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Light- induced electron transfer and ATP synthesis in a carotene synthesizing insect.

Valmalette JC, Dombrovsky A, Brat P, Mertz C, Capovilla M, Robichon A - Sci Rep (2012)

Bottom Line: We report here that the capture of light energy in living aphids results in the photo induced electron transfer from excited chromophores to acceptor molecules.The redox potentials of molecules involved in this process would be compatible with the reduction of the NAD+ coenzyme.This appears as an archaic photosynthetic system consisting of photo-emitted electrons that are in fine funnelled into the mitochondrial reducing power in order to synthesize ATP molecules.

View Article: PubMed Central - PubMed

Affiliation: IM2NP UMR 7334 CNRS, Université du Sud Toulon Var, P.O. Box 20132, 83957 La Garde CEDEX, France.

ABSTRACT
A singular adaptive phenotype of a parthenogenetic insect species (Acyrthosiphon pisum) was selected in cold conditions and is characterized by a remarkable apparition of a greenish colour. The aphid pigments involve carotenoid genes well defined in chloroplasts and cyanobacteria and amazingly present in the aphid genome, likely by lateral transfer during evolution. The abundant carotenoid synthesis in aphids suggests strongly that a major and unknown physiological role is related to these compounds beyond their canonical anti-oxidant properties. We report here that the capture of light energy in living aphids results in the photo induced electron transfer from excited chromophores to acceptor molecules. The redox potentials of molecules involved in this process would be compatible with the reduction of the NAD+ coenzyme. This appears as an archaic photosynthetic system consisting of photo-emitted electrons that are in fine funnelled into the mitochondrial reducing power in order to synthesize ATP molecules.

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NAD+/NADH balance in cytosol and particulate (mitochondria) fractions in dark- and light-conditioned aphids.The dosage was performed with orange (A) and white (B) aphids conditioned in light or dark using methyphenylsulfonate and tetrazolium salts (see Methods). Briefly, 50 adult aphids (orange and white phenotypes), kept in dark for three days or alternatively kept in light photoperiodicity (18/6 hours), were grinded and assayed for the NAD+/NADH balance. The experiments were repeated three times. Bars are the mean +/− S.E. **P<0.005. The Raman imaging between 0 to 100 µm in depth was performed and shows a double layer structure of carotenoid compounds (C). A control carotene signature in Raman imaging corresponding to the analysis in (C) is shown in (D).
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f7: NAD+/NADH balance in cytosol and particulate (mitochondria) fractions in dark- and light-conditioned aphids.The dosage was performed with orange (A) and white (B) aphids conditioned in light or dark using methyphenylsulfonate and tetrazolium salts (see Methods). Briefly, 50 adult aphids (orange and white phenotypes), kept in dark for three days or alternatively kept in light photoperiodicity (18/6 hours), were grinded and assayed for the NAD+/NADH balance. The experiments were repeated three times. Bars are the mean +/− S.E. **P<0.005. The Raman imaging between 0 to 100 µm in depth was performed and shows a double layer structure of carotenoid compounds (C). A control carotene signature in Raman imaging corresponding to the analysis in (C) is shown in (D).

Mentions: Finally the balance NAD+/NADH was measured in the light versus dark context. A series of experiments shows unambiguously a significant increase of the reduced co-enzyme level in particulate fraction enriched in mitochondria when the orange aphids are exposed to light (figure 7). Intriguingly, a drastic decrease in NAD+ (oxidized) concentration was found in the soluble fraction of the extract when the orange aphids were maintained in dark, suggesting that its synthesis is partly controlled by light. By contrast and as expected, the white aphid variants display weak levels of NAD+/NADH, which seem little affected by light (figure 7). Together these data reinforce the hypothesis that light, through biological membranes enriched in pigments, triggers a reducing power that in fine is captured by co-enzymes like NAD+. This reduced co-enzyme is known to transit inside mitochondria through a shuttle mechanism and deliver electrons for the respiratory chain machinery ending with the H+ inflow-driven ATP synthesis131415. Amazingly, we observe that carotene molecules are disposed as a bilayer under the cuticule from 0 to 40 µM in depth, suggesting that this structure might present an optimal efficiency to harvest light energy (figure 7).


Light- induced electron transfer and ATP synthesis in a carotene synthesizing insect.

Valmalette JC, Dombrovsky A, Brat P, Mertz C, Capovilla M, Robichon A - Sci Rep (2012)

NAD+/NADH balance in cytosol and particulate (mitochondria) fractions in dark- and light-conditioned aphids.The dosage was performed with orange (A) and white (B) aphids conditioned in light or dark using methyphenylsulfonate and tetrazolium salts (see Methods). Briefly, 50 adult aphids (orange and white phenotypes), kept in dark for three days or alternatively kept in light photoperiodicity (18/6 hours), were grinded and assayed for the NAD+/NADH balance. The experiments were repeated three times. Bars are the mean +/− S.E. **P<0.005. The Raman imaging between 0 to 100 µm in depth was performed and shows a double layer structure of carotenoid compounds (C). A control carotene signature in Raman imaging corresponding to the analysis in (C) is shown in (D).
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC3420219&req=5

f7: NAD+/NADH balance in cytosol and particulate (mitochondria) fractions in dark- and light-conditioned aphids.The dosage was performed with orange (A) and white (B) aphids conditioned in light or dark using methyphenylsulfonate and tetrazolium salts (see Methods). Briefly, 50 adult aphids (orange and white phenotypes), kept in dark for three days or alternatively kept in light photoperiodicity (18/6 hours), were grinded and assayed for the NAD+/NADH balance. The experiments were repeated three times. Bars are the mean +/− S.E. **P<0.005. The Raman imaging between 0 to 100 µm in depth was performed and shows a double layer structure of carotenoid compounds (C). A control carotene signature in Raman imaging corresponding to the analysis in (C) is shown in (D).
Mentions: Finally the balance NAD+/NADH was measured in the light versus dark context. A series of experiments shows unambiguously a significant increase of the reduced co-enzyme level in particulate fraction enriched in mitochondria when the orange aphids are exposed to light (figure 7). Intriguingly, a drastic decrease in NAD+ (oxidized) concentration was found in the soluble fraction of the extract when the orange aphids were maintained in dark, suggesting that its synthesis is partly controlled by light. By contrast and as expected, the white aphid variants display weak levels of NAD+/NADH, which seem little affected by light (figure 7). Together these data reinforce the hypothesis that light, through biological membranes enriched in pigments, triggers a reducing power that in fine is captured by co-enzymes like NAD+. This reduced co-enzyme is known to transit inside mitochondria through a shuttle mechanism and deliver electrons for the respiratory chain machinery ending with the H+ inflow-driven ATP synthesis131415. Amazingly, we observe that carotene molecules are disposed as a bilayer under the cuticule from 0 to 40 µM in depth, suggesting that this structure might present an optimal efficiency to harvest light energy (figure 7).

Bottom Line: We report here that the capture of light energy in living aphids results in the photo induced electron transfer from excited chromophores to acceptor molecules.The redox potentials of molecules involved in this process would be compatible with the reduction of the NAD+ coenzyme.This appears as an archaic photosynthetic system consisting of photo-emitted electrons that are in fine funnelled into the mitochondrial reducing power in order to synthesize ATP molecules.

View Article: PubMed Central - PubMed

Affiliation: IM2NP UMR 7334 CNRS, Université du Sud Toulon Var, P.O. Box 20132, 83957 La Garde CEDEX, France.

ABSTRACT
A singular adaptive phenotype of a parthenogenetic insect species (Acyrthosiphon pisum) was selected in cold conditions and is characterized by a remarkable apparition of a greenish colour. The aphid pigments involve carotenoid genes well defined in chloroplasts and cyanobacteria and amazingly present in the aphid genome, likely by lateral transfer during evolution. The abundant carotenoid synthesis in aphids suggests strongly that a major and unknown physiological role is related to these compounds beyond their canonical anti-oxidant properties. We report here that the capture of light energy in living aphids results in the photo induced electron transfer from excited chromophores to acceptor molecules. The redox potentials of molecules involved in this process would be compatible with the reduction of the NAD+ coenzyme. This appears as an archaic photosynthetic system consisting of photo-emitted electrons that are in fine funnelled into the mitochondrial reducing power in order to synthesize ATP molecules.

Show MeSH
Related in: MedlinePlus