Fungi that live off radiation

Some of you may have already read this on BoingBoing or /., but if you haven't, here's the big news: there is now evidence that fungi may be able to obtain metabolic energy from ionizing radiation. By ionizing radiation I don't mean that stuff that we see as light, and that plants use to obtian energy through photosynthesis; I mean nuclear radiation. As in, the stuff that kills you (e.g., what Caesium 137 emits). This is cool.

The study (Dadachova et al. 2007) was published in PLoS One, meaning that it's completely open access. So, while I'll summarize a few of the biological details here, if you want all the nitty gritty, head over there and read away.

The researchers started their search by noticing that fungi growing in radiation-intense environments (e.g., around the Chernobyl reactor) tended to have extremely high levels of melanin in their cells (yes, the same type of pigment that humans have in their skin). While this melanin has been hypothesized to function in a protective role (by absorbing radiation and dealing with the free radicals that are produced), the researchers wondered if the fungi might be able to use melanin, and the high-energy electrons it produces, for more than just protection.

To start, Dadachova et al. did a number of biochemical experiments: they showed that the fungal species they were working with (Cryptococcocus neoformans, Cladosporium sphaerospermum, and Wangiella dermatitidis) expressed melanin, analyzed the fungal melanin via HPLC and ESR, and determined that melanin exposed to radiation could speed up other oxidation reduction reactions (i.e, that radiation could affect the metabolic reactions of the cell). To show that melanin could affect oxidation reduction reactions, Dadachova et al. isolated melanin from fungal cells, mixed it with NADH and ferricyanide, and then showed that the rate of the NADH\ferricyanide oxidation reduction reaction increased when the solution was exposed to radiation. While Dadachova et al. state that the mechanism by which radiation energy is absorbed by melanin and transfered to biochemical reactions is unknown, based on their work it sounds like what might be going on is that melanin is eventually reducing NAD to NADH. This would be elegantly simple metabolically, as one of the primary products of the Krebs cycle (i.e., the cycle in fungi that metabolizes sugar) is NADH; NADH from the Krebs cycle is then used to power the electron transport chain, which ends up producing ATP. So, if melanin was reducing NAD to NADH using energy from radiation, it would be extremely simple to turn that NADH into usable ATP¹.

Dadachova et al. were able to obtain a mutant strain of C. neoformans [Lac(-)] that was unable to produce melanin. Thus, to test the hypothesis that melanin is the pigment that absorbs radiation, and that this radiation absorption provides useful energy, Dadachova et al. grew both melanin-producing and non-melanin-producing C. neoformans in either irradiated or non-irradiated conditions². The results are below:


Growth of normal C. neoformans (left) or non-melanin-producing C. neoformans (right) in either irradiated or non-irradiated conditions. Modified from figure 6 of Dadachova et al. (2007).
This is exactly what we'd expect to see if melanin was providing energy for growth: the melanin-producing fungi grew faster when exposed to radiation (the red bar in the left graph), but when the fungi were unable to produce melanin, there was not much of a difference between the irradiated and non-irradiated fungal growth (right graph).

Dadachova et al. were able to do essentially the same experiment with another species of fungus, W. dermatitidis, which they were also able to obtain a non-melanin-producing mutant of. Again, the results show that the fungi grew better when exposed to radiation:


Growth of normal W. dermatitidis (left) or non-melanin-producing W. dermatitidis (right) in either irradiated or non-irradiated conditions. Modified from figure 8 of Dadachova et al. (2007).
One thing to note here is that radiation does not appear to be required for these fungi to live; the mutant strains that don't produce melanin (and thus presumably cannot use this energy-gathering pathway) still grew, and the fungi that did produce melanin were able to grow even in the absence of extra radiation. Thus, this mechanism is not directly analogous to plant photosynthesis (as photosynthesis is typically the sole mechanism by which plants obtain energy, while radiation is not the sole energy source for these fungi).

When we think of organisms growing based on electromagnetic radiation, we think of plants, which get energy from light and carbon from carbon dioxide. Plants use the energy they get from light to take carbon dioxide from the atmosphere and assemble it into sugars (which nicely store the energy they've captured from light in a chemical form). Plants are therefore known as photoautotrophs (photo: getting energy from light; autotroph: obtaining carbon from an inorganic source, such as carbon dioxide). Animals, along with fungi and many other non-photosynthesizers, typically get their energy from organic molecules (i.e, sugar, fat, protein), and their carbon from those same organic molecules. Thus, animals and fungi are known as chemoheterotrophs.

A question with these radiation-using fungi follows: are these fungi fixing carbon dioxide from the atmosphere, like plants, or are they getting carbon from organic molecules, like most other fungi do? In other words, are these fungi heterotrophs (like most other fungi) or autotrophs (like plants)? To partially test this, the researchers added acetate (an organic form of carbon) to the fungal growth medium, and labeled that acetate with carbon-14. They then exposed both the normal fungi and the non-melanin-producing fungi to radiation, and observed that the normal fungi incorporated significantly more carbon-14-labeled acetate into their cells when they were exposed to radiation. Since the fungi were absorbing the acetate at higher rates when exposed to radiation, it seems as though the fungi are still using heterotrophic mechanisms of carbon uptake (i.e., they're not autotrophs, though note that they didn't directly test for absorption of carbon dioxide).

So, as Dadachova et al. say in their discussion,

[W]e cautiously suggest that the ability of melanin to capture electromagnetic radiation combined with its remarkable oxidation-reduction properties may confer upon melanotic organisms the ability to harness radiation for metabolic energy. The enhanced growth of melanotic fungi in conditions of radiation fluxes suggests the need for additional investigation to ascertain the mechanism for this effect.

Looks like it's time to go add another line to that "sources of energy for growth" slide in my lecture.

¹ Note that this is pure speculation on my part, and I'm most certainly not a biochemist.
² For the irradiated growth conditions, Dadachova et al. exposed the fungi "to a radiation field of 0.05 mGy/hr created by ¹⁸⁸Re/¹⁸⁸W isotope generator".

Dadachova E., RA Bryan, X Huang, T Moadel, AD Schweitzer, P Aisen, JD Nosanchuk, and A Casadevall. 2007. Ionizing Radiation Changes the Electronic Properties of Melanin and Enhances the Growth of Melanized Fungi. PLoS ONE 2(5): e457. doi:10.1371/journal.pone.0000457. Full-text.