Scientists have found an unprecedented evolutionary modification deep within the cells of the lowly human body louse (Pediculus humanus): the tiny blood sucker contains not one but 18 separate mitochondrial chromosomes.

A female human body louse (Pediculus humanus corporis). Photo courtesy of Richard Webb and Renfu Shao

"It's a big surprise to me and my colleagues," wrote Renfu Shao, lead author of the newly published Genome Research paper describing the discovery, in an email to The Scientist. "Since the human mitochondrial genome was sequenced in 1981, more than 1500 animals have been sequenced for complete mitochondrial genomes," he wrote. With the exception of some oddball ciliates, flagellates and cnidarians, virtually all animals have a single, circular mitochondrial chromosome that contains approximately 37 genes. "Thus, it has almost been taken for granted that any animals would have a single mitochondrial chromosome with all mitochondrial genes on it."

David Rand, a Brown University evolutionary geneticist who was not involved with the study, told The Scientist that multiple mitochondrial chromosomes in animals were exceedingly rare and that the presence of the 18 "mini chromosomes" in the mitochondria of the louse was "clearly a novel organization."

Shao, a postdoc in the lab of University of Queensland evolutionary geneticist Stephen Barker, and his collaborators used whole-genome shotgun sequencing to uncover the unique genetic structure of the body louse's mitochondrial genome after several years of failing to amplify the entire mitochondrial genome using traditional sequencing methods. Each of the 18 mini chromosomes found in the body louse's mitochondria were only 3-4 kb long and contained 1-3 of the total 37 mitochondrial genes.

Multiple mitochondrial chromosomes may allow the organism to streamline replication and transcription of individual genes, since generally, genes on a single strand of mitochondrial DNA are transcribed together, Shao explained. He added that if the DNA on multiple mitochondrial chromosomes is replicating in concert, replication of the entire mitochondrial genome would occur faster.

The evolution of this unique mitochondrial genome structure is not likely due to a single "big bang" event, the authors say. Where typical single mitochondrial chromosomes have only one copy of the sequences necessary to initiate replication and transcription, each of the louse's mini chromosomes has its own set of instructions. This, said Shao, points to a more complicated evolution towards multiple mitochondrial chromosomes.

"We think that the multiple minichromosomes were generated from a series of events that involved excision and rejoining of fragments of [mitochondrial] chromosome over a long period of time," he wrote. As non-coding, control regions from the single chromosome were copied and excised along with a few genes, the resulting mini chromosome may have functioned more efficiently than the region on the single chromosome; the redundant region on the larger chromosome would have then been deleted, explained Shao. It would take just a few more excision events to arrive at 18 mini chromosomes with all the functionality of their single-circle ancestor.

The findings generate many physiological questions about how the louse manages to keep track of separate mitochondrial chromosomes. During cell division, for example, all 18 mini chromosomes must be copied and transferred seamlessly to daughter mitochondria -- no easy task. If one is missing, said Shao, the new mitochondria would not function properly. "It is a mystery to us how these minimitochondrial chromosomes are 'herded' into daughter mitochondria and daughter cells at mitochondrial and cell division."

"Clearly the cell has solved this in some way," added Rand, "because [the lice] are extant."

Rand said that whole-genome sequencing may yet uncover more examples of such mitochondrial organization. "Certainly as we move to more whole-genome analyses of mitochondrial DNA, we may be more likely to pick this up," he said. Other parasites, he noted, might be a good place to look. Plasmodium falciparum, one of the protozoan parasites that causes malaria in humans, he said, has one of the smallest mitochondrial genomes known, though this reduction has left the single chromosome strategy intact.


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