Glucose Oxidation to Pyruvate Is Not Essential for Brucella suis Biovar 5 Virulence in the Mouse Model

Brucella species cause brucellosis, a worldwide extended zoonosis. The brucellae are related to free-living and plant-associated α2-Proteobacteria and, since they multiply within host cells, their metabolism probably reflects this adaptation. To investigate this, we used the rodent-associated Brucel...

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Autores: Lázaro-Antón, L. (Leticia)|||/items/914740d0-4db1-482f-81fa-bbff2cada166, de-Miguel, M.J. (María Jesús)|||/items/cfc74851-e6d4-4126-a8f6-71e55b7e72f7, Barbier, T. (Thibault)|||/items/b67b44cc-f10c-4bfc-bd12-d5992a13e810, Conde-Álvarez, R. (Raquel)|||/items/7a805559-3962-434b-9df9-ec243d61b5aa, Muñoz, P. (Pilar)|||/items/4e98f4c8-d3e4-4fb3-b781-07a0bcb652bc, Letesson, J.J. (Jean Jacques)|||/items/310147b5-d631-4025-ad82-d3e696cc9a4c, Iriarte-Cilveti, M. (Maite)|||/items/5b20b123-3967-4f07-b577-13d13aa57363, Moriyon, I. (Ignacio)|||/items/834b4ce9-a879-4ba7-8884-39d0ddd88c7b, Zuñiga-Ripa, A. (Amaia)|||/items/9aa6da2e-e507-4319-a12c-092436f70feb
Tipo de documento: artigo
Data de publicação:2021
País:España
Recursos:Universidad de Navarra
Repositório:Dadun. Depósito Académico Digital de la Universidad de Navarra
Idioma:inglês
OAI Identifier:oai:dadun.unav.edu:10171/69677
Acesso em linha:https://hdl.handle.net/10171/69677
Access Level:Acceso aberto
Palavra-chave:Brucella
Metabolism
Glucose
Entner-Doudoroff
Virulence
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spelling Glucose Oxidation to Pyruvate Is Not Essential for Brucella suis Biovar 5 Virulence in the Mouse ModelLázaro-Antón, L. (Leticia)|||/items/914740d0-4db1-482f-81fa-bbff2cada166de-Miguel, M.J. (María Jesús)|||/items/cfc74851-e6d4-4126-a8f6-71e55b7e72f7Barbier, T. (Thibault)|||/items/b67b44cc-f10c-4bfc-bd12-d5992a13e810Conde-Álvarez, R. (Raquel)|||/items/7a805559-3962-434b-9df9-ec243d61b5aaMuñoz, P. (Pilar)|||/items/4e98f4c8-d3e4-4fb3-b781-07a0bcb652bcLetesson, J.J. (Jean Jacques)|||/items/310147b5-d631-4025-ad82-d3e696cc9a4cIriarte-Cilveti, M. (Maite)|||/items/5b20b123-3967-4f07-b577-13d13aa57363Moriyon, I. (Ignacio)|||/items/834b4ce9-a879-4ba7-8884-39d0ddd88c7bZuñiga-Ripa, A. (Amaia)|||/items/9aa6da2e-e507-4319-a12c-092436f70febBrucellaMetabolismGlucoseEntner-DoudoroffVirulenceBrucella species cause brucellosis, a worldwide extended zoonosis. The brucellae are related to free-living and plant-associated α2-Proteobacteria and, since they multiply within host cells, their metabolism probably reflects this adaptation. To investigate this, we used the rodent-associated Brucella suis biovar 5, which in contrast to the ruminant-associated Brucella abortus and Brucella melitensis and other B. suis biovars, is fast-growing and conserves the ancestral Entner-Doudoroff pathway (EDP) present in the plant-associated relatives. We constructed mutants in Edd (glucose-6-phosphate dehydratase; first EDP step), PpdK (pyruvate phosphate dikinase; phosphoenolpyruvate ⇌ pyruvate), and Pyk (pyruvate kinase; phosphoenolpyruvate → pyruvate). In a chemically defined medium with glucose as the only C source, the Edd mutant showed reduced growth rates and the triple Edd-PpdK-Pyk mutant did not grow. Moreover, the triple mutant was also unable to grow on ribose or xylose. Therefore, B. suis biovar 5 sugar catabolism proceeds through both the Pentose Phosphate shunt and EDP, and EDP absence and exclusive use of the shunt could explain at least in part the comparatively reduced growth rates of B. melitensis and B. abortus. The triple Edd-PpdK-Pyk mutant was not attenuated in mice. Thus, although an anabolic use is likely, this suggests that hexose/pentose catabolism to pyruvate is not essential for B. suis biovar 5 multiplication within host cells, a hypothesis consistent with the lack of classical glycolysis in all Brucella species and of EDP in B. melitensis and B. abortus. These results and those of previous works suggest that within cells, the brucellae use mostly 3 and 4 C substrates fed into anaplerotic pathways and only a limited supply of 5 and 6 C sugars, thus favoring the EDP loss observed in some species.Dadun. Depósito Académico Digital Universidad de Navarra20242024-07-1720212021-01-0120212021-01-01journal articlehttp://purl.org/coar/resource_type/c_6501info:eu-repo/semantics/articleapplication/pdfhttps://hdl.handle.net/10171/69677reponame:Dadun. Depósito Académico Digital de la Universidad de Navarrainstname:Universidad de NavarraInglésengopen accesshttp://purl.org/coar/access_right/c_abf2info:eu-repo/semantics/openAccessoai:dadun.unav.edu:10171/696772026-06-21T12:47:57Z
dc.title.none.fl_str_mv Glucose Oxidation to Pyruvate Is Not Essential for Brucella suis Biovar 5 Virulence in the Mouse Model
title Glucose Oxidation to Pyruvate Is Not Essential for Brucella suis Biovar 5 Virulence in the Mouse Model
spellingShingle Glucose Oxidation to Pyruvate Is Not Essential for Brucella suis Biovar 5 Virulence in the Mouse Model
Lázaro-Antón, L. (Leticia)|||/items/914740d0-4db1-482f-81fa-bbff2cada166
Brucella
Metabolism
Glucose
Entner-Doudoroff
Virulence
title_short Glucose Oxidation to Pyruvate Is Not Essential for Brucella suis Biovar 5 Virulence in the Mouse Model
title_full Glucose Oxidation to Pyruvate Is Not Essential for Brucella suis Biovar 5 Virulence in the Mouse Model
title_fullStr Glucose Oxidation to Pyruvate Is Not Essential for Brucella suis Biovar 5 Virulence in the Mouse Model
title_full_unstemmed Glucose Oxidation to Pyruvate Is Not Essential for Brucella suis Biovar 5 Virulence in the Mouse Model
title_sort Glucose Oxidation to Pyruvate Is Not Essential for Brucella suis Biovar 5 Virulence in the Mouse Model
dc.creator.none.fl_str_mv Lázaro-Antón, L. (Leticia)|||/items/914740d0-4db1-482f-81fa-bbff2cada166
de-Miguel, M.J. (María Jesús)|||/items/cfc74851-e6d4-4126-a8f6-71e55b7e72f7
Barbier, T. (Thibault)|||/items/b67b44cc-f10c-4bfc-bd12-d5992a13e810
Conde-Álvarez, R. (Raquel)|||/items/7a805559-3962-434b-9df9-ec243d61b5aa
Muñoz, P. (Pilar)|||/items/4e98f4c8-d3e4-4fb3-b781-07a0bcb652bc
Letesson, J.J. (Jean Jacques)|||/items/310147b5-d631-4025-ad82-d3e696cc9a4c
Iriarte-Cilveti, M. (Maite)|||/items/5b20b123-3967-4f07-b577-13d13aa57363
Moriyon, I. (Ignacio)|||/items/834b4ce9-a879-4ba7-8884-39d0ddd88c7b
Zuñiga-Ripa, A. (Amaia)|||/items/9aa6da2e-e507-4319-a12c-092436f70feb
author Lázaro-Antón, L. (Leticia)|||/items/914740d0-4db1-482f-81fa-bbff2cada166
author_facet Lázaro-Antón, L. (Leticia)|||/items/914740d0-4db1-482f-81fa-bbff2cada166
de-Miguel, M.J. (María Jesús)|||/items/cfc74851-e6d4-4126-a8f6-71e55b7e72f7
Barbier, T. (Thibault)|||/items/b67b44cc-f10c-4bfc-bd12-d5992a13e810
Conde-Álvarez, R. (Raquel)|||/items/7a805559-3962-434b-9df9-ec243d61b5aa
Muñoz, P. (Pilar)|||/items/4e98f4c8-d3e4-4fb3-b781-07a0bcb652bc
Letesson, J.J. (Jean Jacques)|||/items/310147b5-d631-4025-ad82-d3e696cc9a4c
Iriarte-Cilveti, M. (Maite)|||/items/5b20b123-3967-4f07-b577-13d13aa57363
Moriyon, I. (Ignacio)|||/items/834b4ce9-a879-4ba7-8884-39d0ddd88c7b
Zuñiga-Ripa, A. (Amaia)|||/items/9aa6da2e-e507-4319-a12c-092436f70feb
author_role author
author2 de-Miguel, M.J. (María Jesús)|||/items/cfc74851-e6d4-4126-a8f6-71e55b7e72f7
Barbier, T. (Thibault)|||/items/b67b44cc-f10c-4bfc-bd12-d5992a13e810
Conde-Álvarez, R. (Raquel)|||/items/7a805559-3962-434b-9df9-ec243d61b5aa
Muñoz, P. (Pilar)|||/items/4e98f4c8-d3e4-4fb3-b781-07a0bcb652bc
Letesson, J.J. (Jean Jacques)|||/items/310147b5-d631-4025-ad82-d3e696cc9a4c
Iriarte-Cilveti, M. (Maite)|||/items/5b20b123-3967-4f07-b577-13d13aa57363
Moriyon, I. (Ignacio)|||/items/834b4ce9-a879-4ba7-8884-39d0ddd88c7b
Zuñiga-Ripa, A. (Amaia)|||/items/9aa6da2e-e507-4319-a12c-092436f70feb
author2_role author
author
author
author
author
author
author
author
dc.contributor.none.fl_str_mv Dadun. Depósito Académico Digital Universidad de Navarra
dc.subject.none.fl_str_mv Brucella
Metabolism
Glucose
Entner-Doudoroff
Virulence
topic Brucella
Metabolism
Glucose
Entner-Doudoroff
Virulence
description Brucella species cause brucellosis, a worldwide extended zoonosis. The brucellae are related to free-living and plant-associated α2-Proteobacteria and, since they multiply within host cells, their metabolism probably reflects this adaptation. To investigate this, we used the rodent-associated Brucella suis biovar 5, which in contrast to the ruminant-associated Brucella abortus and Brucella melitensis and other B. suis biovars, is fast-growing and conserves the ancestral Entner-Doudoroff pathway (EDP) present in the plant-associated relatives. We constructed mutants in Edd (glucose-6-phosphate dehydratase; first EDP step), PpdK (pyruvate phosphate dikinase; phosphoenolpyruvate ⇌ pyruvate), and Pyk (pyruvate kinase; phosphoenolpyruvate → pyruvate). In a chemically defined medium with glucose as the only C source, the Edd mutant showed reduced growth rates and the triple Edd-PpdK-Pyk mutant did not grow. Moreover, the triple mutant was also unable to grow on ribose or xylose. Therefore, B. suis biovar 5 sugar catabolism proceeds through both the Pentose Phosphate shunt and EDP, and EDP absence and exclusive use of the shunt could explain at least in part the comparatively reduced growth rates of B. melitensis and B. abortus. The triple Edd-PpdK-Pyk mutant was not attenuated in mice. Thus, although an anabolic use is likely, this suggests that hexose/pentose catabolism to pyruvate is not essential for B. suis biovar 5 multiplication within host cells, a hypothesis consistent with the lack of classical glycolysis in all Brucella species and of EDP in B. melitensis and B. abortus. These results and those of previous works suggest that within cells, the brucellae use mostly 3 and 4 C substrates fed into anaplerotic pathways and only a limited supply of 5 and 6 C sugars, thus favoring the EDP loss observed in some species.
publishDate 2021
dc.date.none.fl_str_mv 2021
2021-01-01
2021
2021-01-01
2024
2024-07-17
dc.type.none.fl_str_mv journal article
http://purl.org/coar/resource_type/c_6501
dc.type.openaire.fl_str_mv info:eu-repo/semantics/article
format article
dc.identifier.none.fl_str_mv https://hdl.handle.net/10171/69677
url https://hdl.handle.net/10171/69677
dc.language.none.fl_str_mv Inglés
eng
language_invalid_str_mv Inglés
language eng
dc.rights.none.fl_str_mv open access
http://purl.org/coar/access_right/c_abf2
dc.rights.openaire.fl_str_mv info:eu-repo/semantics/openAccess
rights_invalid_str_mv open access
http://purl.org/coar/access_right/c_abf2
eu_rights_str_mv openAccess
dc.format.none.fl_str_mv application/pdf
dc.source.none.fl_str_mv reponame:Dadun. Depósito Académico Digital de la Universidad de Navarra
instname:Universidad de Navarra
instname_str Universidad de Navarra
reponame_str Dadun. Depósito Académico Digital de la Universidad de Navarra
collection Dadun. Depósito Académico Digital de la Universidad de Navarra
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