"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

November 3, 2011

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.