Inner Nature: Photosynthetic and light-harvesting animals

By Vidya Rajan, Columnist, The Times

Photosynthesis – a term that pretty much everyone understands – uses sunlight, carbon dioxide, water, and the light-harvesting green molecule, chlorophyll, to make sugars and release oxygen. Photosynthesis is carried out by free-living cyanobacteria, as well as plants and algae which contain chloroplasts, which are really just internal cyanobacteria, inside their cells. There are also a few animals that carry out photosynthesis, and this is the story of how they came about.

Around 2 billion years ago, a class of bacteria called cyanobacteria were doing photosynthesis (which releases oxygen). But oxygen is very reactive and inimical to life. Cyanobacteria threw out the oxygen and managed its toxic effects, but a class of bacteria called purple-sulfur bacteria[1] went one step further and began to actively use the oxygen released by cyanobacteria in their metabolic pathways to break down organic molecules. So, as cyanobacteria made sugar and oxygen from water and carbon dioxide and the sun’s energy, and purple-sulfur bacteria broke down sugar with oxygen to release water and carbon dioxide and released a lot of energy. This is how oxygen became an integral part of the chemical process for breaking down sugars quickly and efficiently. But there were still a group of bacteria called “archaebacteria” which were being slowly poisoned by the oxygen and luckily, around 1.5 billion years ago, one engulfed purple sulfur bacteria in a singular event to make of the greatest partnerships ever seen. The archaebacterium and purple-sulfur bacterium united into a single cell and the greatest partnership ever was the eukaryote.

Eukaryotes diverged into three groups – animals, fungi and algae. Animals and fungi are heterotrophic and generally require organic molecules, whereas algae are autotrophic, and can make organic molecules from carbon dioxide, water and sunlight. Oddities also exist: Some single-celled animals called protozoa are mixotrophic, that is able to live both as food-eating or photosynthetic organisms, depending on access to light. Clams and corals are symbiotic with photosynthetic algae to obtain food from sunlight, but this partnership is reversible. When water temperatures rise, the algae eject, causing what is called a “bleaching” event.

But true partnerships would require both partners to go down with the ship, so to speak.[3] Chloroplasts are fairly common among a class of marine molluscs called ‘saccoglossans’ or sea slugs, which were first described in the 1800s, but the presence of chloroplasts in the slugs was only noticed in the 1960s. These slugs are short-lived (about 10 months) and feed on an algae. Unusually, instead of digesting all the plant material, the slug extracts living chloroplasts from its food and inserts them into the gut lining. Because it is a thin and transparent animal, light can still penetrate its body, and the chloroplasts function to pump sugar directly into the slug. This process of stealing chloroplasts is called “’kleptoplasty’ (klepto=steal; plastid=type of cellular organelle). The plastids die with the slug rather than being passed on into its eggs; that is, each new generation of slug has to acquire its own kleptoplasts. Some genera of slugs capable of this process are Elysia, Plakobranchus, Costasiella, Thuridilla, Alderia, Lobiger, and Oxynoe. Each slug eats a specific alga from which it obtains its chloroplasts. Given sunlight, this slug is now capable of generating all the food it needs from photosynthesis. Fun fact: these animals are also hermaphrodites, capable of making both eggs and sperm, although they do not self-fertilize. (Mating is a vicious process in nudibranchs. For more information, see Reference [4].)

Surprises do not stop there. Another macroscopic animals which behaves like the saccoglossan is the spotted salamander (c maculatum). The scientific name was conferred by Johann Jakob von Tschudi, but he may have been dyslexic, because he actually meant the genus to be Amblystoma: in Greek amblus means ‘dull’ whereas amby means “cup”; Johann probably intended to say “blunt mouth” rather than “cup mouth”. Anyway, these animals are anything but dull. These salamanders harbor algae inside their cells which position themselves near mitochondria. The algae do photosynthesis, and the mitochondria quickly consume the oxygen and break down the sugars the algae produce, and release energy. The biggest surprise though, was when Canadian researcher Ryan Kerney was examining eggs of the salamander and noticed algae inside them![6] These salamanders were seeding the cells of the next generation with their own photosynthetic algae! This symbiosis has since been studied to learn how the salamander’s immune system spares the algae and how the stable genetic and physiological incorporation of a new organelle has been achieved.

The oriental hornet and pea aphid also show sensitivity to light, but this ability is intrinsic rather than being conferred by algae-turned-chloroplasts.[7] Both these animals have light harvesting pigments in their bodies. The pea aphid, Acyrthosiphon pisum, is unique among animals for the ability to synthesize carotenoids (which are also used in animal eyes for vision, but they have to be obtained from food) and move them to their cuticle, the outer body layer.[8] Here, it appears that the carotenoids absorb sunlight, because orange aphids showed higher levels of the energy molecule ATP than white ones. Nancy Moran of Yale University in Connecticut who discovered that these animals have genes for carotenoid production is not convinced of the use of carotenoids for photosynthesis, because these are plant-sucking animals which get plenty of sugar. But they may be a battery backup for when sugars are not available. The jury is still out.

Then there is the oriental hornet, Vespa orientalis. Animals which fluoresce under UV light were known and V. orientalis is one of them. In 1977 Jacob Ishay and team investigated their light-related properties and noticed a photoelectric effect[9] (the effect that Einstein explained which won his one and only Nobel Prize.) That is, in the presence of light, a measurable current developed. The molecule that absorbed the light was identified as xanthoperin. This yellow molecule is present in the yellow band of the abdomen but is more abundant in workers than in drones or queens, with Ishay and team inferring that it was related to activities workers, but not drones or queens did, such as digging and flight.[10]^,[11] A solar cell made using xanthoperin showed its ability to harvest solar energy as being weak but present, and it is surmised to provide a little additional energy to the hornets. Liver-enzyme activity was also affected by shining a light and independent metabolic links to liver-enzyme activity and energy production and usage are noted. Not much else is yet known.

Lots of animals have yellow bands or fluoresce under UV. Is it time to shine a light on them?

 

References:

[1]. The metabolic pathways of photosynthesis and respiration are very similar but run in opposite directions, so the pathways have many similarities. The reaction for photosynthesis is: 6CO2 + 6H2O + 2 photons  C6H12O6 + 6O2; for respiration it is C6H12O6 + 6O2  6CO2 + 6H2O + ~32 ATP. ATP is the energy molecule used in all living organisms. Thus each photon accounts for about 16 ATP.

[2]. Nature.com. (2014). The origin of mitochondria and chloroplasts | Learn Science at Scitable. [online] Available at: https://www.nature.com/scitable/content/the-origin-of-mitochondria-and-chloroplasts-14747702/

[3]. Rybak, S. (2013). 4 Incredible Photosynthetic Animals. [online] Uloop. Available at: https://www.uloop.com/news/view.php/77109/4-incredible-photosynthetic-animals

[4]. BBC Earth. The Mating Game: Meet the Penis-fencing Flatworm. https://youtu.be/czOIoDbkKQc?si=2j_FVXcfHYLhSlSS

[5]. Wikipedia. (2022). Elysia chlorotica. [online] Available at: https://en.wikipedia.org/wiki/Elysia_chlorotica

[6]. Kerney, R., Kim, E., Hangarter, R.P., Heiss, A.A., Bishop, C.D. and Hall, B.K. (2011). Intracellular invasion of green algae in a salamander host. Proceedings of the National Academy of Sciences, [online] 108(16), pp.6497–6502. doi:https://doi.org/10.1073/pnas.1018259108

[7]. Garreth (2022). 4 Animals that Photosynthesize (A to Z List & Pictures) – Fauna Facts. [online] Faunafacts.com. Available at: https://faunafacts.com/examples-of-animals-that-photosynthesize/https://faunafacts.com/examples-of-animals-that-photosynthesize/

[8]. Lougheed, K. (2012). Photosynthesis-like process found in insects. Nature. doi:https://doi.org/10.1038/nature.2012.11214

[9]. Ishay, J.S., Croitoru, N. Photoelectric properties of the ‘yellow strips’ of social wasps. Experientia 34, 340–342 (1978). https://doi.org/10.1007/BF01923023

[10]. Ishay, J.S. (2004). Hornet flight is generated by solar energy: UV irradiation counteracts anaesthetic effects. Journal of electron microscopy, [online] 53(6), pp.623–33. doi:https://doi.org/10.1093/jmicro/dfh077

[11]. Plotkin, M., Hod, I., Zaban, A., Boden, S.A., Bagnall, D.M., Galushko, D. and Bergman, D.J., 2010. Solar energy harvesting in the epicuticle of the oriental hornet (Vespa orientalis). Naturwissenschaften, 97, pp.1067-1076. DOI 10.1007/s00114-010-0728-1