Apicomplexans. The term probably means little to you unless you have ever faced the prospect of contracting Malaria. Even still, it is unlikely that you are aware that Plasmodium falciparum, the causative agent of Malaria, is a member of a large group of parasites, classified as the apicomplexans. Other members include Toxoplasma gondii (Toxoplasmosis), Cryptosporidium parvum (Cryptosporidiosis) Trypanosoma brucei (African sleeping sickness) and Trypanosoma cruzi (Chagas Disease), among others.
Apicomplexans, in general, are nasty bugs that infect numerous animal species as parasites and pathogens. At ~6000 described species and many more yet to be discovered, the apicomplexan lineage is possibly the most diverse lineage of parasites known. They also have an unlikely origin, betrayed by a miniaturized organelle, called the "apicoplast". This organelle was known for many years before it was shown to be a highly reduced plastid in the mid-90s, and later determined to be derived from an endosymbiosis with a red algae. While no longer photosynthetic, the apicoplast carries out cellular functions, such as heme, fatty acid and amino acid biosynthesis for the cell. It maintains a genome, but the vast majority of active proteins in the apicoplast are encoded in the nucleus and targeted via a 5' leader signal on the mRNA and a complex targeting pathway. The apicoplast is essential for the cell and has, not surprisingly, drawn a lot of interest as a drug target.
Until a couple of months ago, the apicomplexans were thought to be entirely obligate parasites. However, Saffo et al. (2010) discovered a likely exception in an unlikely place. Members of the genus Nephromyces have long been known to inhabit the renal sac of certain small sea squirts (Molgula, Fig. 1). While living in this rather undesirable location, they feed on the kidney stones of the sea squirt and release nutrient back that the sea squirts utilize. For a long time these invaders were thought to be fungi, but they have some very unfungal characteristics, such as a biflagellate stage of their life history (fungi are, like their relatives the animals, uniflagellated) and a worm-like form that can be found in the sea squirt blood stream. DNA work done by Saffo and colleagues shows very clearly that Nephromyces are actually members of the Apicomplexa.
Fig. 1. Molgula sea squrit, home of Nephromyces. Image source.
Interestingly, this is not a case where these symbionts or mutualists (it is not clear yet*) are early diverging members of the apicomplexans that may have gotten out before the whole group went parasitic. Instead, they are nested squarely in the midst of their nasty cousins, indicating a revesion from parasitic to a friendlier life style - an event that is exceedingly rare in nature. So how and why did they do it.
Well, to start with, Nephromyces have apparently lost the apicoplast. There are other apicomplexans that have accomplished this, so there is no direct link between loss of the apicoplast and loss of a parasitic life style, but it is interesting. Second, Nephromyces has either lost or significantly reduced an apicomplexan structure called the rhoptry, which is the secretory structure used by infective stages of apicomplexans to gain entry into host cells. Third, and perhaps more importantly, the Nephromyces themselves harbor a symbiont. Their symbiont is a bacterium, which is thought to aid the Nephromyces in digesting the kidney stones it uses for nutrients. Nephromyces has therefore traded in its relic plastid and parasitic life style for its own bacterial symbiont and symbiotic relationship with Molgula.
This last point is particularly interesting, because the transition from parasite to symbiont is, as I pointed out above, rare. The basis for this is thought to stem from the specialization (from genome to morphology) required to be an effective parasite. Once you go parasite, you never go back. So this third party involvement is intriguing because the bacterial symbiont of Nephromyces may have allowed it to exploit a new niche and shirk the evolutionary path that it seemed predetermined to follow.
At its very core, the interaction of two organisms that results in one being inside the other can only go one of two ways - either the internal cell takes over as a parasite or the internal cell is enslaved as a symbiont. The interplay between Nephromyces and the bacterium it harbors should provide clues into two key evolutionary pathways by virtue of what the bacterium supplies to Nephromyces, which has allowed it to go from the parasite that controls its host's cell, to the symbiont that is controlled by its host.
* Nephromyces are not vertically passed from parent to offspring, but need to be taken up from the environment each generation. Therefore, they fall closer on the symbiont spectrum to the dinoflagellates found in coral than obligate intracellular symbionts like the Wolbachia found in aphids.
Note added in proof Carl Zimmer also has a post up about this paper. Go check it out for a different perspective.
Saffo MB, McCoy AM, Rieken C, & Slamovits CH (2010). Nephromyces, a beneficial apicomplexan symbiont in marine animals. Proceedings of the National Academy of Sciences of the United States of America, 107 (37), 16190-5 PMID: 20736348