This post is the latest in a continuing series called "Wonderful Things".
The most complicated fungal cell known to science belongs to a parasite called Haptoglossa mirabilis first lured into a rotifer-baited trap in the soil of a tropical greenhouse in a Toronto suburb on October 7, 1979. Inside that trap lay a cell so intricate and finely tuned it gives jellyfish stinging cells a run for their money.
Ordinary soil is a veritable torture chamber for small animals like nematode worms -- small round worms -- and bdelloid rotifers -- microscopic animals with twin undulating crowns of cilia and gnashing jaws -- and the like. The many ways to die include sticky traps and spores, stabbing and bloodsucking by other nematodes, and fungal nooses that suddenly inflate and strangle. But there is yet another cunning way. For the soil may be studded with harpoon-loaded cannons ready to fire at the slightest nudge. Like this one:
Let it not be said that humans are alone on Earth in devising elegant, horrific artillery pieces. For the fate that lies in store for the nematodes and rotifers that graze this gun is not a pleasant one. They will be stabbed, injected, and then eaten alive from the inside by one or more tumor-like cell masses before the parasite sprouts tubes that burst through their host's skin and eject two-tailed swimming spores like escape pods from a dying star cruiser. Getting shot by Haptoglossa qualifies as a bad day.
First, I should clarify that although the organism that makes this gun is fungal, it is not a Fungus proper. It is an oomycete, which looks and acts a lot like a fungus the way a whale looks and acts a lot like a fish. The pathogen that caused the Irish Potato Famine -- Phytophthora infestans -- is also an oomycete. Oomycetes -- also called water molds -- were mistaken for Fungi when first discovered, but clues in their anatomy, biochemistry and DNA eventually outed them as distant relatives of true fungi. But fungus with a small f can sometimes be used to describe a form group of organisms that look and act like the true Fungi, and that is the sense I call it fungal here.
Haptoglossa's gun has more in common with the mechanically-powered catapults, trebuchets, and ballistas of the Greeks and Romans than modern guns employing gunpowder. It relies on physics, not chemistry, for power. The gun is anchored by a thick glue (14) that props up at a low angle and anchors the weapon during firing. At the base of the cannon lies a giant water vacuole -- essentially a big sealed balloon filled with water. It, and the entire rest of the cell are kept at high pressure by the cell. George Barron's hypothesis for how Haptoglossa fires holds that there is a built-in line of physical weakness in the muzzle of the gun (sort of like the line of built-in weakness in a tube of refrigerated biscuit dough that bursts open when you press the seam with the back of a spoon).
The gun's muzzle leads to a bore loaded with a harpoon with laminated barbs(6). The layers have space between them that makes them compressible inside the bore of the gun. Once fired, however, the barbs spring forward and prevent the harpoon from slipping out of the struggling target. The purpose of the harpoon is to puncture the skin of the animal host. But the harpoon alone is relatively harmless. The deadly work of the gun is accomplished by something that follows close behind.
When an animal bumps the tip, it breaks somehow at this line of weakness near the muzzle and releases the pressure on the cytoplasm. The pressure in the vacuoles remains high, and the sudden pressure differential ejects the harpoon, its bore, and a long flexuous tube continuous with the base of the bore (8, 9, and 10).
The tube is closed at the end, and so its ejection is a bit like turning the inverted finger of a rubber glove right-side out by blowing air into the glove. As the entire system everts, cyotoplasm rushes into the everting tube along with pre-stored cell wall and cell membrane components. It follows the harpoon into the animal, and once inside the tip promptly inflates with the help of the pre-stored construction material into a "sporidium" (grey cell with dashed line above). The entire process takes only about 1/10 of a second.
Here is what a real fired gun that has missed its mark looks like:
If the gun has fired successfully, the sporidium will end up inside a rotifer or nematode but still be attached to the gun outside. As the animal struggles to break away from the cell that has impaled it, the sporidium usually breaks off from the gun cell and the animal slithers off, none the wiser.
Mycologist George Barron, who first described this species, wrote a vivid description of what he observed through the microscope When Haptoglossa Attacks:
When a rotifer passed close to a cell, the base of the cell remained fixed, but the tip moved gently to and fro in the current caused by the passing rotifer ... When a rotifer moves across a field of injection cells, it comes to a sudden stop then writhes and struggles furiously at the point of attack. Presumably, the cell has been fired and the rotifer impaled by the spear-like extension. The adhesive power of the mucous pad anchoring the injection cell to the substrate is sufficiently strong that it can temporarily hold a struggling rotifer. Almost immediately or within a few sec[onds] the rotifer will pull free. Sometimes escape takes as long as 30 sec[onds]. When the rotifer moves off, the empty injection cell can be seen still attached to the substrate or the rotifer may break the adhesive bond and swim off with the empty cell sticking into its cuticle.
Would that all journal articles were so lucid. Barron further notes that infected rotifers continue moving around during infection, making them vulnerable to serial infection. In a petri dish Haptoglossa firing range, as many as 12 sporidia have been found in one hapless rotifer.
What happens next is familiar to anyone familiar with the machinations of parasitoid wasps. The sporidium divides and grows into a pill-shaped or spherical "thallus". In the first image, below, you can see a rotifer who's been injected with at least five, and possibly six or seven Haptoglossa sporoidia. Below (3 and 5) that are the disturbingly large, masses that the tiny sporidia grow up to be.
When sufficient size is reached, the thallus grows one or more evacuation tubes -- as you can see in image 5 above -- that penetrate the body of their host once more. Here are some more views of the evacuation tubes, and the distressing size of Haptoglossa thalli with respect to their host (Image 9 is a field of mature unfired guns):
Double-tailed swimming spores emerge, and at least in George Barron's laboratory, swim only briefly before settling down, dropping their tails, and encyst. Very quickly, the cysts spill their contents into the body of a new growing gun cell that emerges from it (9, above).The empty cyst case often clings to the top of it even after it matures. Alternatively, cysts can grow more swimming spores, perhaps if the encysted spore somehow senses that the rotifers and nematodes are partying elsewhere.
The way in which Haptoglossa gun cells work their deadly magic is extraordinary, particularly when you consider that all the machinery involved and described above is contained within but a single cell. One horrible, incredible cell.
But their design has perhaps one shortcoming that may help explain their incredible complexity and lethal efficiency: The gun cells of H. mirabilis exist for no other purpose than to shoot small animals. Once fired, they are dead and done. As any gunslinger can tell you, when you've only got a single bullet in the chamber, you've got to make that one shot count.
Barron G.L. (1980). A New Haptoglossa Attacking Rotifers by Rapid Injection of an Infective Sporidium, Mycologia, 72 (6) 1186. DOI: http://dx.doi.org/10.2307/3759573
Barron G.L. (1987). The Gun Cell of Haptoglossa mirabilis, Mycologia, 79 (6) 877. DOI: http://dx.doi.org/10.2307/3807689