Allantoin catabolism influences the production of antibiotics in Streptomyces coelicolor

Autores
Navone, Laura; Casati, Paula; Licona Cassani, Cuauhtémoc; Marcellin, Esteban; Nielsen, Lars K.; Rodriguez, Eduardo Jose; Gramajo, Hugo Cesar
Año de publicación
2014
Idioma
inglés
Tipo de recurso
artículo
Estado
versión publicada
Descripción
Purines are a primary source of carbon and nitrogen in soil; however, their metabolism is poorly understood in Streptomyces. Using a combination of proteomics, metabolomics, and metabolic engineering, we characterized the allantoin pathway in Streptomyces coelicolor. When cells grew in glucose minimal medium with allantoin as the sole nitrogen source, quantitative proteomics identified 38 enzymes upregulated and 28 downregulated. This allowed identifying six new functional enzymes involved in allantoin metabolism in S. coelicolor. From those, using a combination of biochemical and genetic engineering tools, it was found that allantoinase (EC 3.5.2.5) and allantoicase (EC 3.5.3.4) are essential for allantoin metabolism in S. coelicolor. Metabolomics showed that under these growth conditions, there is a significant intracellular accumulation of urea and amino acids, which eventually results in urea and ammonium release into the culture medium. Antibiotic production of a urease mutant strain showed that the catabolism of allantoin, and the subsequent release of ammonium, inhibits antibiotic production. These observations link the antibiotic production impairment with an imbalance in nitrogen metabolism and provide the first evidence of an interaction between purine metabolism and antibiotic biosynthesis.
Fil: Navone, Laura. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Rosario. Instituto de Biología Molecular y Celular de Rosario; Argentina
Fil: Casati, Paula. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Rosario. Centro de Estudios Fotosintéticos y Bioquímicos (i); Argentina
Fil: Licona Cassani, Cuauhtémoc. University Of Queensland; Australia
Fil: Marcellin, Esteban. University Of Queensland; Australia
Fil: Nielsen, Lars K.. University Of Queensland; Australia
Fil: Rodriguez, Eduardo Jose. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Rosario. Instituto de Biología Molecular y Celular de Rosario; Argentina
Fil: Gramajo, Hugo Cesar. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Rosario. Instituto de Biología Molecular y Celular de Rosario; Argentina
Materia
Allantoina
Streptomyces Coelicolor
Catabolismo
Antibióticos
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:11336/7859
Acceder
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network_name_str CONICET Digital (CONICET)
spelling Allantoin catabolism influences the production of antibiotics in Streptomyces coelicolorNavone, LauraCasati, PaulaLicona Cassani, CuauhtémocMarcellin, EstebanNielsen, Lars K.Rodriguez, Eduardo JoseGramajo, Hugo CesarAllantoinaStreptomyces CoelicolorCatabolismoAntibióticoshttps://purl.org/becyt/ford/1.6https://purl.org/becyt/ford/1Purines are a primary source of carbon and nitrogen in soil; however, their metabolism is poorly understood in Streptomyces. Using a combination of proteomics, metabolomics, and metabolic engineering, we characterized the allantoin pathway in Streptomyces coelicolor. When cells grew in glucose minimal medium with allantoin as the sole nitrogen source, quantitative proteomics identified 38 enzymes upregulated and 28 downregulated. This allowed identifying six new functional enzymes involved in allantoin metabolism in S. coelicolor. From those, using a combination of biochemical and genetic engineering tools, it was found that allantoinase (EC 3.5.2.5) and allantoicase (EC 3.5.3.4) are essential for allantoin metabolism in S. coelicolor. Metabolomics showed that under these growth conditions, there is a significant intracellular accumulation of urea and amino acids, which eventually results in urea and ammonium release into the culture medium. Antibiotic production of a urease mutant strain showed that the catabolism of allantoin, and the subsequent release of ammonium, inhibits antibiotic production. These observations link the antibiotic production impairment with an imbalance in nitrogen metabolism and provide the first evidence of an interaction between purine metabolism and antibiotic biosynthesis.Fil: Navone, Laura. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Rosario. Instituto de Biología Molecular y Celular de Rosario; ArgentinaFil: Casati, Paula. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Rosario. Centro de Estudios Fotosintéticos y Bioquímicos (i); ArgentinaFil: Licona Cassani, Cuauhtémoc. University Of Queensland; AustraliaFil: Marcellin, Esteban. University Of Queensland; AustraliaFil: Nielsen, Lars K.. University Of Queensland; AustraliaFil: Rodriguez, Eduardo Jose. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Rosario. Instituto de Biología Molecular y Celular de Rosario; ArgentinaFil: Gramajo, Hugo Cesar. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Rosario. Instituto de Biología Molecular y Celular de Rosario; ArgentinaSpringer2014-01info:eu-repo/semantics/articleinfo:eu-repo/semantics/publishedVersionhttp://purl.org/coar/resource_type/c_6501info:ar-repo/semantics/articuloapplication/pdfapplication/pdfapplication/pdfapplication/pdfhttp://hdl.handle.net/11336/7859Navone, Laura; Casati, Paula; Licona Cassani, Cuauhtémoc; Marcellin, Esteban; Nielsen, Lars K.; et al.; Allantoin catabolism influences the production of antibiotics in Streptomyces coelicolor; Springer; Applied Microbiology and Biotechnology; 98; 1; 1-2014; 351-3601432-0614enginfo:eu-repo/semantics/altIdentifier/url/http://link.springer.com/article/10.1007%2Fs00253-013-5372-1info:eu-repo/semantics/altIdentifier/doi/10.1007/s00253-013-5372-1info:eu-repo/semantics/openAccesshttps://creativecommons.org/licenses/by-nc-sa/2.5/ar/reponame:CONICET Digital (CONICET)instname:Consejo Nacional de Investigaciones Científicas y Técnicas2025-10-22T12:09:56Zoai:ri.conicet.gov.ar:11336/7859instacron: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:34982025-10-22 12:09:57.074CONICET Digital (CONICET) - Consejo Nacional de Investigaciones Científicas y Técnicasfalse
dc.title.none.fl_str_mv Allantoin catabolism influences the production of antibiotics in Streptomyces coelicolor
title Allantoin catabolism influences the production of antibiotics in Streptomyces coelicolor
spellingShingle Allantoin catabolism influences the production of antibiotics in Streptomyces coelicolor
Navone, Laura
Allantoina
Streptomyces Coelicolor
Catabolismo
Antibióticos
title_short Allantoin catabolism influences the production of antibiotics in Streptomyces coelicolor
title_full Allantoin catabolism influences the production of antibiotics in Streptomyces coelicolor
title_fullStr Allantoin catabolism influences the production of antibiotics in Streptomyces coelicolor
title_full_unstemmed Allantoin catabolism influences the production of antibiotics in Streptomyces coelicolor
title_sort Allantoin catabolism influences the production of antibiotics in Streptomyces coelicolor
dc.creator.none.fl_str_mv Navone, Laura
Casati, Paula
Licona Cassani, Cuauhtémoc
Marcellin, Esteban
Nielsen, Lars K.
Rodriguez, Eduardo Jose
Gramajo, Hugo Cesar
author Navone, Laura
author_facet Navone, Laura
Casati, Paula
Licona Cassani, Cuauhtémoc
Marcellin, Esteban
Nielsen, Lars K.
Rodriguez, Eduardo Jose
Gramajo, Hugo Cesar
author_role author
author2 Casati, Paula
Licona Cassani, Cuauhtémoc
Marcellin, Esteban
Nielsen, Lars K.
Rodriguez, Eduardo Jose
Gramajo, Hugo Cesar
author2_role author
author
author
author
author
author
dc.subject.none.fl_str_mv Allantoina
Streptomyces Coelicolor
Catabolismo
Antibióticos
topic Allantoina
Streptomyces Coelicolor
Catabolismo
Antibióticos
purl_subject.fl_str_mv https://purl.org/becyt/ford/1.6
https://purl.org/becyt/ford/1
dc.description.none.fl_txt_mv Purines are a primary source of carbon and nitrogen in soil; however, their metabolism is poorly understood in Streptomyces. Using a combination of proteomics, metabolomics, and metabolic engineering, we characterized the allantoin pathway in Streptomyces coelicolor. When cells grew in glucose minimal medium with allantoin as the sole nitrogen source, quantitative proteomics identified 38 enzymes upregulated and 28 downregulated. This allowed identifying six new functional enzymes involved in allantoin metabolism in S. coelicolor. From those, using a combination of biochemical and genetic engineering tools, it was found that allantoinase (EC 3.5.2.5) and allantoicase (EC 3.5.3.4) are essential for allantoin metabolism in S. coelicolor. Metabolomics showed that under these growth conditions, there is a significant intracellular accumulation of urea and amino acids, which eventually results in urea and ammonium release into the culture medium. Antibiotic production of a urease mutant strain showed that the catabolism of allantoin, and the subsequent release of ammonium, inhibits antibiotic production. These observations link the antibiotic production impairment with an imbalance in nitrogen metabolism and provide the first evidence of an interaction between purine metabolism and antibiotic biosynthesis.
Fil: Navone, Laura. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Rosario. Instituto de Biología Molecular y Celular de Rosario; Argentina
Fil: Casati, Paula. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Rosario. Centro de Estudios Fotosintéticos y Bioquímicos (i); Argentina
Fil: Licona Cassani, Cuauhtémoc. University Of Queensland; Australia
Fil: Marcellin, Esteban. University Of Queensland; Australia
Fil: Nielsen, Lars K.. University Of Queensland; Australia
Fil: Rodriguez, Eduardo Jose. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Rosario. Instituto de Biología Molecular y Celular de Rosario; Argentina
Fil: Gramajo, Hugo Cesar. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Rosario. Instituto de Biología Molecular y Celular de Rosario; Argentina
description Purines are a primary source of carbon and nitrogen in soil; however, their metabolism is poorly understood in Streptomyces. Using a combination of proteomics, metabolomics, and metabolic engineering, we characterized the allantoin pathway in Streptomyces coelicolor. When cells grew in glucose minimal medium with allantoin as the sole nitrogen source, quantitative proteomics identified 38 enzymes upregulated and 28 downregulated. This allowed identifying six new functional enzymes involved in allantoin metabolism in S. coelicolor. From those, using a combination of biochemical and genetic engineering tools, it was found that allantoinase (EC 3.5.2.5) and allantoicase (EC 3.5.3.4) are essential for allantoin metabolism in S. coelicolor. Metabolomics showed that under these growth conditions, there is a significant intracellular accumulation of urea and amino acids, which eventually results in urea and ammonium release into the culture medium. Antibiotic production of a urease mutant strain showed that the catabolism of allantoin, and the subsequent release of ammonium, inhibits antibiotic production. These observations link the antibiotic production impairment with an imbalance in nitrogen metabolism and provide the first evidence of an interaction between purine metabolism and antibiotic biosynthesis.
publishDate 2014
dc.date.none.fl_str_mv 2014-01
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/11336/7859
Navone, Laura; Casati, Paula; Licona Cassani, Cuauhtémoc; Marcellin, Esteban; Nielsen, Lars K.; et al.; Allantoin catabolism influences the production of antibiotics in Streptomyces coelicolor; Springer; Applied Microbiology and Biotechnology; 98; 1; 1-2014; 351-360
1432-0614
url http://hdl.handle.net/11336/7859
identifier_str_mv Navone, Laura; Casati, Paula; Licona Cassani, Cuauhtémoc; Marcellin, Esteban; Nielsen, Lars K.; et al.; Allantoin catabolism influences the production of antibiotics in Streptomyces coelicolor; Springer; Applied Microbiology and Biotechnology; 98; 1; 1-2014; 351-360
1432-0614
dc.language.none.fl_str_mv eng
language eng
dc.relation.none.fl_str_mv info:eu-repo/semantics/altIdentifier/url/http://link.springer.com/article/10.1007%2Fs00253-013-5372-1
info:eu-repo/semantics/altIdentifier/doi/10.1007/s00253-013-5372-1
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
application/pdf
dc.publisher.none.fl_str_mv Springer
publisher.none.fl_str_mv Springer
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 12.982451

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