Gulliver and the Lilliputians

by Elio & Merry

"I found my arms and legs were
strongly fastened on each side
to the ground." Gulliver's Travels,
as illustrated by Milo Winter.

Two archaea walk into a bar and the bartender says… No, we don't have an ending for this joke (tell us if you do), but if the temperature of the bar were around 90°C and the locality a hydrothermal vent off Iceland, there is a chance that the pair sauntering in could be one of the most interesting duos around. One partner is Ignococcus hospitalis, an archaeon of respectable dimensions (2μm diameter) that is often seen in close association with the much smaller Nanoarchaeon equitans.

To start with, the names of the organisms were chosen with care. Ignococcus means “fiery coccus;" hospitalis, “host;" equitans, “horse rider.” So, what about them?

I. hospitalis is an anaerobic chemolithotroph that gets its energy from oxidizing elemental sulfur using molecular hydrogen as the electron donor. N. equitans is tiny—approximately 400 nm in diameter—and has one of the smallest known genomes—some 490 kb. It lacks nearly all genes for lipid, cofactor, amino acid, and nucleotide biosynthesis. Not surprisingly, it can't be grown alone in the lab. It obtains its membrane lipids from its partner, and likely its amino acids, as well. For more intimate details, see a new report in the Journal of Bacteriology that describes an interesting collection of physiological and structural studies.

Transmission electron micrographs of ultrathin sections of I.
hospitalis and N. equitans following cryoprocessing. CM, cyto-
plasmic membrane; OM, outer membrane; Pp, periplasm; PV,
periplasmic vesicles. White arrows point to the contact site
where the I. hospitalis outer membrane is in close contact
with the cytoplasmic membrane. Bars, 1mm. Source

One would expect such a drain of resources to have some negative impact on the host cells, but in the lab I. hospitalis grows just as well with or without its partner. Its doubling time is not reduced, and neither is the final cell density. However, something is going on. During exponential growth in co-cultures, about a third of the Ignococcus cells are seen to carry 2-3 N. equitans cells. When entering the stationary phase, most Ignococcus cells are covered with as many as ten N. equitans, reminding us of Gulliver outnumbered and overrun by Lilliputians. On the other hand, N. equitans does not proliferate until the host enters stationary phase. Who’s inhibiting whom? This sounds complicated. The authors suggest: …that the association of I. hospitalis and N. equitans represents a highly specialized system. Consequently, assignment to the classical category of symbiosis, commensalism, or parasitism might not be possible even in the future.

But N. equitans has other unique traits that are both extraordinary and intriguing. Phylogenetically, it is a thing onto itself. For starters, it is the only characterized member of the kingdom Nanoarchaeota, a group thought to represent a very ancient branch of the tree of life, maybe going all the way back to the beginning (the precise branching point being still under debate). Its diminutive genome possesses unique and potentially ancient ancestral traits. Five of its tRNAs are encoded by genes that are split along the genome. The RNAs are later spliced together. Nowhere else does one find this way of making tRNAs. In all cases, the split occurs at a site adjacent to the anticodon—the normal location for tRNA introns. One is prompted to wonder about the why and the how of this trans splicing mechanism, as well as to speculate about the evolutionary origins of tRNAs. (For the latest, click here.) There are numerous protein-encoding genes that are split, too. And unlike other Archaea, this organism lacks operons. Not that it lacks the genes, but instead of being clustered, they are scattered about the genome.

Another distinguishing feature is that N. equitans is arguably the best, although perhaps not the only, example of a parasitic archaeon. Why the Archaea have not exhibited greater gusto for a parasitic lifestyle is an open question.

Comments

[Autumn Cochrane]

Okay, I'm going to ask a question, and then try to answer it, and see if I'm right.

QUESTION: If N.Eq. lacks nearly all genes for lipids, cofactors, amino acids, and nucleotide biosynthesis, shouldn't it be classified as a virus?

Possible Answer: It's because of the "lacks nearly" phrase, isn't it. It does carry some genes for its own lipids, etc., while viruses don't carry any of these genes. (?)

Another question: Since I know very little of the genome of viruses, what exactly does the viral genome encode for?

Note: As always, thanks for the blog, and thanks for the TQ's! I find them actually fun to ponder. The blog is a great way to learn and pick up little bits of advanced biology concepts. I'm going to be like a walking textbook by the time I go off to a 4-year university (LOL)!

Autumn,
See a discussion of what's of a virus in TQ#6, which includes a comment of yours. A popular view of the distinction is that a virus breaks up into its constituents during replication, something a cell never does. You'll see more about this in the blog soon. The genes are carried by viral genomes is a big question, as they vary between a few and many hundreds. Mimivirus is said to have some 900!

Elio

Elio

[elio]

Christopher,

You most informative blog piece "The Nature of Nanoarchaeum" should be read by all interested in its phylogeny. It's at http://catalogue-of-organisms.blogspot.com/2008/05/nature-of-nanoarchaeum.html

Thanks for pointing it out.

Elio

[Christopher Taylor]

I personally don't buy 'Nanoarchaeum' as a superbasal archaebacterium - it seems more likely to be a derived euryarchaeote with an accelerated evolutionary rate. I wrote about this at http://catalogue-of-organisms.blogspot.com/2008/05/nature-of-nanoarchaeum.html.