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The Mystery Rust of Kivalina, Alaska

The views expressed are those of the author and are not necessarily those of Scientific American.

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A scanning electron micrograph of an unidentified rust spore from Alaska. Note the gorgeous projections that look like they've been turned on a lathe.

Author’s note: This is the last of a series of four posts in Fungi Month here at TAA. Enjoy!

Last month a mysterious orange film (“goo” in the media vernacular) washed up on the shores of a northwest Alaskan village called Kivalina. Experts suspected crustacean eggs; locals were unnerved. In retrospect, reports that the substance “dried into a powder” should have been suspicious, as should reports that the orange stuff also appeared on the water in rain buckets. Either the crustaceans really got around, or all was not as it seemed.

An orange powder seems an odd product for the drying of crustacean eggs, but could make perfect sense for fungi — specifically, the rust fungi. And indeed, that is what experts believe them now to be. And yet, for all the gumshoe work, they really still have no idea what they actually were — or what produced such an explosion in a place that had not seen such an event in the memory of anyone living.

Rusts are all plant parasites, but unlike the smuts — their close relatives, who I wrote about here earlier this month — they don’t specialize in hijacking plant parts for their nefarious purposes; instead they embed their reproductive structures in plant tissue in a system that can only be described as a byzantine dance of propagules. Some rusts have make up to five different sorts of spores in five different structures on two different hosts. It’s a bit dizzying keeping up with it all.

Before I fry your neurons with a rust life-cycle chart, let’s take a slightly larger view. There are thousands of species of rust, and all are plant parasites, many of which specialize in giving farmers — and biologists — headaches: coffee, asparagus, beans, snapdragons, carnations, roses, and wheat all have rusts that have achieved or are working on infamy. One rust — cedar-apple — makes distinctively alien orange goo starbursts on eastern red cedar (really a juniper) in the United States; its alternate host is apple.

A cedar-apple rust (Gymnosporangium juniperi-virginianae) gall on eastern red cedar after rain. When they're not wet, instead of looking like something your kids would enjoy eating or dropping down your shirt, they look like wooden balls with little satanic horns.

The reason they are called rusts is obvious: they make plants look rusty by discharging orange, powdery spores on leaves and stems during at least one of their many life stages. Here’s a photo I took of a rust dropping powdery orange spores in a rather undignified manner from a wild rose when I was on my boreal toad-hunting trip in July:

In completing their reproductive gymnastics, rusts produce some pretty interesting microscopic structures, or fruiting bodies, as mycologists sometimes call them.

Inside one of them, called a spermagonium or pycnium, sterile, stiff, tapering filaments called periphyses converge and push up on the plant epidermis. They rupture it, forming a little hole called an ostiole, and sometimes protrude through it like tentacles. Tailless male gametes called spermatia (or pycniospores) are formed inside and exuded in droplets of sweet, sticky nectar.

Nearby, “receptive hyphae” (high-fee — fungal filaments that make up their bodies) also protrude through the hole. Nectar-seeking insects land, get a sugar fix, and then take off with some hitchhiking spermatia stuck — in some embarrassing configuration, no doubt — to their feet or bodies. When they land on another spermagonium/pycnium, the spermatia/pycnia can then fuse with and fertilize the receptive hyphae. You know what this should remind you of, of course: a flower. A fungal flower, in fact, convergently evolved to suit the same purpose. And like some flowers, rusts have a rudimentary male/female system (mycologists boringly call the mating types A1 and A2) that ensures spermatia from a given spermagonium can’t fertilize their own receptive hyphae

OK. That is ONE of the FIVE possible life stages of a rust fungus. I’ve tried to shield you from this as long as possible. But I can’t hold back any more. Behold: the full horror of the life cycle of a heteroecious (two-host), macrocyclic (way too many spore-types) rust:

For the bionerds, delight in digesting this. For the rest of you, all that’s necessary is to notice what a headache it must have been getting this all figured out. For the record, not all rust fungi have life cycles this complex. Some have only one host, and some have only a few of the structures described above. But you get the idea.

This particular life cycle belongs to a rust fungus that is on my own personal ****-list. It is white pine blister rust — Cronartium ribicola — introduced to North America around 1900 and just now reaching Colorado after killing untold numbers of five-needle pines across the west. It has come south from Montana. And it is set to start killing our venerable limber and bristlecone pines, which I wrote about in June here. But I digress.

Each of those little cross sections in the drawing is a vertical section through a tiny cup-like structure on a stem or leaf. The potato-like objects inside are the spores. N is haploid(one copy of the chromosomes) and 2N is diploid, but N+N is a special fungal thing. It means the cells are dikaryotic — they have two nuclei from mating but they haven’t yet fused. Fungi have a tendency to have some part of their life cycle involve this odd-couple state. In humans, as you’ll recall, the nuclei of sperm and egg waste no time in fusing once the sperm makes its intentions known.

There is also a beautiful variety in the structure, color, and texture of rust teliospores — the resting stage for many rusts — which were traditionally used to classify them. They are often spiky or pegged dark brown visual confections of one to several cells, in chains, layers, or on stalks. At least one teliospore I looked at was a multicellular bundle with a striking resemblance to pattypan squash.

It is the urediospores (produced in the uredia) which are usually rusty orange (aeciospores can be orangey too), and these are the spores that scientists believe exploded into view in Alaska.

But the scientists at the NOAA lab in Charleston, South Carolina, that did the identification could not give the rust a species name. It didn’t match anything they had worked with before, they said, and they noted that there are many unidentified rust species lurking in Arctic tundra; as you can imagine, mycologists, a scarce resource in any climate, are not particularly abundant in northwest Alaska.

When I contacted the lab this week to find out if they had any further information on the rust’s identity, they said they did not. And unless some inquiring mycologist with time on their hands (ha!) has time to take a look, that is all we will probably ever know. And yet it gets a girl wondering: where *did* all those spores come from? What tundra plant could have possibly been so parasitized without anyone noticing? It’s not like rusts hide the fact they’re hanging out on plants — quite the opposite. And for an explosion of spores so profuse that they coated the ocean and washed ashore, there must have been something brewing on a biblical scale on the unfortunate hosts east of town. And what was it about this year that made them go crazy? If you’ve been paying to any news of the Arctic in the last five years, you can probably make an educated guess.

Before I close this post, though, I have a question about rusts I’d like to pose: if a rust has two hosts, they’re usually only distantly related. For instance, wheat stem rust’s hosts are common barberry and various grasses, straddling the gap between monocot and dicot flowering plants. White pine blister rust feeds on five-needle pines and various currants and gooseberries, shifting between the conifers and flowering plants. Uredinopsis osmundae shuttles between balsam fir and cinnamon ferns, crossing a huge taxonomic gap between seed-making and spore-making plants. Why?

And this leads to a larger question, which some of the wiser minds among you may understand, which is why so many parasites both of animals and plants seem to enjoy doing the host shuffle at all, much less across giant taxonomic gaps (there are many animal parasites, for instance, that shuttle between vertebrates and invertebrates like snails or annelid worms)? What benefit could having two sets of biologies and immune systems to navigate possibly offer when you could confine yourself to the comfy and familiar environs of just one host? I’m interested in your thoughts, so please feel free to share below. I should probably know the answer to this since I read Parasite Rex once upon a time, but I do not. Forgive me, St. Carl.

Jennifer Frazer About the Author: Jennifer Frazer is a AAAS Science Journalism Award-winning science writer. She has degrees in biology, plant pathology/mycology, and science writing, and has spent many happy hours studying life in situ. Follow on Twitter @JenniferFrazer.

The views expressed are those of the author and are not necessarily those of Scientific American.

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  1. 1. Pragmatist 2:52 am 09/28/2011

    Wouldn’t the ‘two host’ system offer two ‘reservoirs’,
    or ‘safe havens’ in the event of a die off or local disaster to one or the other host.
    A forest fire for the trees and their replacement with the re-growth shrubs eg.?
    (I do assume that the time spent with one or the other
    is not somehow limited.)
    * Could one of the ‘reservoirs’ for this particular organism be aquatic, (kelp eg.)?
    That would explain the lack of immediately visible concentrations.
    * Need the host be vegetable? The ‘slime’ appeared in the water. Could jelly fish, (known to be increasing
    in oceans), be one of the hosts?

    Link to this
  2. 2. Jennifer Frazer in reply to Jennifer Frazer 9:26 am 09/28/2011

    Your first idea is a natural one, and I may be thinking about this wrong, but typically these alternating parasites can’t complete their life cycle without time on both hosts. In fact, early wheat stem rust elimination campaigns were based on this exact idea: they tried to kill and uproot all the currants/gooseberries in the region of the wheat crops in order to eliminate the disease from the area. Not only did this not work well, committing genocide against an innocent bystander species also seems wrong. We’re learning today too that rusts have considerable latitude in their choice of alternate hosts, so getting rid of all the currants/gooseberries probably wouldn’t have solved the problem either.

    No one has ever found an aquatic host species for a rust, but that doesn’t mean it couldn’t exist — particularly given their ability to infect plants from across the evolutionary spectrum. I did a post about an infectious yeast that somehow managed to jump hosts from dolphins to humans to wood and bark last fall. I do, however, think it would have to be an aquatic plant or green alga to be plausible for a rust, since they are obligate parasites. Animals and red or brown algae seem far too distantly related. Also, the spores usually need to be dry to be wind-blown for dispersal, and coming from the ocean probably wouldn’t be conducive to that. But who knows?

    Link to this
  3. 3. rhamelin 11:26 pm 09/28/2011

    Nice paper. When I had read about the orange goo I was pretty sure it was rust spores. As for the two hosts, there is a theory about host radiation, for example, a rust that alternates between a conifer and a deciduous tree would have first evolved on the conifer and then jumped and radiated on the deciduous tree species which evolved later.

    As for identifying the rust species, it would be very easy to do with a DNA barcoding approach (e.g. see Feau, N., A. Vialle, M. Allaire, P. Tanguay, D. L. Joly, P. Frey, B. E. Calland and R. C. Hamelin. 2009. Fungal pathogen (mis-) identifications: A case study with DNA barcodes on Melampsora rusts of aspen and white poplar. Mycological Research 113: 713-724.
    Feau, N., A. Vialle, M. Allaire, W. Maier and R. C. Hamelin. 2011. DNA barcoding in the rust genus Chrysomyxa and its implications for the phylogeny of the genus. Mycologia.

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  4. 4. Jennifer Frazer in reply to Jennifer Frazer 10:07 am 09/29/2011

    Re: DNA barcoding — I know!! It would at least be possible to see what known species it is most closely related to. I can’t understand why someone isn’t doing this unless it is prohibitively expensive, but I don’t get that impression.

    Link to this
  5. 5. rhamelin 10:29 am 09/29/2011

    DNA barcoding is relatively cheap, prob less than $10 per sample. It would tell you what rust is most closely related, or match it if it is a rust that’s already known. At least it would place it in a group that would indicate which host it infects. It’s a no-brainer and I don’t know what they haven’t done it!

    Link to this
  6. 6. Contagions Round-up 15: Vampires, Vikings and Viruses « Contagions 12:01 am 09/30/2011

    [...] Frazer of The Artful Amoeba writes about a rust bloom in Alaska, funny how so many ancient so called primitive organisms (like fungi and jellyfish) are thriving on [...]

    Link to this
  7. 7. idjoly 11:25 pm 10/13/2011

    Hey rhamelin, get a sample and barcode it!

    Wonder if it could come from Hawaii… would need to look at a map of winds in the Pacific Ocean. They still have problems with guava rust on Ohi’a trees which make up to 80% of the Hawaii forests. It is highly susceptible and I heard that a few years ago, there was a orange mat on the ground of heavily infected forests.

    I also wanted to point that comment #2 from Jennifer mix two rusts. Wheat stem rust alternates on barberry, which the US tried to eradicate. White pine blister rust alternates on currants and gooseberries, which the US also tried to eradicate. Talking about stem rust, you should google for “M115 bomb”. After World War II, the US created a bomb designed to propagate wheat stem rust… what happened in Alaska could be the testing of a similar bomb or a failed bioterrorist act… ;p

    Link to this
  8. 8. tagayarak 7:56 pm 03/6/2012

    One possible benefit for having two types of biologies and immune systems is an ability to survive climate change. For the rust that can switch between large taxonomic gaps in “prey” species, this confers a possible evolutionary advantage when the natural order of succession occurs as a result of climate change. Those that cannot switch during times of rapid successional changes (which happens relatively quickly in the arctic vs. other moderate climates)may be more inclined to being selected out of the ecosystem. Just a thought…

    Link to this
  9. 9. Jennifer Frazer in reply to Jennifer Frazer 9:40 am 03/8/2012

    Hey guys — Thanks for your comments. I’ve never been to Kivalina, but the NOAA website confirming the identification states that black spruce is common near creeks and streams around Kivalina. So even if tundra is the prevalent habitat around there, it doesn’t mean there aren’t spruce in the riparian habitat as well.
    Specifically, they say:

    Black Spruce (Picea mariana) commonly lines rivers in this region of Alaska and Labrador Tea is a common plant in the understory.

    Rusts are obligate parasites of multiple hosts, so even if the majority of spores did come from Labrador Tea (which is possible!), there would have to be spruce in the area to allow the rust to complete its life cycle. So there must be spruces somewhere!

    Link to this
  10. 10. Stumps trump time travel by revealing decades in one glimpse « Boreal Bites 3:17 am 05/27/2012

    [...] As anyone who has ever worn flip-flops to a gym or dorm shower knows, fungi don’t just break down detritus beautifully, they also plague the living. Sooty molds can cover leaves, soil fungi can kill off seedlings, rusts can baffle Alaskans. [...]

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