title: Alkalizing reactions streamline cellular metabolism in acidogenic microorganisms.
abstract: 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.
authors.affiliation: Dipartimento di Scienze e Tecnologie Alimentari e Microbiologiche, Università degli Studi di Milano, Milan, Italy.
authors.forename: Stefania
authors.initials: S
authors.lastname: Arioli
authors.forename: Enzio
authors.initials: E
authors.lastname: Ragg
authors.forename: Leonardo
authors.initials: L
authors.lastname: Scaglioni
authors.forename: Dimitrios
authors.initials: D
authors.lastname: Fessas
authors.forename: Marco
authors.initials: M
authors.lastname: Signorelli
authors.forename: Matti
authors.initials: M
authors.lastname: Karp
authors.forename: Daniele
authors.initials: D
authors.lastname: Daffonchio
authors.forename: Ivano
authors.initials: I
authors.lastname: De Noni
authors.forename: Laura
authors.initials: L
authors.lastname: Mulas
authors.forename: Marco
authors.initials: M
authors.lastname: Oggioni
authors.forename: Simone
authors.initials: S
authors.lastname: Guglielmetti
authors.forename: Diego
authors.initials: D
authors.lastname: Mora
mesh_terms: D000143:Acids / Q000378:metabolism*; D000255:Adenosine Triphosphate / Q000378:metabolism; D000468:Alkalies / Q000378:metabolism*; D000641:Ammonia / Q000378:metabolism; D001419:Bacteria / Q000254:growth & development / Q000378:metabolism*; D002255:Carbonic Acid / Q000378:metabolism; D017753:Ecosystem; D004734:Energy Metabolism; D006019:Glycolysis; D006863:Hydrogen-Ion Concentration; D006868:Hydrolysis; D007770:L-Lactate Dehydrogenase / Q000378:metabolism; D050296:Microbial Viability; D048249:Streptococcus thermophilus / Q000254:growth & development / Q000378:metabolism; D014508:Urea / Q000378:metabolism; D014510:Urease / Q000378:metabolism; D001616:beta-Galactosidase / Q000378:metabolism
chemical_list: D000143:Acids; D000468:Alkalies; D002255:Carbonic Acid; D000641:Ammonia; D000255:Adenosine Triphosphate; D014508:Urea; D007770:L-Lactate Dehydrogenase; D001616:beta-Galactosidase; D014510:Urease