Light-harvesting chlorophyll pigments enable mammalian mitochondria to capture photonic energy and produce ATP
Chlorophyll-mediated energy capture in animal mitochondria Obtaining energy from the environment is fundamental to all forms of life, but only photosynthetic organisms are able to directly capture sunlight and convert it into biological energy as ATP, e.g. through light-absorbing chlorophyll molecules of plant chloroplasts. With their diet, animals take up chlorophyll, which is then converted into different metabolites that retain the ability to absorb light at wavelengths that can penetrate into animal tissues. But what are the consequences of light absorption by these metabolites? In this study, Ilyas Washington and colleagues address this question by assessing the function of chlorophyll metabolites in Caenorhabditis elegans and in mice. They find that addition of the light-capturing chlorophyll metabolite pyropheophorbide-a (P-a) to the animal diet leads to it entering the circulation and becoming enriched in mitochondria; there, it results in higher concentration of ATP when the animals are exposed to light. The authors also show that P-a extends the life span of C. elegans that are exposed to light. With regard to the molecular mechanism, the biochemical experiments performed here suggest that P-a modulates the mitochondrial ATP stores by catalysing the reduction of coenzyme Q – a slow step in ATP synthesis. Taken together, the data presented here suggest that, similarly to plants and photosynthetic organisms, animals also possess metabolic pathways to derive energy directly from sunlight.
Both increased sun exposure and the consumption of green vegetables are correlated with better overall health outcomes in a variety of diseases of aging. These benefits are commonly attributed to an increase in vitamin D from sunlight exposure and consumption of antioxidants from green vegetables. Our work suggests these explanations might be incomplete. Sunlight is the most abundant energy source on this planet. Throughout mammalian evolution, the internal organs of most animals, including humans, have been bathed in photonic energy from the sun. Do animals have metabolic pathways that enable them to take greater advantage of this abundant energy source?
The demonstration that:
(1) light-sensitive chlorophyll-type molecules are sequestered into animal tissues; (2) in the presence of the chlorophyll metabolite P-a, there is an increase in ATP in isolated animal mitochondria, tissue homogenates and in C. elegans, upon exposure to light of wavelengths absorbed by P-a; and (3) in the presence of P-a, light alters fundamental biology resulting in up to a 17% extension of life span in C. elegans
suggests that, similarly to plants and photosynthetic organisms, animals also possess metabolic pathways to derive energy directly from sunlight.
We show that dietary metabolites of chlorophyll can enter the circulation, are present in tissues, and can be enriched in the mitochondria. When incubated with a light-capturing metabolite of chlorophyll, isolated mammalian mitochondria and animal-derived tissues, have higher concentrations of ATP when exposed to light, compared with animal tissues not mixed with the metabolite. We demonstrate that the same metabolite increases ATP concentrations, and extends the median life span of Caenorhabditis elegans [worm], upon light exposure; supporting the hypothesis that photonic energy capture through dietary-derived metabolites may be an important means of energy regulation in animals. The presented data are consistent with the hypothesis that metabolites of dietary chlorophyll modulate mitochondrial ATP stores by catalyzing the reduction of coenzyme Q. These findings have implications for our understanding of aging, normal cell function and life on earth.