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Pre‐steady‐state kinetics and solvent isotope effects support the “billiard‐type” transport mechanism in <scp>Na</scp><sup>+</sup>‐translocating pyrophosphatase

Anssi M. Malinen, Viktor A. Anashkin, В. Н. Орлов, Alexander V. Bogachev, Reijo Lahti, Alexander A. Baykov

2022Protein Science13 citationsDOIOpen Access PDF

Abstract

Abstract Membrane‐bound pyrophosphatase (mPPase) found in microbes and plants is a membrane H + pump that transports the H + ion generated in coupled pyrophosphate hydrolysis out of the cytoplasm. Certain bacterial and archaeal mPPases can in parallel transport Na + via a hypothetical “billiard‐type” mechanism, also involving the hydrolysis‐generated proton. Here, we present the functional evidence supporting this coupling mechanism. Rapid‐quench and pulse‐chase measurements with [ 32 P]pyrophosphate indicated that the chemical step (pyrophosphate hydrolysis) is rate‐limiting in mPPase catalysis and is preceded by a fast isomerization of the enzyme‐substrate complex. Na + , whose binding is a prerequisite for the hydrolysis step, is not required for substrate binding. Replacement of H 2 O with D 2 O decreased the rates of pyrophosphate hydrolysis by both Na + ‐ and H + ‐transporting bacterial mPPases, the effect being more significant than with a non‐transporting soluble pyrophosphatase. We also show that the Na + ‐pumping mPPase of Thermotoga maritima resembles other dimeric mPPases in demonstrating negative kinetic cooperativity and the requirement for general acid catalysis. The findings point to a crucial role for the hydrolysis‐generated proton both in H + ‐pumping and Na + ‐pumping by mPPases.

Topics & Concepts

PyrophosphateChemistryInorganic pyrophosphatasePyrophosphataseHydrolysisATP hydrolysisThermotoga maritimaSubstrate (aquarium)ATPaseStereochemistryEnzymeBiochemistryEscherichia coliBiologyGeneEcologyATP Synthase and ATPases ResearchIon Transport and Channel RegulationLipid Membrane Structure and Behavior
Pre‐steady‐state kinetics and solvent isotope effects support the “billiard‐type” transport mechanism in <scp>Na</scp><sup>+</sup>‐translocating pyrophosphatase | Litcius