Alkalizing reactions streamline cellular metabolism in acidogenic microorganisms

An understanding of the integrated relationships among the principal cellular functions that govern the bioenergetic reactions of an organism is necessary to determine how cells remain viable and optimise their fitness in the environment. Urease is a complex enzyme that catalyzes the hydrolysis of u...

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Published in:PLoS ONE
Main Authors: S. Arioli, E.M. Ragg, L. Scaglioni, D. Fessas, M. Signorelli, D.G. Daffonchio, I. De Noni, S.D. Guglielmetti, D. Mora, M. Karp, L. Mulas, M. Oggioni
Other Authors: D. Fessa, L. Mula
Format: Article in Journal/Newspaper
Language:English
Published: Public Library of Science 2010
Subjects:
Online Access:http://hdl.handle.net/2434/149703
https://doi.org/10.1371/journal.pone.0015520
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author S. Arioli
E.M. Ragg
L. Scaglioni
D. Fessas
M. Signorelli
D.G. Daffonchio
I. De Noni
S.D. Guglielmetti
D. Mora
M. Karp
L. Mulas
M. Oggioni
author2 S. Arioli
E.M. Ragg
L. Scaglioni
D. Fessa
M. Signorelli
M. Karp
D.G. Daffonchio
I. De Noni
L. Mula
M. Oggioni
S.D. Guglielmetti
D. Mora
author_facet S. Arioli
E.M. Ragg
L. Scaglioni
D. Fessas
M. Signorelli
D.G. Daffonchio
I. De Noni
S.D. Guglielmetti
D. Mora
M. Karp
L. Mulas
M. Oggioni
author_sort S. Arioli
collection The University of Milan: Archivio Istituzionale della Ricerca (AIR)
container_issue 11
container_start_page e15520
container_title PLoS ONE
container_volume 5
description An understanding of the integrated relationships among the principal cellular functions that govern the bioenergetic reactions of an organism is necessary to determine how cells remain viable and optimise their fitness in the environment. Urease is a complex enzyme that catalyzes the hydrolysis of urea to ammonia and carbonic acid. While the induction of urease activity by several microorganisms has been predominantly considered a stress-response that is initiated to generate a nitrogen source in response to a low environmental pH, here we demonstrate a new role of urease in the optimisation of cellular bioenergetics. We show that urea hydrolysis increases the catabolic efficiency of Streptococcus thermophilus, a lactic acid bacterium that is widely used in the industrial manufacture of dairy products. By modulating the intracellular pH and thereby increasing the activity of β-galactosidase, glycolytic enzymes and lactate dehydrogenase, urease increases the overall change in enthalpy generated by the bioenergetic reactions. A cooperative altruistic behaviour of urease-positive microorganisms on the urease-negative microorganisms within the same environment was also observed. The physiological role of a single enzymatic activity demonstrates a novel and unexpected view of the non-transcriptional regulatory mechanisms that govern the bioenergetics of a bacterial cell, highlighting a new role for cytosol-alkalizing biochemical pathways in acidogenic microorganisms.
format Article in Journal/Newspaper
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language English
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journal:PLOS ONE
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spelling ftunivmilanoair:oai:air.unimi.it:2434/149703 2025-01-16T21:28:10+00:00 Alkalizing reactions streamline cellular metabolism in acidogenic microorganisms S. Arioli E.M. Ragg L. Scaglioni D. Fessas M. Signorelli D.G. Daffonchio I. De Noni S.D. Guglielmetti D. Mora M. Karp L. Mulas M. Oggioni S. Arioli E.M. Ragg L. Scaglioni D. Fessa M. Signorelli M. Karp D.G. Daffonchio I. De Noni L. Mula M. Oggioni S.D. Guglielmetti D. Mora 2010 http://hdl.handle.net/2434/149703 https://doi.org/10.1371/journal.pone.0015520 eng eng Public Library of Science info:eu-repo/semantics/altIdentifier/pmid/21152088 info:eu-repo/semantics/altIdentifier/wos/WOS:000284755100091 volume:5 issue:11 firstpage:e15520.1 lastpage:e15520.8 journal:PLOS ONE http://hdl.handle.net/2434/149703 doi:10.1371/journal.pone.0015520 info:eu-repo/semantics/altIdentifier/scopus/2-s2.0-78649790948 info:eu-repo/semantics/openAccess Settore AGR/16 - Microbiologia Agraria info:eu-repo/semantics/article 2010 ftunivmilanoair https://doi.org/10.1371/journal.pone.0015520 2024-01-02T23:27:08Z An understanding of the integrated relationships among the principal cellular functions that govern the bioenergetic reactions of an organism is necessary to determine how cells remain viable and optimise their fitness in the environment. Urease is a complex enzyme that catalyzes the hydrolysis of urea to ammonia and carbonic acid. While the induction of urease activity by several microorganisms has been predominantly considered a stress-response that is initiated to generate a nitrogen source in response to a low environmental pH, here we demonstrate a new role of urease in the optimisation of cellular bioenergetics. We show that urea hydrolysis increases the catabolic efficiency of Streptococcus thermophilus, a lactic acid bacterium that is widely used in the industrial manufacture of dairy products. By modulating the intracellular pH and thereby increasing the activity of β-galactosidase, glycolytic enzymes and lactate dehydrogenase, urease increases the overall change in enthalpy generated by the bioenergetic reactions. A cooperative altruistic behaviour of urease-positive microorganisms on the urease-negative microorganisms within the same environment was also observed. The physiological role of a single enzymatic activity demonstrates a novel and unexpected view of the non-transcriptional regulatory mechanisms that govern the bioenergetics of a bacterial cell, highlighting a new role for cytosol-alkalizing biochemical pathways in acidogenic microorganisms. Article in Journal/Newspaper Carbonic acid The University of Milan: Archivio Istituzionale della Ricerca (AIR) PLoS ONE 5 11 e15520
spellingShingle Settore AGR/16 - Microbiologia Agraria
S. Arioli
E.M. Ragg
L. Scaglioni
D. Fessas
M. Signorelli
D.G. Daffonchio
I. De Noni
S.D. Guglielmetti
D. Mora
M. Karp
L. Mulas
M. Oggioni
Alkalizing reactions streamline cellular metabolism in acidogenic microorganisms
title Alkalizing reactions streamline cellular metabolism in acidogenic microorganisms
title_full Alkalizing reactions streamline cellular metabolism in acidogenic microorganisms
title_fullStr Alkalizing reactions streamline cellular metabolism in acidogenic microorganisms
title_full_unstemmed Alkalizing reactions streamline cellular metabolism in acidogenic microorganisms
title_short Alkalizing reactions streamline cellular metabolism in acidogenic microorganisms
title_sort alkalizing reactions streamline cellular metabolism in acidogenic microorganisms
topic Settore AGR/16 - Microbiologia Agraria
topic_facet Settore AGR/16 - Microbiologia Agraria
url http://hdl.handle.net/2434/149703
https://doi.org/10.1371/journal.pone.0015520