Threesome: the hidden partner in lichen symbioses

Are you lichen that diversity? Many species can be easily found growing on rocks, as in this example from western USA

Are you lichen that diversity? Many species can be easily found growing on rocks, as in this example from western USA.
Photo by arbyreed (CC BY-NC-SA 2.0)

Groundbreaking new research has revised our understanding of one of the oldest symbiotic partnerships on Earth; scientists recently discover that lichens comprise more than just two mutually beneficial organisms. Almost 150 years ago, lichens became the most prominent example of symbiosis, a mutualism between an ascomycete fungus and a photosynthesising symbiont. The new study, published in Science last month, suggests a third partner has been lurking in the mix.

Most people know lichens as the epitome of nature’s classic symbiotic relationship, forming crusty growths on trees, rocks and rotting stumps, from tropical forests to icy cold tundra. Despite their rather odd appearance, lichens form a unique composite and are the dominant vegetation on as much as 8% of the Earth’s land surface1.

Filaments of the fungus provide structural support and environmental protection, while an alga or cyanobacterium provides food for its fungal home by photosynthesising – a relationship that benefits both individuals. Many variations exist on this theme, equating to the myriad of shapes and colours of lichen species around the world.

Letharia vulpina, one of many lichen species globally that houses yeast as a third symbiotic partner.

Letharia vulpina, one of many lichen species globally that houses yeast as a third symbiotic partner.
Photo by Franz Xaver (CC BY-SA 3.0)

However, in the study led by the University of Montana, lichen researchers used metatranscriptomics to show that there is more to the lichen symbiosis than meets the eye. As well as a fungal ‘mycobiont’ and a photosynthetic algal and/or cyanobacterial ‘photobiont’ partner, lichens also contain basidiomycete Cyphobasidium yeasts2. These are single-celled fungi that likely produce chemicals to help protect lichens against predators and harmful microbes. What’s more, these lichen-inhabiting Cyphobasidium lineages are to be recognised as an entirely new order – Cyphobasidiales.

The group’s data were checked many times to rule out contamination before confirming their remarkable result. As well as genes of the two known symbionts, some of the expressed genes they detected belonged to Basidiomycota fungi – the same phylum that includes your supermarket mushrooms. These Cyphobasidium yeasts are not at all related to the yeast used to brew beer or bake bread (which belong to the phylum Ascomycota).

Despite decades of molecular and microscopic studies, it is remarkable that basidiomycete yeasts have evaded detection in lichens until now. The discovery is therefore quite monumental. Lichens have been harbouring a partner we never knew existed, a secret partner whose occurrence may unravel several previously unexplained mysteries about lichens and their remarkable forms.

Take Bryoria fremontii and B. tortuosa, two lichen species found in Missoula, for example. Both lichens were thought to share the same symbiotic partners, yet the former is brown and innocuous, while the latter is yellow and poisonous. Sophisticated genetic techniques revealed that instead of minute genetic differences between their algal partners, a fungus from a completely different phylum was responsible for this variation3. The fungus coats the other members of its triad with noxious acids that deter infections and predation. Has a missing piece of the lichen puzzle been found?

The chemically-unique species group of Bryoria fremontii (left), with reddish-brown hue, and B. tortuosa (right), which has a yellow-brown hue.

The chemically-unique species group of Bryoria fremontii (left), with reddish-brown hue, and B. tortuosa (right), which has a yellow-brown hue. These two species have been distinguished for 90 years by the thallus-wide production of the pulvinic acid derivative vulpinic acid, which causes a yellow-ish appearance. Recent analyses show the two lichens have a differential abundance of Cyphobasidiales yeasts. Scale = 2 mm.
Figure from Velmala et al. (2009), used with permission.

Following this discovery in Bryoria, the group screened for the presence of Cyphobasidium in other major lichen groups. Further analyses of 56 different lichens from around the world’s six continents revealed that each lichen has its own specific association with a different basidiomycete yeast. This textbook-rewriting discovery may help to explain why lichenologists have largely failed to re-create lichen partnerships in the lab. Although we may be entering a new era in lichen research, the conclusion seems to be that there is a great deal more work to be done…!

References

1. Purvis W. (2000) Lichens. London, UK: The Natural History Museum.

2. Spribille T, Tuovinen V, Resl P, Vanderpool D, Wolinski H, Aime MC, Schneider K, Stabentheiner E, Toome-Heller M, Thor G, Mayrhofer H, Johannesson H and McCutcheon JP (2016) Basidiomycete yeasts in the cortex of ascomycete macrolichens. Science 353 (6298): 488–492.

3. Velmala S, Myllys L, Halonen P, Goward T and Ahti T (2009) Molecular data show that Bryoria fremontii and B. tortuosa (Parmeliaceae) are conspecific. The Lichenologist 41 (3): 231–242.

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