Regulation of the Plasma Membrane H+-ATPase: Tale of an Ancient Proton Transporter

Janus Falhof

Abstract

The plasma membrane (PM) H+-ATPase is responsible for generating the electrochemical gradientthat drives the secondary transport of nutrients across the cellular membrane. It belongs to a familyof cation and lipid transporters that are vital to many organisms. PM H+-ATPases are Type P3AATPases and are generally perceived to be present in Archaea, algae, fungi and plants. The everexpanding sequence databases give us an opportunity to reevaluate our current knowledge of theevolutionary origin of PM H+-ATPases. In a phylogenetic study we found that a number of bacterialsequences grouped together with known PM H+-ATPase. Further biochemical analysis confirmedthat one of these putative bacterial PM H+-ATPases did indeed pump protons and stronglysuggested that PM H+-ATPases are present in bacteria. The PM H+-ATPases are closely related to agroup of bacterial Mg2+ transporters that share many of the same structural features that are knownto define a P-type ATPase. This close relation often renders it difficult to distinguish between thetwo families when grouping new uncharacterized protein sequences. We found that a conservedproton gating residue and a proposed built-in counter ion can serve as a future determinant whengrouping PM H+ and Mg2+-ATPases. The activity of some plant PM H+-ATPases is tightlyregulated by the actions of the autoinhibitory terminal domains, a feature not found in all plantsharboring proton pumps. We found that regulation by the C-terminal domain evolved with the firstland plants and that their green algae ancestor does not have this mechanism of regulation. Thisindicates that with the development of more complex organisms the need for a tighter regulation ofthe H+- ATPase activity has also evolved.Since the late 1980`s it have been known that lysophospholipids upregulate the activity of the PMH+-ATPases. It was though unknown whether this activation was specific and which characteristicsof the activating lipid that plays a role. We found that the effect of the lipid lysophophatidylcholine(lysoPC) was indeed specific and not dependent on binding the activating protein 14-3-3. Thelength of the fatty acid chain proved to be a determining factor in the activating level of lysoPC aswell as the nature of the glycerol group and it was found that the choline head-group did not appearto play any major role in the activating level of lysoPC. The fungal PM H+-ATPase is interestinglynot affected by lysoPC, indicating that the regulatory mechanism of lysoPC could be a featureevolved specifically in plants. The in-vivo relevance for this finding in plants remains to be provenbut the involvement of lipids in regulation of other P-type ATPases points at a possible commontheme of regulation by phosphorlipids.

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