All for One, and One for All!

by Mark Martin
 

Panic grass growing well at a soil tem­perature of over 50 °C (123 °F). Source

When I recently attended the 6th International Symbiosis Society Congress in Madison, Wisconsin, I was awed by the fascinating forms that symbiotic relationships take among diverse organisms. One talk that particularly in­trigued me was from the laboratory of Marilyn Roossinck of the Samuel Roberts Nobel Foundation in Oklahoma, which described the mutualistic relationship between a virus, an endophytic fungus, a monocot, and elevated temperatures in geothermal soils. It also made me con­sider how readily we seem to associate the word "virus" with pathogenic associations, when nature is often far more subtle when it comes to mutualistic partnerships.
 

The story began in 2002 when it was found that a type of grass growing in the geothermal zones of Yellowstone National Park – panic grass, Dichanthelium lanuginosum – was able to survive intermittent high temperatures in geothermal soils (up to 65°C.) due to its association with an endophytic fungus, Curvularia protuberata. The fun­gus is essential to the plant's ability to tolerate tempera­tures that are lethal to the non-colonized plant. Panic grass, incidentally, has nothing to do with botanical phobias; instead, the name derives from the Latin panicum, referring to foxtail millet.
 
 
 
 
 
 

The thermal areas of Yellowstone Nation­al Park are home to thermotolerant mi­crobes, and even a few macrobes! Source

Endophytic fungi are quite common among plants and have been implicated in a number of mutualistic associa­tions that display enhanced stress tolerance. But the story was far stranger than this. It turns out that the "thermal tolerance" trait conferred by the endophytic fungus is actually due to a specific RNA virus onboard. (See the 2007 report in Science.) This dsRNA virus is aptly named "Curvularia thermal tolerance virus" (CThTV). In­fected fungal mycelia contain two viral dsRNA molecules: a 2.2 kb dsRNA molecule that encodes two ORFs related to viral replication and a 1.8 kb dsRNA molecule with two ORFs with no similarity to any protein of known function.
 

It has long been known that viruses can modulate the ability of a fungus to interact pathogenically with a host organism, but this is the first report showing a clear-cut mutualistic interplay. Isolates of C. protuberata "cured" of CThTV by freeze-thaw and desiccation cycles conferred no thermal tolerance on the host plant; re-infection of the virus-free fungus with CThTV restored its ability to confer thermal tolerance to the panic grass.
 
 
 

Panic grass phenotype after laboratory testing of thermotolerance (soil tem­pe­rature cycling between 65°C for ten hours a day and 37°C for fourteen hours a day, for two weeks). Legend: Wt = plant infected with virus-bearing fungi. An = plant infected with previously "cured" fungi carrying reintroduced virus. VF = plant infected with virus-free fungi. NS = plant not infected by fungi. Source

The Roossinck group went on to show that C. protube­ra­ta carrying CThTV could colonize eudicots such as toma­to, and even provide some thermal tolerance to the new host plant. However, colonization was not as extensive and the thermal tolerance was not as pronounced as with panic grass. As one might guess, work is continuing to determine the mechanism by which the uncharac­ter­ized ORFs within the 1.8 dsRNA of CThTV confer the ther­mal tolerance in this fungal-plant mutualism.
 

This kind of fungal-conferred stress tolerance may be much more that a rare oddity. In fact, there is some evidence that the ability of fungi (with or without viral modification) to increase stress tolerance is fairly com­mon, and evolutionarily ancient. The existence of mul­tiple "partners" involved in a mutualism has been de­scribed for ants, leeches, and many other associations. This relationship between Dichanthelium lanuginosum, Curvularia protuberata, and CThTV is reminiscent of the interrelationships between bacteriophage, Wolbachia, and insects described here.
 

Clearly, in what appears to be a warming world, understanding how plants can tolerate and prosper at elevated temperatures is an intriguing topic. To a "symbiophile" like myself, learning that the plant has a fungal partner, and that the fungal partner has a viral passenger – and all are working together in a finely tuned mutualistic dance – is a hot topic indeed!
 

Reference
Marquez, L., Redman, R., Rodriguez, R., & Roossinck, M. (2007). A Virus in a Fungus in a Plant: Three-Way Symbiosis Required for Thermal Tolerance Science, 315 (5811), 513–515. DOI 10.1126/science.1136237

 
 

 

Mark is associate professor in the Department of Biology, University of Puget Sound, an Associate Blogger for STC, and a passionate advocate for the Small Things.

 
 

 
 

Comments

[Mark O. Martin]

Nice comments from all! My first attempt to reply was eaten with gusto by my web browser crashing. So here I go again:

1. First, this entire discussion reminds me of the following:

“So naturalists observe, a flea
Has smaller fleas that on him prey;
And these have smaller still to bite ‘em;
And so proceed ad infinitum.”
-Jonathan Swift (“Poetry: A Rhapsody”).

2. Dr. Worthen, I have known Jorg Graf for a number of years, and his passion for leech-microbial associations (and his puckish sense of humor) always lead me to following this topic. He gave a superb seminar at the symbiosis symposium, for example.

3. Apologies for misunderstanding qetzal’s comment. I believe that a “Russian Nesting Dolls” paradigm for thinking about microbial interactions (in some cases, “intra-action”?) is useful and accurate. Merry’s topic is particularly instructive (I came to that line of thinking while considering “R-bodies” and the “kappa” phenotype in the protist Paramecium---look at how much more is known nowadays!).

We tend to think in reductionist terms, looking at simple systems and associations to gain an intellectual foothold on a problem. And there has been much benefit from that approach.

But looking, for example, at gut microbiota creates a different kettle of metaphorical fish, with over a thousand phylotypes to consider. There are many classes of “microbial associate” in that case, clearly, including: residents that use the location as a surface and little more, co-ops that contribute to upkeep or defense, transients that are just passing through (!), and “squatters” that “set up shop” in a disturbed or damaged location, to name a few.

Some of the associations may turn out to be trivial to understand, and others rivaling systems biology style complexity.

This makes me think, in turn, of “group activities” among microbes where “cheating” arises (say, among myxobacters, as studied by Greg Velicer and others). Surely such “cheating” will occur among the many denizens of a complex microbiota…ranging from (again) trivial examples to the very subtle.

I am then reminded of this great quote:
“All organisms are nothing but a bag of other organisms walking around.”
-Thomas Miller (UC Riverside).

Some of those organisms cooperate. Others fight. Still others are oblivious to one another. In a way, we are all ecospheres, writ moderately large. And enormous---whole worlds!--- to the microbes around us!

Thanks for the nice comments.