Microsporidia ramblings

I saw this article about Colony Collapse Disorder (CCD) Tuesday morning, which referred to this paper that implicates Nosema ceranae as the cause of all the bee deaths in the U.S. and Europe. I'm no expert in bee pathology or entomology (my bug policy is "swat first, ask questions later"), but I'm extremely interested in weird critters with weird genomes. Nosema fits the bill.

When I was in grad school, the Microsporida, of which Nosema is a member, were considered to be among the most primitive eukaryotes out there, since they lack mitochondria. It was thought that they branched off the evolutionary tree of the eukarytes before the acquisition of mitochondria. Now we know that the nuclear genomes of Microsporidia contain mitochondrial genes and that they have an organelle called a mitosome, which looks like it used to be a mitochondrion. So now Microsporidia are thought to be highly derived from something like a fungus. In case you're keeping track, going from primitive eukaryote to related-to-fungi is about a billion years of evolution.

Microsporidia also have weird genomes. Microsporidia are intracellular parasites, which means they don't just infect your body, they infect your cells, kind of like viruses. The genomes of Microsporidia are some of the tiniest eukaryotic genomes, which kind of makes sense since they're parasites. The complete genome of Encephalitozoon cuniculi has been sequenced, and it's only 2.9 Mb. That's smaller than many bacterial genomes, and it's about 1000 times smaller than the human genome. It has very little intergenic DNA, no repetitive elements, thirteen introns, and only about 2000 genes with surprisingly short reading frames. Other microsporidia have larger genomes, and Nosema species have 10-15 Mb genomes, which is a pretty big difference.

Why does this matter? Genome reduction is a pretty common phenomenon, which I've commented on before (in an Impact article about mycoplasmas). We typically find that parasites and some mutualists have highly reduced genomes, with many fewer genes than free-living counterparts. From a creationist perspective, it's tempting to conclude that the loss of genes contributed to or even caused the development of the parasitic lifestyle (that's exactly what I argued about the mycoplasmas). Now, I think that idea seems almost too naive. I did a survey for the 2006 BSG conference that looked at genome size in relation to lifestyle among bacteria, and I found that many pathogens had larger genomes than their free-living (congeneric) relatives. I'm not saying that gene loss and genome decay is not linked to pathogenicity, but it can't be the whole story.

Microsporidia add to this question, since they really look like they were designed to have tiny genomes and to be intracellular symbionts. It's not like they have normal eukarytic chromosomes with fewer genes, which would imply that they just lost genes. Instead, microsporidial genomes have a surprisingly different organization than many eukaryotes, which goes beyond just losing genes. Furthermore, there aren't any close relatives with really big genomes. All the microsporidia have tiny genomes. They range in size from about 2.3 to 20 Mb, but that's it. Did they lose genes? Or did they ever have them in the first place? If they've always been small, if they were created to be intracellular symbionts, how did they become pathogenic? If Nosema really does cause CCD, how did that happen? And why now?

I wish I knew, but I don't. Someone should look into that. For more on microsporidian genomes, see this paper:

Keeling and Slamovits. 2004. Simplicity and complexity of microsporidian genomes. Eukaryotic Cell 3(6):1363-1369.

Meanwhile, here's a paper in the latest PNAS that should interest my friend Joe:

Hoshi et al. 2009. A unique virulence factor for proliferation and dwarfism in plants identified from a phytopathogenic bacterium. PNAS 106(15):6416-6421.

I'll be back in a few days with another "From the Library."