Light-harvesting chlorophyll pigments enable mammalian mitochondria to capture photonic energy and produce ATP
ABSTRACT
Sunlight is the most abundant energy source on this planet. However, the ability to convert sunlight into biological energy in the form of adenosine-5′-triphosphate (ATP) is thought to be limited to chlorophyll-containing chloroplasts in photosynthetic organisms.
Here we show that mammalian mitochondria can also capture light and synthesize ATP when mixed with a light-capturing metabolite of chlorophyll. The same metabolite fed to the worm Caenorhabditis elegans leads to increase in ATP synthesis upon light exposure, along with an increase in life span.
We further demonstrate the same potential to convert light into energy exists in mammals, as chlorophyll metabolites accumulate in mice, rats and swine when fed a chlorophyll-rich diet. Results suggest chlorophyll type molecules modulate mitochondrial ATP by catalyzing the reduction of coenzyme Q, a slow step in mitochondrial ATP synthesis.
We propose that through consumption of plant chlorophyll pigments, animals, too, are able to derive energy directly from sunlight.
INTRODUCTION
Determining how organisms obtain energy from the environment is fundamental to our understanding of life. In nearly all organisms, energy is stored and transported as adenosine-5′-triphosphate (ATP). In animals, the vast majority of ATP is synthesized in the mitochondria through respiration, a catabolic process. However, plants have co-evolved endosymbiotically to produce chloroplasts, which synthesize light-absorbing chlorophyll molecules that can capture light to use as energy for ATP synthesis. Many animals consume this light-absorbing chlorophyll through their diet. Inside the body, chlorophyll is converted into a variety of metabolites (Ferruzzi and Blakeslee, 2007; Ma and Dolphin, 1999) that retain the ability to absorb light in the visible spectrum at wavelengths that can penetrate into animal tissues. We sought to elucidate the consequences of light absorption by these potential dietary metabolites. 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, 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.
Conclusion
Both increased sun exposure (Dhar and Lambert, 2013; John et al., 2004; Kent et al., 2013a; Kent et al., 2013b; Levandovski et al., 2013) and the consumption of green vegetables (Block et al., 1992; Ferruzzi and Blakeslee, 2007; van't Veer et al., 2000) 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. Additional studies should confirm these conclusions.
