Revisiting the cellular mechanisms of strong luminal alkalinization in the anterior midgut of larval mosquitoes

SUMMARY This review provides alternatives to two well established theories regarding membrane energization by H+ V-ATPases. Firstly, we offer an alternative to the notion that the H+ V-ATPase establishes a protonmotive force (pmf) across the membrane into which it is inserted. The term pmf, which was introduced by Peter Mitchell in 1961 in his chemiosmotic hypothesis for the synthesis of ATP by H+ F-ATP synthases, has two parts, the electrical potential difference across the phosphorylating membrane, Δψ, and the pH difference between the bulk solutions on either side of the membrane, ΔpH. The ΔpH term implies three phases – a bulk fluid phase on the H+ input side, the membrane phase and a bulk fluid phase on the H+ output side. The Mitchell theory was applied to H+ V-ATPases largely by analogy with H+ F-ATP synthases operating in reverse as H+ F-ATPases. We suggest an alternative, voltage coupling model. Our model for V-ATPases is based on Douglas B. Kell's 1979 `electrodic view' of ATP synthases in which two phases are added to the Mitchell model – an unstirred layer on the input side and another one on the output side of the membrane. In addition, we replace the notion that H+ V-ATPases normally acidify the output bulk solution with the hypothesis, which we introduced in 1992, that the primary action of a H+ V-ATPase is to charge the membrane capacitance and impose a Δψ across the membrane; the translocated hydrogen ions (H+s) are retained at the outer fluid–membrane interface by electrostatic attraction to the anions that were left behind. All subsequent events, including establishing pH differences in the outside bulk solution, are secondary. Using the surface of an electrode as a model, Kell's`electrodic view' has five phases – the outer bulk fluid phase, an outer fluid–membrane interface, the membrane phase, an inner fluid–membrane interface and the inner bulk fluid phase. Light flash,H+ releasing and binding experiments and other evidence provide convincing support for Kell's electrodic view yet Mitchell's chemiosmotic theory is the one that is accepted by most bioenergetics experts today. First we discuss the interaction between H+ V-ATPase and the K+/2H+ antiporter that forms the caterpillar K+ pump, and use the Kell electrodic view to explain how the H+s at the outer fluid–membrane interface can drive two H+ from lumen to cell and one K+ from cell to lumen via the antiporter even though the pH in the bulk fluid of the lumen is highly alkaline. Exchange of outer bulk fluid K+ (or Na+) with outer interface H+ in conjunction with (K+ or Na+)/2H+ antiport, transforms the hydrogen ion electrochemical potential difference, \batchmode \documentclass[fleqn,10pt,legalpaper]{article} \usepackage{amssymb} \usepackage{amsfonts} \usepackage{amsmath} \pagestyle{empty} \begin{document} \(\overline{{\mu}}_{\mathrm{H}}\) \end{document}, to a K+electrochemical potential difference, \batchmode \documentclass[fleqn,10pt,legalpaper]{article} \usepackage{amssymb} \usepackage{amsfonts} \usepackage{amsmath} \pagestyle{empty} \begin{document} \(\overline{{\mu}}_{\mathrm{K}}\) \end{document} or a Na+electrochemical potential difference, \batchmode \documentclass[fleqn,10pt,legalpaper]{article} \usepackage{amssymb} \usepackage{amsfonts} \usepackage{amsmath} \pagestyle{empty} \begin{document} \(\overline{{\mu}}_{\mathrm{Na}}\) \end{document}. The \batchmode \documentclass[fleqn,10pt,legalpaper]{article} \usepackage{amssymb} \usepackage{amsfonts} \usepackage{amsmath} \pagestyle{empty} \begin{document} \(\overline{{\mu}}_{\mathrm{K}}\) \end{document} or \batchmode \documentclass[fleqn,10pt,legalpaper]{article} \usepackage{amssymb} \usepackage{amsfonts} \usepackage{amsmath} \pagestyle{empty} \begin{document} \(\overline{{\mu}}_{\mathrm{Na}}\) \end{document} drives K+- or Na+-coupled nutrient amino acid transporters (NATs), such as KAAT1(K+ amino acid transporter 1), which moves Na+ and an amino acid into the cell with no H+s involved. Examples in which the voltage coupling model is used to interpret ion and amino acid transport in caterpillar and larval mosquito midgut are discussed.

Section: Complexity Of Membrane Energization and Energy Utilizationmentioning

confidence: 85%

Voltage coupling of primary H+ V-ATPases to secondary Na+- or K+-dependent transporters

Harvey

2009

“…Serotonin is also involved in regulation of peripheral tissues in larval A. aegypti, but the role of serotonin in the physiological responses of larval A. aegypti to feeding are less clear than in Rhodnius. Serotonin stimulates acid/base transport of the larval mosquito midgut, and fluid secretion by the Malpighian tubules (Clark and Bradley, 1996;Clark and Bradley, 1997;Clark et al, 1999;Onken et al, 2008;Onken and Moffett, 2009); actions likely to be associated with feeding. However, Clark and Bradley detected no changes in hemolymph serotonin levels of larval A. aegypti in response to feeding status (Clark and Bradley, 1997).…”

Section: Effects Of Paroxetine On Wriggling Locomotionmentioning

confidence: 99%

Modulation of appetite and feeding behavior of the larval mosquito Aedes aegypti (L.) by the serotonin-selective reuptake inhibitor paroxetine: shifts between distinct feeding modes and the influence of feeding status.

Kinney

Panting

Clark

2013

The effects of the serotonin-selective reuptake inhibitor paroxetine (2×10 -5 mol l -1) on behavior of the larval mosquito Aedes aegypti are described. Four discrete behavioral states dominate larval behavior: wriggling, two distinct types of feeding, and quiescence. Feeding behaviors consist of foraging along the bottom of the container (substrate browsing), and stationary filter feeding while suspended from the surface film. Fed larvae respond to paroxetine with increased wriggling, and reductions in both feeding behaviors. In contrast, food-deprived larvae treated with paroxetine show no change in the proportion of time spent wriggling or feeding, but shift from stationary filter feeding to substrate browsing. Thus, actions of paroxetine in fed larvae are consistent with suppression of appetite and stimulation of wriggling, whereas paroxetine causes fooddeprived larvae to switch from one feeding behavior to another. Further analysis of unfed larvae revealed that paroxetine decreased the power stroke frequency during wriggling locomotion, but had no effect on the swimming velocity during either wriggling or substrate browsing. These data suggest that: (1) serotonergic pathways may trigger shifts between distinct behaviors by actions on higher level (brain) integrating centers where behaviors such as feeding and locomotion are coordinated; (2) these centers in fed and fooddeprived larvae respond differently to serotonergic stimulation suggesting sensory feedback from feeding status; and (3) serotonergic pathways also modulate central pattern generators of the nerve cord where the bursts of action potentials originate that drive the rhythmic muscle contractions of wriggling.

“…The physiological roles of VHA in insects (Baumann and Walz, 2012;Onken and Moffett, 2009;Wieczorek et al, 2009) and mammals (Brown et al, 2009;Jefferies et al, 2008;Saroussi and Nelson, 2009;Wagner et al, 2004) are periodically reviewed. Similarly, recent comprehensive reviews have discussed the involvement of VHA in H + secretion and NaCl absorption in freshwater crustaceans, fish and amphibians (Evans et al, 2005;Larsen et al, 2014;Perry and Gilmour, 2006).…”

Section: Introductionmentioning

confidence: 99%

Novel and potential physiological roles of vacuolar-type H+-ATPase in marine organisms

Tresguerres

2016

The vacuolar-type H + -ATPase (VHA) is a multi-subunit enzyme that uses the energy from ATP hydrolysis to transport H + across biological membranes. VHA plays a universal role in essential cellular functions, such as the acidification of lysosomes and endosomes. In addition, the VHA-generated H + -motive force can drive the transport of diverse molecules across cell membranes and epithelia for specialized physiological functions. Here, I discuss diverse physiological functions of VHA in marine animals, focusing on recent discoveries about base secretion in shark gills, potential bone dissolution by Osedax boneeating worms and its participation in a carbon-concentrating mechanism that promotes coral photosynthesis. Because VHA is evolutionarily conserved among eukaryotes, it is likely to play many other essential physiological roles in diverse marine organisms. Elucidating and characterizing basic VHA-dependent mechanisms could help to determine species responses to environmental stress, including (but not limited to) that resulting from climate change.