Ophiocordyceps unilateralis

Have you ever been so intoxicated that you start walking erratically, stumble away from your friends, stagger around in circles, clamber onto things that you wouldn't normally be seen near, and the next thing you know, you are strapped down in unfamiliar surroundings, unable to extricate yourself? Well, that pretty much describe what happens to ants which become infected with the famous "zombie ant" fungus - Ophiocordyceps unilateralis.

Much has been written about this famous fungus which turns ants into zombies - it is a parasite which captures the same part of our psyche as the monstrosities of horror movies, and there is evidence to suggest that these fungi have been tormenting ants for at least tens of millions of years. But despite all that attention, few people have actually witnessed or documented the sequence of behaviour leading up to the infected ant's paralysis and death. But in a paper published this year, a group of researchers followed the behaviour of ants infected with the famous "zombie"-inducing fungus and compare them to their uninfected brethren.

They noticed a few peculiarities with the behavioural repertoire of infected ants which stood out. While healthy ants studiously stick to the usual lanes of ant traffic, climbing into the canopy to forage with all the other busy worker ants, "zombie ants" are loners which meander around in the understory by themselves, are unresponsive to most stimuli, and frequently stumble and fall from the branches they are walking on. Essentially, the ants act absolutely drunk, indeed, the researchers described the behaviour of the "zombie ants" as a "drunkard's walk" in their paper. Another weird thing that infected ants start doing is their tendency to crawl all over and bite into leaves - something which healthy ants don't tend to do. There's a good reason why the fungus steers the ant towards leaves and afflict it with this oral fixation - it is preparing it for the next step in the fungus' development.

For the fungus to successfully reproduce, the ant must die - but it must die in a particular position to maximise the viability and dispersal of the fungal spores, specifically in the humid understory, hanging from the underside of a leaf, about 25 cm (about 10 inches) above the ground. But once the fungus maneuver the ant into position, how does it get the host to comply and stay there? The researchers made fine histological cross-section of the infected ant's head and found that once the fungus has made the ant locks its mandible in place, it busily gets to work dissolving the muscles which control those mandibles, ensuring that the ant will be locked in a death grip forevermore. A few days after the ant dies while gripping onto, the fungal stalk emerges from the head of the ant, ready to spray its spores down to the soil below to create more drunken "zombie ants".

Image from the Wikipedia.

Reference:

Hughes DP, Andersen SB, Hywel-Jones NL, Himaman W, Billen J, Boomsma JJ. (2011) Behavioral mechanisms and morphological symptoms of zombie ants dying from fungal infection. BMC Ecology 11:13

Postscript: A few hours after I wrote this post, I found out that Carl Zimmer has already written about this study (why, of course! *facepalm*), so if you want to read his version instead, you can see it here.

Polypocephalus sp.

Today's parasite might be thought of as an "aquatic Toxoplasma" in that it also induces behavioral changes in its hosts. Polypocephalus is a genus of tapeworms that infects both shrimp (Litopenaeus setiferus) and then likely rays such as the Atlantic stingray, (Dasyatis sabina). The larvae of the cestode invade the neural tissue of the shrimp hosts, particularly in the abdominal ganglia. Studies recently showed that the more larval tapeworms a shrimp had, the more time these hosts spent walking on the substrate, as opposed to sitting still or swimming. Although the authors had predicted that they would see an increase in swimming behavior because that might expose them to predation more readily, perhaps just the increased activity in general is enough to promote transmission. Nonetheless, this was an exciting insight into a potentially new system for studying parasite manipulation of their hosts.

Source: Carreon, N., Z. Faulkes, and B. L. Fredensborg. 2011. Polypocephalus sp. infects the nervous system and increases activity of commercially harvested shrimp. Journal of Parasitology 97:755-759

Image from figure of that paper.

Bursaphelenchus xylophilus

Today's parasite is the nematode Bursaphelenchus xylophilus, a well-known tree-killer responsible for the devastating plant disease known as pine wilt. Originating in North America, it has since been spread over much of Asia, and has recently been introduced to Europe. This nematode is transported by longhorn beetles known as "pine sawyers", and gain initial access to the tree through the feeding wound created by that insect. So the arrival of a B. xylophilus-laden beetle pretty much amounts to a death sentence for a pine tree. While pine trees in North America have coevolved with B. xylophilus and developed resistance or tolerance for the parasite, it has caused widespread wilting and death to the pine trees of Japan. So how can such a tiny worm bring down an entire pine forest?

For B. xylophilus, or any other plant parasites for that matter, a tree is a formidable fortress - protected by walls and scaffolding of tough cellulose, and canals of deadly resin. Plant cell wall presents the main barrier to any plant parasites - it is a tough material to break down, and most animals are incapable of doing so without the aid of symbiotic microbes. In addition, the vascular tissue of many coniferous plants like pine are saturated with resin - a thick, sticky cocktail of aromatic chemicals (from which we derive many useful substances including solvents, varnishes, adhesive and perfume) which would overwhelm and kill most invaders. Yet none of those defenses seem to deter B. xylophilus - not only can it break through the thick cellulose barrier of the pine tree, it actually lives within the resin canals of its host, which is practically the most lethal place within the tree. It would be akin to living in a moat of toxic tar.

A recent study published in PLoS Pathogens on the genome of B. xylophilus offers vital clues to how this nematode exploits its pine tree host. One of the most important enzymes for plant exploitation is cellulase - it is used to break down cellulose structures and allow potential parasites to enter and navigate through the host. Bursaphelenchus xylophilus is able to produce a unique combination of 34 enzymes for breaking down cellulose and carries a diverse suite of genes for producing enzymes that detoxify the aromatic compounds found in resin. So how did this tree killer acquire the necessary molecular machinery to invade and disarm its host?

The wide range of detoxifying genes in the B. xylophilus genome appear to be multiple duplication of pre-existing genes which are also found in other nematodes, such as the well-known standard lab worm Caenorhabditis elegans - B. xylophilus just happen to have more of copies of those genes to cope with the wider array of toxins it encounters. However, the cellulase genes have a much more unusual origin. Out of the 34 cellulase enzymes produced by B. xylophilus, 11 of those enzymes are not found in any other nematode, but are most similar to those produced by fungi. So how does a nematode end up producing fungal enzymes?

The answer might be through horizontal gene transfer (HGT). The closest living relatives of B. xylophilus are fungi-eating worms which are transported by beetles to dead and dying trees. Once they reach their destination, they disembark from their beetle vectors and feed on the fungi which have colonised the dead trees. In a case of you are what you eat, the ancestors of B. xylophilus appeared to have incorporated a whole suite of useful genes from their food, allowing them to bypass the process of feeding on fungi which are growing on dead trees and just go straight to breaking down live plant tissue.

Image from figure of the paper.

Reference:

Kikuchi T, Cotton JA, Dalzell JJ, Hasegawa K, Kanzaki N, et al. (2011) Genomic Insights into the Origin of Parasitism in the Emerging Plant Pathogen Bursaphelenchus xylophilus. PLoS Pathog 7(9): e1002219. doi:10.1371/journal.ppat.1002219