Arma virumque cano (“I sing of the arms and the man”). So starts Virgil’s Aeneid. I have wondered why anyone would want to sing the praise of armaments, as this is not my cup of tea. There is, however, biological weaponry that I think deserves our admiration. One of the most elaborate examples is the mechanism found in Haptoglossa, an enigmatic fungus that has been provisionally classified with the oomycetes or water molds. An entire fungal cell is injected into a passing nematode or rotifer, there to develop at the expense of the host. Mechanisms for injecting biologically active material are not uncommon; they are seen in pathogenic bacteria, viruses, jellyfish, and stinging nettles, among others. But it is a rare organism that possesses the intricate machinery required to actively introduce a whole cell into a fast-moving and unsuspecting host.
An apology first: I use anthropocentric talk here, not because it’s the right thing to do, but because it is convenient. Unicellular Haptoglossa motile spores (zoospores) differentiate in a few hours into a fancy structure called a “gun cell,” which is capable of injecting a projectile—a spore—in toto into a grazing rotifer or a nematode. Once inside, the spore develops into a vegetative fungal body that consumes the host and grows to fully occupy its body cavity in a few days. Motile spores are then produced and released from the carcass of the host, starting the cycle anew. Thus, Haptoglossa is an obligate parasite and infection is required for survival.
What are the steps in the firing of a gun cell? Gun cells typically anchor to the substrate by their sticky base, and there they wait for an unsuspecting small animal to happen by. When a suitable host touches the business end of the gun, it is held there by a host-specific adhesive. Haptoglossa, by the way, means "sticky tongue." Injecting the projectile requires close contact with the host. This is not like a bullet flying through space. After attaching, the prepared projectile is shot through the muzzle of the gun cell, penetrating the animal's epidermis. A tube inside the gun cell is then turned inside out, forming a narrow conduit through which the Haptoglossa nucleus and cytoplasm pass into the animal's body. The whole process takes but a fraction of a second.
The structural differentiation of gun cells has been documented in great detail. The image of a section through a mature gun cell tells part of the story. One sees what looks like a wicked harpoon with a long shaft and barbs at its pointed end. Mournfully, it reminds one of the harpoons used to capture and kill whales by whaling ships. Scary-looking though this may be, the picture is slightly deceiving because the “barbs” are not hooks used to grab onto the host, but rather they are coiled proteins in a jack-in-the-box like arrangement. A similar arrangement in horseshoe crab sperm was recently shown to function as a biological spring capable of storing mechanical energy. Release of this energy to do work requires neither the action of motor proteins nor actin polymerization. It seems possible that Haptoglossa may use such a spring mechanism to fire its projectile. On the other hand, some researchers suggest that firing results from the rapid build up of osmotic pressure in the swollen basal part of the gun cell, and still others postulate contraction of actin filaments triggered by a rapid influx of calcium ions. The debate and the research continue.
The cycle of Haptoglossa development is completed when the spores are released from the infected host.
The videos show this is an explosive process, resulting in the discharge of thousands of spores. The video on top shows the release of small non-motile spores (aplanospores) of Haptoglossa polymorpha from a nematode host. The video below shows the release of motile spores (zoospores) from a nematode host of Haptoglossa dickii. Nematodes beware! (Both videos are courtesy of Drs. Sally Glockling and Gordon Beakes)
Of course, Haptoglossa is not alone in its ability to penetrate into other living cells. Sperm do it. Protozoa do it. Even bacteria and viruses do it. Each has its own mechanism to effect penetration, some simple-sounding, others quite intricate. Most require at least some active participation by the host. Haptoglossa (and some of its distant relatives) beats them all for the intricacy and beauty of its engineering design. I, for one, stand in awe of such structural sophistication. Someone should set Haptoglossa's performance to music.