Light activation of the sodium pump in blowfly photoreceptors
- 53 Downloads
The oxygen consumption of the compound eye in the blowfly was determined during light exposure and in darkness by a manometric measuring technique. Within the first 10 s of exposure to bright white light the oxygen uptake increased up to 20 × the resting value in darkness, which is 2.4 to 3×10−5ml oxygen x min−1 × eye−1.
The time course of oxygen consumption during 3-min light stimulation proceeded in two phases: an initial dynamic phase, followed by a decline to a maintained phase of almost constant amplitude. The time course of the dynamic phase varied with the intensity and wavelength of the stimulating light. In contrast, within the intensity range used, oxygen consumption during the maintained phase was about double the resting value in darkness, irrespective of intensity and wavelength of the light stimulus. The time course of the decline in oxygen consumption during light exposure paralleled the electrophysiologically recorded time course of decrease in amplitude of the photoreceptor response.
Light-induced oxygen consumption decreased continuously after replacement of the extracellular fluid in the eye by solutions of increasing potassium concentration. Oxygen uptake in darkness was influenced less. It is concluded that the additional oxygen consumption during light exposure is mainly caused by activation of the sodium-potassium pump.
Replacing extracellular sodium by choline did not markedly reduce the oxygen uptake. This result indicates that, after perfusion of the eye, sodium is pumped out of the cell, causing a sodium gradient to be re-established. Alternatively, the ion pump can accept choline and thus is not highly specific for sodium.
Complete exchange of extracellular sodium by calcium or magnesium 150 mmol/l caused only a small reduction in light-induced oxygen consumption. This observation can be explained by an ion exchange coupled to the ion transport mechanism. The intracellular store of sodium after the replacement is sufficient to form a small sodium gradient, which drives a sodium-calcium exchanger. Sodium itself is actively pumped out. This coupled transport mechanism seems to be sensitive to the extracellular anion composition, since chloride markedly reduced the transport rate.
The oxygen consumption above steady state, following excitation by blue light, was about six times higher in rhodopsin-rich eyes than in rhodopsin-poor eyes. Oxygen uptake following light exposure thus depends on the absolute rhodopsin content in the rhabdomeres. Sequential stimulations by blue-red or red-blue light showed that the higher oxygen uptake following light exposure in rhodopsin-rich eyes is caused by the excess in excited metarhodopsin molecules, which is strongly correlated with the PDA signal.
ATP consumption per absorbed light quantum decreases supralinearly with increasing stimulus intensity. Light intensities eliciting photoreceptor responses of a maximal amplitude of 0.64 induce an initial ATP consumption of about 54000 molecules per absorbed quantum. Exposure to bright white light, hitting all rhodopsin molecules many times within 10 s, initially induces a consumption of only 90 ATP molecules per quantum. After 3-min exposure, consumption is reduced to only 7 ATP molecules per quantum. This dramatic reduction in ATP consumption per absorbed quantum occurs within the upper range of physiological light intensities. The results demonstrate that, at low light intensities, most of the energy is used for pump activity. At high physiological intensities, the fraction of energy consumption used for biochemical amplification and adaptation processes becomes more important.
KeywordsOxygen Uptake Light Exposure Extracellular Sodium Sodium Gradient Rhodopsin Molecule
prolonged depolarizing afterpotential
Unable to display preview. Download preview PDF.
- Autrum H, Hamdorf K (1964) Der Sauerstoffverbrauch des Bienenauges in Abhängigkeit von der Temperatur bei Belichtung und im Dunkeln. Z Vergl Physiol 48:266–269Google Scholar
- Autrum H, Tscharntke H (1962) Der Sauerstoffverbrauch der Insektenretina im Licht und im Dunkeln. Z Vergl Physiol 45:695–710Google Scholar
- Brown JE, Coles JA (1987) Simultaneous recording of luciferase luminescence and PO2 inLimulus ventral photoreceptor. J Physiol 382:118PGoogle Scholar
- Chance B, Williams GR (1955) Respiratory enzymes in oxidative phosphorylation. I. Kinetics of oxygen utilization. J Biol Chem 217:383–393Google Scholar
- Coles JA, Orkand RK (1985) Changes in sodium activity during light stimulation in photoreceptors, glia and extracellular space in drone retina. J Physiol 362:415–435Google Scholar
- Dimitracos SA, Tsacopoulos M (1985) The recovery from a transient inhibition of the oxidative metabolism of the photoreceptors of the drone (Apis mellifera ♂). J Exp Biol 119:165–181Google Scholar
- Dörrscheidt-Käfer M (1972) Die Empfindlichkeit einzelner Photorezeptoren im Komplexauge vonCalliphora erythrocephala. J Comp Physiol 81:309–340Google Scholar
- Hamdorf K (1979) The physiology of invertebrate visual pigments. In: Autrum H (ed) Vision in invertebrates (Handbook of sensory physiology, vol VII/6A). Springer, Berlin Heidelberg New York, pp 145–224Google Scholar
- Hamdorf K, Kaschef AH (1964) Der Sauerstoffverbrauch des Facettenauges vonCalliphora erythrocephala in Abhängigkeit von der Temperatur und dem Ionenmilieu. Z Vergl Physiol 48:251–265Google Scholar
- Hamdorf K, Langer H (1966) Der Sauerstoffverbrauch des Facettenauges vonCalliphora erythrocephala in Abhängigkeit von der Wellenlänge des Reizlichtes. Z Vergl Physiol 52:386–400Google Scholar
- Hamdorf K, Razmjoo S (1977) The prolonged depolarizing afterpotential and its contribution to the understanding of photoreceptor function. Biophys Struct Mech 3:163–170Google Scholar
- Hamdorf K, Razmjoo S (1979) Photoconvertible pigment states and excitation inCalliphora; the induction and properties of the prolonged depolarizing afterpotential. Biophys Struct Mech 5:137–161Google Scholar
- Hamdorf K, Schwemer J (1975) Photoregeneration and the adaptation process in insect photoreceptors. In: Snyder AW, Menzel R (eds) Photoreceptor optics. Springer, Berlin Heidelberg New York, pp 263–289Google Scholar
- Hamdorf K, Höglund G, Schlecht P (1978) Ion gradient and photoreceptor sensitivity. J Comp Physiol 125:237–252Google Scholar
- Harris SI, Balaban RS, Mandel LJ (1980) Oxygen consumption and cellular ion transport: evidence for adenosine triphosphate to O2 ratio near 6 in intact cell. Science 208:1148–1150Google Scholar
- Hochstrate P, Hamdorf K (1985) The influence of extracellular calcium on the response of fly photoreceptors. J Comp Physiol A 156:53–64Google Scholar
- Langer H (1960) Über den chemischen Aufbau des Facettenauges vonCalliphora erythrocephala Meig. und seine Veränderungen mit dem Imaginalalter. Z Vergl Physiol 42:595–626Google Scholar
- Langer H (1962) Untersuchungen über die Größe des Stoffwechsels isolierter Augen vonCalliphora erythrocephala Meigen. Biol Zbl 81:691–720Google Scholar
- Langer H (1964) Der Phosphatstoffwechsel des Facettenauges im Dunkeln und im Licht. Helgol Wiss Meeresunters 9:251–260Google Scholar
- Langer H, Lues I, Rivera ME (1976) Arginine phosphates in compound eyes. J Comp Physiol 107:179–184Google Scholar
- Laughlin B, Hardie RC (1978) Common strategies for light adaptation in the peripheral visual systems of fly and dragonfly. J Comp Physiol 128:319–340Google Scholar
- Minke B (1986) Photopigment-dependent adaptation in invertebrates — implications for vertebrates. In: Stieve H (ed) The molecular mechanism of photoreception. Dahlem Konferenzen. Springer, Berlin Heidelberg New York, pp 241–265Google Scholar
- Minke B, Tsacopoulos M (1986) Light induced sodium dependent accumulation of calcium and potassium in the extracellular space of bee retina. Vision Res 26:679–690Google Scholar
- Paulsen R, Bentrop J (1986) Light-modulated biochemical events in fly photoreceptors. Prog Zool 33:299–319Google Scholar
- Perrelet A (1970) The fine structure of the retina of the honeybee drone. Z Zellforsch Mikrosk Anat 108:530–562Google Scholar
- Prop FAJ (1954) A microrespirometer for simultaneous measurement of O2-consumption and CO2-production and its use in determining the respiratory quotient of tissue cultures. Exp Cell Res 7:303–317Google Scholar
- Razmjoo S, Hamdorf K (1980) In support of the ‘Photopigment model’ of vision in invertebrates. J Comp Physiol 135:209–215Google Scholar
- Schwemer J (1979) Molekulare Grundlagen der Photorezeption bei der SchmeißfliegeCalliphora erythrocephala Meig. Habilitationsschrift, BochumGoogle Scholar
- Schwemer J (1983) Pathways of visual pigment regeneration in fly photoreceptors. Biophys Struct Mech 9:287–298Google Scholar
- Schwemer J (1986) Turnover of photoreceptor membrane and visual pigment in invertebrates. In: Stieve H (ed) The molecular mechanism of photoreception. Dahlem Konferenzen. Springer, Berlin Heidelberg New York, pp 303–326Google Scholar
- Tinbergen J, Stavenga DG (1987) Spectral sensitivity of light induced respiratory activity of photoreceptor mitochondria in the intact fly. J Comp Physiol A 160:195–203Google Scholar
- Tsacopoulos M, Poitry S (1982) Kinetics of oxygen consumption after a single flash of light in photoreceptors of the drone (Apis mellifera). J Gen Physiol 80:19–55Google Scholar
- Tsacopoulos M, Poitry S, Borsellino A (1981) Diffusion and consumption of oxygen in the superfused retina of the drone (Apis mellifera) in darkness. J Gen Physiol 77:601–628Google Scholar
- Tsacopoulos M, Orkand RK, Coles JA, Levy S, Poitry S (1983) Oxygen uptake occurs faster than sodium pumping in bee retina after a light flash. Nature 301:604–605Google Scholar
- Tsacopoulos M, Fein A, Poitry S (1986) Stimulus-induced increase of mitochondrial respiration in a single neuron. Experientia 42:642Google Scholar
- Weber KM, Schorrath-Kuschewski G (1976) Nachweis und Verteilung kohlenhydrat-haltiger Verbindungen im Auge der SchmeißfliegeCalliphora vicina. Entomol Germanica 2:305–319Google Scholar