The sodium cycle: A novel type of bacterial energetics

Abstract

The progress of bioenergetic studies on the role of Na⁺ in bacteria is reviewed. Experiments performed over the past decade on several bacterial species of quite different taxonomic positions show that Na⁺ can, under certain conditions, substitute for H⁺ as the coupling ion. Various primary Na⁺ pumps ($\Delta \bar \mu _{Na^ + }$ generators) are described, i.e., Na⁺-motive decarboxylases, NADH-quinone reductase, terminal oxidase, and ATPase. The$\Delta \bar \mu _{Na^ + }$ formed is shown to be consumed by Na⁺ driven ATP-synthase, Na⁺ flagellar motor, numerous Na⁺, solute symporters, and the methanogenesis-linked reverse electron transfer system. InVibrio alginolyticus, it was found that$\Delta \bar \mu _{Na^ + }$, generated by NADH-quinone reductase, can be utilized to support all three types of membrane-linked work, i.e., chemical (ATP synthesis), osmotic (Na⁺, solute symports), and mechanical (rotation of the flagellum). InPropionigenum modestum, circulation of Na⁺ proved to be the only mechanism of energy coupling. In other species studied, the Na⁺ cycle seems to coexist with the H⁺ cycle. For instance, inV. alginolyticus the initial and terminal steps of the respiratory chain are Na⁺ - and H⁺-motive, respectively, whereas ATP hydrolysis is competent in the uphill transfer of Na⁺ as well as of H⁺. In the alkalo- and halotolerantBacillus FTU, there are H⁺ - and Na⁺-motive terminal oxidases. Sometimes, the Na⁺-translocating enzyme strongly differs from its H⁺-translocating homolog. So, the Na⁺-motive and H⁺-motive NADH-quinone reductases are composed of different subunits and prosthetic groups. The H⁺-motive and Na⁺-motive terminal oxidases differ in that the former is ofaa ₃-type and sensitive to micromolar cyanide whereas the latter is of another type and sensitive to millimolar cyanide. At the same time, both Na⁺ and H⁺ can be translocated by one and the sameP. modestum ATPase which is of the F₀F₁-type and sensitive to DCCD. The sodium cycle, i.e., a system composed of primary$\Delta \bar \mu _{Na^ + }$ generator(s) and$\Delta \bar \mu _{Na^ + }$ consumer(s), is already described in many species of marine aerobic and anaerobic eubacteria and archaebacteria belonging to the following genera:Vibrio, Bacillus, Alcaligenes, Alteromonas, Salmonella, Klebsiella, Propionigenum, Clostridium, Veilonella, Acidaminococcus, Streptococcus, Peptococcus, Exiguobacterium, Fusobacterium, Methanobacterium, Methanococcus, Methanosarcin, etc. Thus, the “sodium world” seems to occupy a rather extensive area in the biosphere.