Active transport of Ca2+ in bacteria: Bioenergetics and function

Abstract

The bioenergetics of Ca2+ transport in bacteria are discussed with special emphasis on the interrelationship between transport and other cellular functions such as substrate oxidation by the respiratory chain and oxidative phosphorylation. The unusual polarity of Ca2+ movement provides an exceptional tool to compare active transport and other ATP requiring or generating processes since this ion is actively taken up by everted vesicles in which the coupling-factor ATPase is exposed to the external medium. As inferred from studies with everted vesicles, the active extrusion of Ca2+ by whole cells can be accomplished by substrate driven respiration, hydrolysis of ATP or as in the case of Streptococcus faecalis by a nonhydrolytic unknown process which involves ATP directly. Substrate oxidation and the hydrolysis of ATP result in the generation of a pH gradient which can energize the Ca2+ uptake directly (Ca2+/H+ antiport) or via a secondary Na+ gradient (Ca2+/Na+ antiport). In contrast to exponentially growing cells sporulating Bacilli accumulate Ca2+ during the synthesis of dipicolinic acid. Studies involving Ca2+ transport provided evidence in support of the hypothesis that the Mg2+ ATPase from Escherichia coli not only provides the driving force for various cellular functions but exerts a regulatory role by controlling the permeability of the membrane to protons. The different specificity requirements of various naphthoquinone analogs in the restoration of transport or oxidative phosphorylation, after the natural menaquinone has been destroyed by irradiation, has indicated that a protonmotive force is sufficient to drive active transport. However, in addition to the driving force (protonmotive force) necessary to establish oxidative phosphorylation, a specific spatial orientation of the respiratory components, such as the naphthoquinones, is essential for the utilization of the proton gradient or membrane potential or both. Finally, evidence suggesting that intracellular Ca2+ levels might play a fundamental role in bacterial homeostasis is discussed, in particular the role of Ca2+ in the process of chemotaxis and in conferring bacteria heat stability. A vitamin K-dependent carboxylation reaction has been found in Escherichia coli which is similar to that reported in mammalian systems which results in gamma carboxylation of glutamate residues. Although all of the proteins containing gamma-carboxyglutamate described so far are involved in Ca2+ metabolism, the role of these proteins in Escherichia coli is unknown and remains to be elucidated.

Calcium, cyclic AMP and protein kinase C ? partners in mitogenesis

“…Nevertheless, there were hints of the great things to come when Streptococcus lactis learned to use Ca 2+ to inactivate a surfaceassociated growth inhibitor, nisin, in order to start proliferating [9][10][11] and in the possible use of Ca 2+ by some prokaryotes to drive their simple flagellar motors [12a]. However, they did set the stage for a spectacular biotechnological breakthrough by devising various ways (CaZ+/H +, Ca2+/Na antiporters, CaZ+-ATPase pumps) to avoid loading their interiors with Ca 2+ [13] which could have killed them by precipitating phosphates and activating degradative phospholipases and proteinases [7,8]. Prokaryotes also laid the foundations for another major control system by inventing cyclic AMP and the cyclic AMP-binding/activated CAP protein ('catabolite gene activator protein'), the probable ancestor of the R subunits of our cyclic AMP.…”

AterDDomain-Encoding Gene (SCO2368) Is Involved in Calcium Homeostasis and Participates in Calcium Regulation of a DosR-Like Regulon in Streptomyces coelicolor

“…Tdd8 does not belong to these classes of proteins, and it is unlikely that it acts as a direct sensor for O 2 , NO, or CO. Changes in the redox state could, however, be indirectly sensed by pools of molecules within the cell that include metal ions, such as Ca 2ϩ (41). It has been proposed that Ca 2ϩ acts as a second messenger by controlling membrane permeativity to protons (42,43). Ca 2ϩ signaling may also be involved in adaptation to various stress responses, as tdd8 expression or Tdd8 production is modulated under various stress conditions, including hypoxia (references 6, 7, and 8 and this work).…”

Properties of the Germination Inhibitor of Streptomyces viridochromogenes Spores

“…Of potential relevance to the apparent role of ATPase during Ca2+-induced initiation of germination of S. viridochromogenes spores are the reports of trypsin activated ATPase activity associated with calcium transport in A. vinelandii (Bhattacharyya & Barnes, 1976) and M. phlei (Deves & Brodie, 1981). Release of spore components during the initiation stage of Ca2+-induced germination of S. viridochromogenes ceases immediately upon addition of EDTA and resumes following removal of the chelator and addition of Ca2+ ions (Eaton & Ensign, 1980).…”