Despite the enormity of the planet we live on, there is an even bigger space for life to develop and exist right under our very noses. I’m not talking about the 4^th dimension or the faerie realm; I am talking about the phyllosphere. You see, microorganisms can live inside the leaves, stems, and roots of plants. Overall, the surface area of the phyllosphere is twice as large as the surface area of all land on earth (Zimmerman and Vitousek 2012). Humans have billions of bacteria living inside our bodies to help us live. Plants have this same relationship, but with microbial fungi! Within these plants lie a diversity of life that is a new frontier in science.

A picture of a Nematode. Most of them have a similar morphology.
http://enrichla.org/wp-content/uploads/2012/06/nematodes.jpg

As we start to look into this microcosm of life, we find that these fungi are far from dormant; many of these fungi play important symbiotic roles with the plants.  Nematodes are a soil microorganism found abundantly in most terrestrial soils. Although most of them survive by eating fungi, many of them are considered agricultural pests (Sikora et al. 2008). We have recently found several species of endophytic fungi that decrease the plant damage caused by nematodes (Sikora et al. 2008, Singh et al 2013). These recent studies have been proving the efficacy of using the beneficial endophytes as a natural biocontrol method for agriculture.

Endophytes get even cooler though. Since the discovery of endophytes, we have been looking at what roles they play in their plant hosts. What scientists are finding will surprise you. One scientist from Seattle has been looking at the endophytes that exist in plants that grow by hot springs. The soil in these environments can reach temperatures in excess of 100 degrees Fahrenheit, which is usually beyond the range at which most plants or fungi can survive (Tennesen, 2010). When the plant and its fungal partner are separated from each other, neither can survive in such extreme temperatures. So we know that this heat tolerance is an emergent property of the two species. That means that this trait only exists when the two different species are existing mutualistically. Dr. Rodriguez then took the endophyte from the extremely hot soil and inoculated a tomato plant with them. The tomato with the endophyte can now survive in soil temperatures over 140 degrees Fahrenheit. Later studied showed that this mutualism is actually a 3-way symbiosis (Rodriguez and Redman, 2008). For the endophyte to confer heat tolerance to the host plant, the endophyte needs to be infected with an RNA virus. Similar studies have looked at plants that live in coastal areas, where salt tolerance is something plants need to survive. For some species of plant, the salt tolerance is an emergent property of another fungal symbiosis (Rodriguez and Redman, 2008). The deeper we look into endophytes, the more complexity and interconnectedness we see.

I know this is completely mind blowing, but this rabbit hole keeps going. Are you ready to dive in? The same species of fungi that confers the heat or salt tolerance to the plants are found in other, low-stress environments. However, the endophytes that live in low-stress environments do not confer the same stress-tolerance that the high-stress endophytes do (Rodriguez and Redman, 2008). This means that the endophyte responds differently with its plant partner in different habitats. Basically, the fungus is helping the plant survive in whatever environment the symbiosis developed in. But wait, there’s more: the same species of fungi can be symbiotic, like we have been discussing, or it can be parasitic, depending on the plant species (Rodriguez and Redman, 2008). In some cases, like tomato plants, it can even come down to the variety of tomato. This is stumping scientists. What makes these endophytes choose mutualistic versus parasitic lifestyles? Dr. Rodriguez thinks it can come down to a single mutation.

During the last 5 massive extinctions that our planet has gone through, natural historians have noted an increase in fungal diversity immediately afterwards. Some environmental scientists theorize that we are going through the 6^th major extinction event right now. How are we going to survive this time of extreme change on our planet? Paul Stamets, A forefront mycologist of our times, says that the creatures that ally with fungi survive catastrophes. For generations entire societies have experienced mycophobia, the irrational fear of mushrooms. It is time to transcend the mindset of fear and learn to love fungi, the same way we love the beauty of orchids or the comfort of your domesticated cat. We now know about the symbiotic systems flourishing between plants and fungi. Imagine the kind of emergent properties we could experience once we embrace our fungal partners for the good of the world.

Bibliography

Rodriguez, R. and Redman, R (2008, 19 June). More than 400 million years of evolution and some plants still can’t make it on their own: plant stress tolerance via fungal symbiosis. Journal of Experimental Botany 59(5), 1109-1114.

Sikora, R.A., Et al (2008, July). Mutualistic endophytic fungi and in-planta suppressiveness to plant parasitic nematodes. Biological Control, 46(1), 15-23.

Singh, U.B. Et al (2013, January). Can endophytic Arthrobotrys oligospora modulate accumulation of defence related biomolecules and induced systemic resistance in tomato (Lycopersicon esculentum Mill.) against root knot disease caused by Meloidogyne incognita. Applied Soil Ecology 63, 45-56.

Tennessen, M. (2010, May). More Food From Fungi? Scientific American, 302(5), 27-28.

Zimmerman, N. B. and Vitousek, P.M. (2012, 12 June). Fungal endophyte communities reflect environmental structuring across a Hawaiian landscape. PNAS, 109(32), 13022-13027.

I’m sorry to say, but Science Fiction has lead us astray. Because of television shows like Stargate SG1 and characters like Teal’c (who carries a symbiote Goa’uld) many believe a symbiotic relationship is a relationship in which both parties involved benefit. Alas, this is not always true. In fact, symbiotic simply means a close, prolonged association between two or more different organisms of different species.

Source: http://www.yorku.ca/tnoel/march5/Symbiosis.html

There are actually five different types of symbiotic relationships: Parasitism, commensalism, mutualism, neutralism, and competition. Of these, parasitism and mutualism are the most common relationships formed by fungi.

Parasitism is when one species negatively affects the second species in the relationship. A tapeworm can live in a parasitic symbiotic relationship with a cow. The flea is a parasite on the dog. Corn smut, Ustilago maydis, is a prime example of fungal parasitism of corn.

Photos: Corn – Dieter Spears/iStockphoto.com. Corn Smut Spores – APS Press. Fake Facebook status created with www.statusclone.com

Ustilago maydis, creates tumor-like growths mixed within the kernels of corn on the stalk. This fungus turns a cheery yellow ear of corn into a deformed and grey mass.  These grey tumor-masses are actually kernels that have been infected by U. maydis and filled with teliospores (a type of reproductive cell). In all but central Mexico, this fungus is considered a bothersome disease, but there it is quite the culinary delicacy (The American Phytopathological Society, 2006).

Another example of a parasitic relationship is that of the genus Cordyceps (of which there are many species) and a poor insect host (E.B. Mains, 1958). In this most unfortunate relationship a spore will land in some fashion on a fly and germinate, then stromata (a visible clavate or sometimes branched structure coming out of insect body segments) will form outside of the body. These structures contain the sexual components of the fungi which will release spores when mature. Prior to the release of spores, a particular species in this family, Ophiocordyceps unilateralis, will use neurotoxins to control the movement of ants to climb to the highest part of a grass and bite down to hold on (Harry C. Evans, 2011). This allows the spores to eventually be released in the most prime conditions and location for eventual germination on another unsuspecting ant.

Things are much prettier on the mutualism side of things. The concept of mycorrhizal associations between a fungal partner and a plant partner is the mutualistic symbiosis most commonly referred to when talking about fungi.

Photos: Fir Seedling – Ingrid Barrentine, Northwest Guardian. Microscope Ectomycorrhizae – http://sciweb.nybg.org/science2/hcol/mycorrhizae2.asp.html Fake Facebook status created with www.statusclone.com

In a mycorrhizal partnership a fungal partner will take hold onto the roots of some plant partner and each side will benefit in some way from the association. For instance, the fungus growing around (or in some cases in) the roots of the plant allows for greater surface area of those roots. This greater surface area allows for greater access to water. The fungal partner also helps to shuttle certain nutrients into the plant’s roots (The New York Botanical Garden, 2003). In return, the plant shares some of the carbon created during photosynthesis.

A symbiotic relationship isn’t only a beneficial relationship for both partners. As described above in the fungal examples, there are different types of symbiotic relationships that aren’t positive at all. So before you write your sci-fi novel or television series scripts, be sure to remember these awesome fungi and take into account the diversity of symbiotic relationships and what they look like!

Sources:

The American Phytopathological Society. Common smut of corn. (2006). Retrieved from http://www.apsnet.org/edcenter/intropp/lessons/fungi/Basidiomycetes/Pages/CornSmut.aspx

The New York Botanical Garden. Hidden Partners: Mycorrhizal Fungi and Plants (2003). Retrieved from http://sciweb.nybg.org/science2/hcol/mycorrhizae2.asp.html

E. B. Mains. North American Entomogenous Species of Cordyceps. Mycologia , Vol. 50, No. 2 (Mar. – Apr., 1958) , pp. 169-222

Evans, H. C., Elliot, S., & Hughes, D. Hidden Diversity Behind the Zombie-Ant Fungus Ophiocordyceps unilateralis: Four New Species Described from Carpenter Ants in Minas Gerais, Brazil (March 2, 2011). Retrieved from http://www.plosone.org/article/info:doi/10.1371/journal.pone.0017024

Many people hear the word “fungi” and want to run the opposite direction – associating it with some nasty, toxic mess to stay far away from. I know because of the way people’s faces cringe to express their disgust when I tell them about the program I am enrolled in at my college titled “The Fungal Kingdom”. At this point I can just smile to myself knowing that there is so much these people don’t know about the fungi they are writing off as gross – that without them the world would look a whole lot different. Ever seen that cheesy film “A Day Without a Mexican” that shows how important immigrants from Mexico with actual work ethic are to this country, even though many complain about their presence? Well imagine what “A Day without Fungi” would look like – plants would die, delicious food sources would disappear, forest ecosystems would completely fall apart without any organisms capable of degrading wood, and many animals would have a much harder time digesting their food without the help of fungi in their gut – which is I’m going to talk about.

Chytridiomycota is a phylum of fungi that is widely dispersed globally, occurring in a diverse range of habitats “from the tropics to the arctic regions”. Chytrids can be found in aquatic systems, as plant parasites as well as vertebrate parasites like the infamous Batrachocytrium dendrobatidis responsible for the rapid decline of amphibian populations, but mostly occur in terrestrial habitats. The chytrid body – called the thallus – contains a sac-like structure called a sporangium that produces and stores zoospores (James et al., 2006). Zoospores can swim through aquatic environments using a posteriorly attached flagellum – similar to the sperm of a man that fertilizes an egg to impregnate a woman, zoospores are responsible for giving birth to new chytrids. Zoospores are capable of entering dormant states allowing them to stay alive in droughts and other harsh environments. There are five orders within the Chytridiomycota based on reproductive methods and the structure of zoospores. An especially interesting order, Neocallimastigales, occur as “anaerobic symbionts of the rumen” (James et al., 2006) as well as in intestines of other non-ruminant herbivores.

More often than not, when reading or learning about digestion in herbivores and specifically in ruminants, fungi are never mentioned – since mycology is a relatively new field of study, fungi are routinely left out of equations in which they are key players. As more and more people dive into the world of mycology, we are figuring out just how important fungi are, and finding them in places you might never think to look. All herbivores contain a spread of microflora in their gut to aid in their digestion, since high-fiber diets are very difficult to break down. Included in this gut microflora are the chytrids of Neocallimastigales. All herbivores ferment their food along their digestive tract. In ruminants – which include cows, sheep, goats, ox, deer, and more, fermentation takes place in the rumen – these animals are foregut fermenters, meaning their food is fermented before reaching the “true” stomach, allowing for more efficient digestion. To further explain, Merchen, Elizalde, and Drackly, 1997, write that “digestion by ruminants is the net result of a sequence of processes that occur in different segments of the gastrointestinal tract”. Primary fermentation of food takes place in the reticulo-rumen, then enzymes of host assist in acid hydrolysis and degreadation in the abomasums and small intestine, and lastly secondary fermentation is carried out in the cecum and large intestine (Merchen, et al., 1997).

In order to understand digestion in ruminants it is essential to also understand the microbial communities within these digestion sites. Anaerobic fungi live in areas of the digestive tract to aid in fermentation in ruminants as well as in the gut of non-ruminant herbivores along with bacteria and other microflora.

It’s hard to imagine how microorganisms such as these chytrids were discovered within the gut of animals considering they are tiny creatures living inside long, slimy, complex digestive tracts of select animals. DNA sequences were taken from feces of wild and domestic herbivores using a process called polymerase chain reaction to amplify specific gene strands. Through this sequencing, six genera were found within the Neocallimastigales – Neocallimastix, Piromyces, Orpinomyces, Anaeromyces, Caecomyces, and Cyllamyces – the most recently described genus (Nicholson, McSweeny, Mackie, Brookman, Theodorou, 2010). Species within Neocallimastigales have even been found in landfill sites, further enforcing their role as cellulose degraders (Lockhart et al., 2006). Without this technology it would be impossible to isolate these organisms or phylogenetically relate them to each other and other groups of fungi.

So we know that fungi are present in the gut of herbivores, but how do they actually help the animal? Like all members of Chytridiomycota, chytrids within the Neocallimastigales order reproduce asexually through motile zoospores with flagella, as mentioned earlier. These zoospores allow for “rapid colonisation of freshly ingested plant material” (p. 66 Nicholson et al., 2010) that enter the digestive tract of herbivores. The fungi then excrete fibrolytic enzymes – including cellulases, hemicellulases, proteases, and esterases, to help break down the plant material into three fatty acids – acetic acid, proprionic acid, and butyric acid – which are then used by the animal for energy. Don’t forget that bacteria and some protozoa are also important for this process!

So the next time you see some mold on your tangerine or are served some mushrooms you might think of as dirty and unappealing, remember how diverse fungi are and the key roles they serve in not only ecosystems around the world, but even in the digestive systems of many animals we know and love!

References

Brookman, J., Mackie, R., Mcsweeny, C., Nicholson, M., Theodorou, M. (2010). Diversity of anaerobic gut fungal populations analysed using ribosomal ITS1 sequences in faeces of wild and domesticated herbivores. ScienceDirect, Volume 16, issue 2. Retrieved from http://www.sciencedirect.com.bay.evergreen.edu/science/article/pii/S1075996409000833

James, T., Griffith, G., Letcher, P., Longcore, J., Mozley-Standridge, S., Porter, D., Powell, M, Vilgalys, R. (2006). A molecular phylogeny of flagellated fungi (Chtridiomycota) and description of a new phylum (Blastocladiomycota). Mycologia, 98. Retrieved from http://www.mycologia.org/content/98/6/860.full

Lockhart, R., Van Dyke, M., Beadle, I., Humphreys, P., McCarthy, A. (2006). Molecular Biological Detection of Anaerobic Gut Fungi from Landfill Sites. Applied and Environmental Microbiology, 72. Retrieved from http://aem.asm.org/content/72/8/5659.full

Merchen, N. R., Elizalde, J. C., Drackley, J. K., (1997). Journal of Animal Science. Current perspective on assessing site of digestion in ruminants, 75, 2223-2234.