Truffles and truffle-like fungi have always fascinated me. Unlike the vast majority of other higher fungi, true truffles and truffle-like fungi are hypogeous; carrying out the majority of their life cycle underground. For the species featured in today’s edition of Fungi Friday, this subterraneous ecology makes perfect sense. Given the demanding environments they make their home in, hypogeous fungi escape abiotic factors like low water availability and hot ambient temperatures that would otherwise halt fungal growth. This hypogeous adaptation alone would still not provide enough for Terfezia arenaria to succeed in these desert ecosystems. Additionally, they have evolved symbiotic relationships not only with plants, but with mammal dispersers and bacteria as well. Mutualisms on top of mutualisms ensure that desert truffle-like fungi produce enough spores to contribute to the next generation.
Although this genus is pretty new to me, these desert truffles have been consumed and traded by humans for thousands of years. There are records of truffles being a major trade commodity of Northern Africa during the Roman Empire. These fungi were shipped to Italy from Egypt and Libya by the boatload around 2,000 years ago! Even more interesting, it has been suggested that Terfezia arenaria and other desert truffles were the “manna” sent from God to the Israelites during the 40-year pilgrimage through the desert. Although I didn’t find much that could back up that claim, the distribution of these fungi lines up perfectly with the diaspora of Israelites during that time period.
Terfezia arenaria
One can find Terfezia arenaria across Northern Africa and the Iberian Peninsula in hot and dry dessert-like scrublands. They are easier to find after seasonal rains because their subterraneous bodies swell, and the sandy substrate at the surface mounds and cracks. These mounds may be quite difficult to find, but if one looks out for its primary plant host, you may increase your chances at locating them. The rockrose Helianthemum guttatum is the Moroccan desert truffle’s main plant symbiote.
Like other mycorrhizal relationships, these fungi provide the plant with rare nutrients like nitrogen and phosphorus, while the plant provides its fungus with some of the sugars synthesized through photosynthesis. However, unlike other mycorrhizal relationships, this particular symbiosis can switch from endomycorrhizal to ectomycorrhizal depending on how much available phosphorus there is in the sandy substrate.
A study in 1989 by Fortas and Chevalier showed that at high phosphate levels, ectomycorrhizae would form. In other words, plant roots would become ensheathed in hyphae when phosphorus was readily available. When phosphate was more limited, the hyphae of Terfezia arenaria would form endomycorrhizae; actually penetrating the root cells of its host plant. This is shocking to me! I’ve actually never come across this type of plasticity from both the plant and fungus involved in a mutualism. In every mycorrhizal interaction I’ve learned about prior to this, the plant AND fungus has always been either ecto, OR endomycorrhizal. The ability to shift the fundamental physiology of the mutualism depending on the amount of available nutrients is an incredible and rare adaptation that would only reveal itself these demanding environments.
The fruiting of these fungi is also timed with the maturation and seed formation of its main host plant. In late February, these mature plants produce and disperse seeds. If there is enough available water, this is when Terfezia arenaria likes to emerge from the sandy substrate and release its spores. By timing its spore release with the maturation of its host plant, the fungus has a better chance of colonizing new juvenile plants. As it cracks open the sandy surface above, its outer tissue will begin to break down, and spores will be blown away by wind. But when it comes to dispersal, that is not all. More research needs to be conducted, but several rodents have been observed foraging for these desert truffles. By utilizing both wind dispersal and mammalian dispersal, the chances of colonizing another rockrose increases drastically.
The third symbiosis involved in this incredible species again has to do with nutrient availability. Exudates from the closely related cousin Terfezia boudieri have been shown to promote the growth of the nitrogen fixing bacteria Azotobacter chroococcum, while inhibiting the growth of other, non-functioning bacteria. By promoting the growth of nitrogen fixing bacteria, more nitrogen can be delivered to the host plant, and the plant can synthesize more sugars to send back to the fungus.
A massive hypogeous dessert truffle.
It’s absolutely wild to me when I consider all of these adaptations that have occurred in these desert truffles. No matter what kingdom an organism comes from, if its evolution took place in desert ecosystems, there will always be profound ecological and physiological adaptations that enhance fitness in these demanding places. To escape the heat of the desert and the little available water, these fungi persist in a hypogeous state. To acquire enough carbohydrates to produce enough spores that will allow the continuation of its genetic lineage, it has paired up with the rockrose. To ensure enough nutrients are passed to its plant host, it produces exudates that promote the growth of nitrogen fixing bacteria. The transfer of materials in this ecological complex is possibly the most enthralling information I learned today with the actual mycorrhizal interface being extremely fine-tuned. The mycorrhizal plasticity of the plant and fungus is downright crazy, as the species can switch from endomycorrhizae to ectomycorrhizae depending on the nutrient availability. Today, I officially entered yet another species to my bucket list.