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: Arioli, S, Ragg, E, Scaglioni, L, Fessas, D, Signorelli, M, Karp, M, Daffonchio, D, De Noni, I, Mulas, L, Oggioni, M, Guglielmetti, S, Mora, D
Format: Article in Journal/Newspaper
Language:English
Published: Public Library of Science 2010
Subjects:
Online Access:https://hdl.handle.net/10281/458469
https://doi.org/10.1371/journal.pone.0015520
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author Arioli, S
Ragg, E
Scaglioni, L
Fessas, D
Signorelli, M
Karp, M
Daffonchio, D
De Noni, I
Mulas, L
Oggioni, M
Guglielmetti, S
Mora, D
author2 Arioli, S
Ragg, E
Scaglioni, L
Fessas, D
Signorelli, M
Karp, M
Daffonchio, D
De Noni, I
Mulas, L
Oggioni, M
Guglielmetti, S
Mora, D
author_facet Arioli, S
Ragg, E
Scaglioni, L
Fessas, D
Signorelli, M
Karp, M
Daffonchio, D
De Noni, I
Mulas, L
Oggioni, M
Guglielmetti, S
Mora, D
author_sort Arioli, S
collection Università degli Studi di Milano-Bicocca: BOA (Bicocca Open Archive)
container_issue 11
container_start_page e15520
container_title PLoS ONE
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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.
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journal:PLOS ONE
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spelling ftunivmilanobic:oai:boa.unimib.it:10281/458469 2025-05-25T13:49:07+00:00 Alkalizing reactions streamline cellular metabolism in acidogenic microorganisms Arioli, S Ragg, E Scaglioni, L Fessas, D Signorelli, M Karp, M Daffonchio, D De Noni, I Mulas, L Oggioni, M Guglielmetti, S Mora, D Arioli, S Ragg, E Scaglioni, L Fessas, D Signorelli, M Karp, M Daffonchio, D De Noni, I Mulas, L Oggioni, M Guglielmetti, S Mora, D 2010 ELETTRONICO https://hdl.handle.net/10281/458469 https://doi.org/10.1371/journal.pone.0015520 eng eng Public Library of Science country:US info:eu-repo/semantics/altIdentifier/pmid/21152088 info:eu-repo/semantics/altIdentifier/wos/WOS:000284755100091 volume:5 issue:11 firstpage:1 lastpage:8 numberofpages:8 journal:PLOS ONE https://hdl.handle.net/10281/458469 doi:10.1371/journal.pone.0015520 info:eu-repo/semantics/openAccess Urease info:eu-repo/semantics/article 2010 ftunivmilanobic https://doi.org/10.1371/journal.pone.0015520 2025-04-28T01:57:12Z 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 Università degli Studi di Milano-Bicocca: BOA (Bicocca Open Archive) PLoS ONE 5 11 e15520
spellingShingle Urease
Arioli, S
Ragg, E
Scaglioni, L
Fessas, D
Signorelli, M
Karp, M
Daffonchio, D
De Noni, I
Mulas, L
Oggioni, M
Guglielmetti, S
Mora, D
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 Urease
topic_facet Urease
url https://hdl.handle.net/10281/458469
https://doi.org/10.1371/journal.pone.0015520