ArgentinaFil: Bornemann, Stephen. John Innes Institute; Reino UnidoAmerican Society for Biochemistry and Molecular Biology2017-01info:eu-repo/semantics/articleinfo:eu-repo/semantics/publishedVersionhttp://purl.org/coar/resource_type/c_6501info:ar-repo/semantics/articuloapplication/pdfapplication/pdfapplication/pdfhttp://hdl.handle.net/11336/45674Asención Diez, Matías Damián; Miah, Farzana; Stevenson, Clare E. M.; Lawson, David M.; Iglesias, Alberto Alvaro; et al.; The production and utilization of GDP-glucose in the biosynthesis of trehalose-6-phosphate by Streptomyces venezuelae; American Society for Biochemistry and Molecular Biology; Journal of Biological Chemistry (online); 292; 1-2017; 945-9540021-9258CONICET DigitalCONICETenginfo:eu-repo/semantics/altIdentifier/url/http://www.jbc.org/content/292/3/945info:eu-repo/semantics/altIdentifier/doi/10.1074/jbc.M116.758664info:eu-repo/semantics/openAccesshttps://creativecommons.org/licenses/by-nc-sa/2.5/ar/reponame:CONICET Digital (CONICET)instname:Consejo Nacional de Investigaciones Científicas y Técnicas2025-10-15T15:37:56Zoai:ri.conicet.gov.ar:11336/45674instacron:CONICETInstitucionalhttp://ri.conicet.gov.ar/Organismo científico-tecnológicoNo correspondehttp://ri.conicet.gov.ar/oai/requestdasensio@conicet.gov.ar; lcarlino@conicet.gov.arArgentinaNo correspondeNo correspondeNo correspondeopendoar:34982025-10-15 15:37:57.224CONICET Digital (CONICET) - Consejo Nacional de Investigaciones Científicas y Técnicasfalse
dc.title.none.fl_str_mv The production and utilization of GDP-glucose in the biosynthesis of trehalose-6-phosphate by Streptomyces venezuelae
title The production and utilization of GDP-glucose in the biosynthesis of trehalose-6-phosphate by Streptomyces venezuelae
spellingShingle The production and utilization of GDP-glucose in the biosynthesis of trehalose-6-phosphate by Streptomyces venezuelae
Asención Diez, Matías Damián
Trehalose-6p
Actinobacteria
Glucosyltransferase
Gdp-Glucose
title_short The production and utilization of GDP-glucose in the biosynthesis of trehalose-6-phosphate by Streptomyces venezuelae
title_full The production and utilization of GDP-glucose in the biosynthesis of trehalose-6-phosphate by Streptomyces venezuelae
title_fullStr The production and utilization of GDP-glucose in the biosynthesis of trehalose-6-phosphate by Streptomyces venezuelae
title_full_unstemmed The production and utilization of GDP-glucose in the biosynthesis of trehalose-6-phosphate by Streptomyces venezuelae
title_sort The production and utilization of GDP-glucose in the biosynthesis of trehalose-6-phosphate by Streptomyces venezuelae
dc.creator.none.fl_str_mv Asención Diez, Matías Damián
Miah, Farzana
Stevenson, Clare E. M.
Lawson, David M.
Iglesias, Alberto Alvaro
Bornemann, Stephen
author Asención Diez, Matías Damián
author_facet Asención Diez, Matías Damián
Miah, Farzana
Stevenson, Clare E. M.
Lawson, David M.
Iglesias, Alberto Alvaro
Bornemann, Stephen
author_role author
author2 Miah, Farzana
Stevenson, Clare E. M.
Lawson, David M.
Iglesias, Alberto Alvaro
Bornemann, Stephen
author2_role author
author
author
author
author
dc.subject.none.fl_str_mv Trehalose-6p
Actinobacteria
Glucosyltransferase
Gdp-Glucose
topic Trehalose-6p
Actinobacteria
Glucosyltransferase
Gdp-Glucose
purl_subject.fl_str_mv https://purl.org/becyt/ford/1.6
https://purl.org/becyt/ford/1
dc.description.none.fl_txt_mv Trehalose-6-phosphate synthase OtsA from streptomycetes is unusual in that it uses GDP-glucose as the donor substrate rather than the more commonly used UDP-glucose. We now confirm that OtsA from Streptomyces venezuelae has such a preference for GDP-glucose and can utilize ADP-glucose to some extent too. A crystal structure of the enzyme shows that it shares twin Rossmann-like domains with the UDP-glucose-specific OtsA from Escherichia coli. However, it is structurally more similar to Streptomyces hygroscopicus VldE, a GDP-valienol-dependent pseudoglycosyltransferase enzyme. Comparison of the donor binding sites reveals that the amino acids associated with the binding of diphosphoribose are almost all identical in these three enzymes. By contrast, the amino acids associated with binding guanine in VldE (Asn, Thr, and Val) are similar in S. venezuelae OtsA (Asp, Ser, and Phe, respectively) but not conserved in E. coli OtsA (His, Leu, and Asp, respectively), providing a rationale for the purine base specificity of S. venezuelae OtsA. To establish which donor is used in vivo, we generated an otsA null mutant in S. venezuelae. The mutant had a cell density-dependent growth phenotype and accumulated galactose 1-phosphate, glucose 1-phosphate, and GDP-glucose when grown on galactose. To determine how the GDP-glucose is generated, we characterized three candidate GDP-glucose pyrophosphorylases. SVEN_3027 is a UDP-glucose pyrophosphorylase, SVEN_3972 is an unusual ITP-mannose pyrophosphorylase, and SVEN_2781 is a pyrophosphorylase that is capable of generating GDP-glucose as well as GDP-mannose. We have therefore established how S. venezuelae can make and utilize GDP-glucose in the biosynthesis of trehalose 6-phosphate.
Fil: Asención Diez, Matías Damián. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Santa Fe. Instituto de Agrobiotecnología del Litoral. Universidad Nacional del Litoral. Instituto de Agrobiotecnología del Litoral; Argentina
Fil: Miah, Farzana. John Innes Institute; Reino Unido
Fil: Stevenson, Clare E. M.. John Innes Institute; Reino Unido
Fil: Lawson, David M.. John Innes Institute; Reino Unido
Fil: Iglesias, Alberto Alvaro. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Santa Fe. Instituto de Agrobiotecnología del Litoral. Universidad Nacional del Litoral. Instituto de Agrobiotecnología del Litoral; Argentina
Fil: Bornemann, Stephen. John Innes Institute; Reino Unido
description Trehalose-6-phosphate synthase OtsA from streptomycetes is unusual in that it uses GDP-glucose as the donor substrate rather than the more commonly used UDP-glucose. We now confirm that OtsA from Streptomyces venezuelae has such a preference for GDP-glucose and can utilize ADP-glucose to some extent too. A crystal structure of the enzyme shows that it shares twin Rossmann-like domains with the UDP-glucose-specific OtsA from Escherichia coli. However, it is structurally more similar to Streptomyces hygroscopicus VldE, a GDP-valienol-dependent pseudoglycosyltransferase enzyme. Comparison of the donor binding sites reveals that the amino acids associated with the binding of diphosphoribose are almost all identical in these three enzymes. By contrast, the amino acids associated with binding guanine in VldE (Asn, Thr, and Val) are similar in S. venezuelae OtsA (Asp, Ser, and Phe, respectively) but not conserved in E. coli OtsA (His, Leu, and Asp, respectively), providing a rationale for the purine base specificity of S. venezuelae OtsA. To establish which donor is used in vivo, we generated an otsA null mutant in S. venezuelae. The mutant had a cell density-dependent growth phenotype and accumulated galactose 1-phosphate, glucose 1-phosphate, and GDP-glucose when grown on galactose. To determine how the GDP-glucose is generated, we characterized three candidate GDP-glucose pyrophosphorylases. SVEN_3027 is a UDP-glucose pyrophosphorylase, SVEN_3972 is an unusual ITP-mannose pyrophosphorylase, and SVEN_2781 is a pyrophosphorylase that is capable of generating GDP-glucose as well as GDP-mannose. We have therefore established how S. venezuelae can make and utilize GDP-glucose in the biosynthesis of trehalose 6-phosphate.
publishDate 2017
dc.date.none.fl_str_mv 2017-01
dc.type.none.fl_str_mv info:eu-repo/semantics/article
info:eu-repo/semantics/publishedVersion
http://purl.org/coar/resource_type/c_6501
info:ar-repo/semantics/articulo
format article
status_str publishedVersion
dc.identifier.none.fl_str_mv http://hdl.handle.net/11336/45674
Asención Diez, Matías Damián; Miah, Farzana; Stevenson, Clare E. M.; Lawson, David M.; Iglesias, Alberto Alvaro; et al.; The production and utilization of GDP-glucose in the biosynthesis of trehalose-6-phosphate by Streptomyces venezuelae; American Society for Biochemistry and Molecular Biology; Journal of Biological Chemistry (online); 292; 1-2017; 945-954
0021-9258
CONICET Digital
CONICET
url http://hdl.handle.net/11336/45674
identifier_str_mv Asención Diez, Matías Damián; Miah, Farzana; Stevenson, Clare E. M.; Lawson, David M.; Iglesias, Alberto Alvaro; et al.; The production and utilization of GDP-glucose in the biosynthesis of trehalose-6-phosphate by Streptomyces venezuelae; American Society for Biochemistry and Molecular Biology; Journal of Biological Chemistry (online); 292; 1-2017; 945-954
0021-9258
CONICET Digital
CONICET
dc.language.none.fl_str_mv eng
language eng
dc.relation.none.fl_str_mv info:eu-repo/semantics/altIdentifier/url/http://www.jbc.org/content/292/3/945
info:eu-repo/semantics/altIdentifier/doi/10.1074/jbc.M116.758664
dc.rights.none.fl_str_mv info:eu-repo/semantics/openAccess
https://creativecommons.org/licenses/by-nc-sa/2.5/ar/
eu_rights_str_mv openAccess
rights_invalid_str_mv https://creativecommons.org/licenses/by-nc-sa/2.5/ar/
dc.format.none.fl_str_mv application/pdf
application/pdf
application/pdf
dc.publisher.none.fl_str_mv American Society for Biochemistry and Molecular Biology
publisher.none.fl_str_mv American Society for Biochemistry and Molecular Biology
dc.source.none.fl_str_mv reponame:CONICET Digital (CONICET)
instname:Consejo Nacional de Investigaciones Científicas y Técnicas
reponame_str CONICET Digital (CONICET)
collection CONICET Digital (CONICET)
instname_str Consejo Nacional de Investigaciones Científicas y Técnicas
repository.name.fl_str_mv CONICET Digital (CONICET) - Consejo Nacional de Investigaciones Científicas y Técnicas
repository.mail.fl_str_mv dasensio@conicet.gov.ar; lcarlino@conicet.gov.ar
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score 13.221938

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