Classic story revised: lichens are fungus + algae + yeast (another fungus)

One of the classic stories of biology, taught to virtually every student, is the fact that what we call “lichens” are actually a combination of two very distantly related species: a species of alga and a species of fungus. (Sometimes the “alga” is really a species of cyanobacteria, formerly called “blue green algae” but not really algae.) It is offered as the paradigm of a true symbiosis, in which two species living together each provide something for the other. In the case of lichens, the alga provides the products of photosynthesis as nutrients, while the fungus provides structure, protection, nutrients, and moisture.  They’ve coevolved to the extent that while the algal partner can sometimes be found living freely on its own, the fungus is never found on its own. Finally, most (but not all) of the fungal partners in a lichen are ascomycetes (“sac fungi”)—a phylum in the fungal kingdom.

Lichens vary tremendously in their growth form depending on the partners; here are three examples taken from the Wikipedia article:

Well, this classic story has just been revised in a new online paper in Science by Toby Spribille et al. (reference below; free download). Spribille and his colleagues note that although this partnership has been described for decades, attempts to reconstruct a lichen in the lab by combining the fungal and algal partner always failed: researchers could simply not obtain the characteristic structure seen in nature. Their new paper gives an astounding result that may explain this failure: there’s a third partner in this symbiosis, and it’s yet another fungus—a yeast, which is a “basiodiomycete”, a different phylum that includes mushrooms and puffballs.

I’ll be brief.  Spribille et al. discovered the new partner when studying two lichens that looked very different (one produced an acid that made it yellow), but turned out to have the same algal and fungal partners. They were, in effect, the same species of lichen (though of course species delineation is tricky in this group). Why were they so different? They decided to study gene expression in the two forms using genes identified in ascomycetes and algae. No differences were found. But when they expanded their search to other types of fungi, they found that some basidiomycete genes were expressed in one form but not the other, even though no basidiomycetes were supposed to be there.

They then determined that other lichens also had a third basidiomycete partner, but one that differed among lichen “species”.  Although only 42 of the 56 sampled lichen genera had related basidiomycetes (indicating that the partnership may not be required in all lichens), they conclude that “basidiomycete fungi are ubiquitous and global associates of the world’s most speciose radiation of macrolichens.”

Finally, they visualized the cells, which was hard to do because they’re sparse and embedded in the lichen cortex (its skin). They finally managed to visualize the yeast cells, at first detected only by their gene transcripts, by “FISH” (fluorescent in situ hybridization) analysis: making RNA transcripts of the yeasts that hybridized to fluorescent molecules. And then they could see this:

Figure from paper. (A) B. fremontii, with (B) few FISH-hybridized live yeast cells at the level of the cortex. (C) B. tortuosa, with (D) abundant FISH-hybridized cortical yeast cells (scale bars, 20 μm).

The previous failure to detect the presence of another fungal partner may explain why scientists haven’t been able to synthesize lichens from their components: they were leaving out the third partner. 

And why wasn’t this partner detected before? The authors suggest that the genes in the new partner simply weren’t detected in the usual gene-sequencing procedures, which can be biased toward detecting genes present in greater numbers.

This shows that long-established stories can be drastically revised by new findings, and that the classic tale of this symbiosis may have to be revised a bit. It remains to be seen whether this new, third partner is actually required for the lichen to form, and, if so, if it really partakes in a symbiosis as well, giving stuff to its two partners and getting back from them. It could even be parasitic or neutral, or have a symbiosis with one of the two other partners and a different relationship with the other. To add the classic ending to scientific papers, “Much work remains to be done.”

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Spribille, T. et al.  2016. Basidiomycete yeasts in the cortex of ascomycete macrolichens. Science.  Published online 21 JUL 2016 DOI: 10.1126/science.aaf8287