ATP synthesis catalyzed by a V-ATPase: an alternative pathway for energy conservation operating in plant vacuoles?

Abstract

The electrochemical H + gradient generated in tonoplast vesicles isolated from maize seeds was found to be able to drive the reversal of the catalytic cycle of both vacuolar H + -pumps (Façanha and de Meis, 1998). Here we describe the reversibility of the vacuolar V-type H + -ATPase (V-ATPase) even in the absence of the H + gradient in a water-Me 2 SO co-solvent mixture, resulting in net synthesis of [γ-32 P]ATP from [ 32 P]P i and ADP. The water-Me 2 SO (5 to 20 %) media promoted inhibition of both PP i hydrolysis and synthesis reactions whereas it slightly affected the ATP hydrolysis and clearly stimulated the ATP synthesis, which was unaffected by uncoupling agents (FCCP, Triton X-100 or NH 4 + ). This effect of Me 2 SO on the ATP⇔ 32 P exchange reaction seems to be related to a decrease of the apparent K m of the V-ATPase for P i . The results are in accordance to the concept that the energetics of ATP synthesis catalysis depends on the solvation energies interacting in the enzyme microenvironment. A possible physiological significance of this phenomenon for the metabolism of desiccation-tolerant plant cells is discussed.

Vacuolar respiration of nitrate coupled to energy conservation in filamentous Beggiatoaceae

“…In eukaryotic vacuoles the internal pH is usually controlled by V-ATPases that pump protons inward at the expense of ATP (Rea and Poole, 1993;Uyama and Michibata, 1993;Masayoshi, 2000;Nelson et al, 2000;Kane and Smardon, 2003;Seidel, 2009). Nevertheless, in plant vacuoles (Façanha and Okorokova-Façanha, 2008) and in the prokaryotic organism Thermus thermophilus (Toei et al, 2007) energy conservation by V-ATPases has been reported. In Gram-negative bacteria the ETC and PMF-coupled ATPases are associated with the cytoplasmic membrane.…”

The Plant V-ATPase

“…A decrease in cytosolic pH further increases the affinity to ATP to counteract cytosolic acidification and the regulation pays attention to cytosolic and luminal pH; information on the pH might be transported to the other side of the membrane, possibly by protonation of proteins ( Davies et al, 1994 ; Rienmueller et al, 2012 ). For completeness, ATP-synthesis was observed on the V-ATPase of maize vacuoles in the presence of a Me 2 SO-containing medium, which decreases the K m for phosphate because of the altered solvation energy of phosphate, and this reaction was observed even in the absence of a proton gradient ( Façanha and Okorokova-Façanha, 2008 ). The authors suggest that this might also occur as an energy-conserving mechanism in dehydrating environments like, for instance, seed cells.…”