Of Archaeal Periplasm and Iconoclasm

http://schaechter.asmblog.org/schaechter/2010/02/of-archaeal-periplasm-iconoclasm.html

Biology is the iconoclast's paradise. Over and over, cherished beliefs, some dating back for centuries, fall to the ground as exceptions to the rule are discovered. To the long list of such exceptions, we now add the finding by groups in Regensburg and Frankfurt that the outer membrane of an archaeon, Ignicoccus hospitalis, is energized and capable of generating ATP. Granted, this is a hyperthermophile who helped shatter the ancient belief that life at high temperatures is not possible, thus hardly a conformist. But this discovery is, to say the least, unexpected.

The old tenet is that the energetic business-end of prokaryotes is the cell membrane, whether surrounded by an outer membrane, as in gram-negatives, or not, as in gram-positives. I should know, I taught this for umpteen years. True, in gram-negatives, energy can be transmitted to the outer membrane via the Ton system (a system that provides energy for the transport of iron siderophores, vitamin B12, and some colicins), but the reverse, making energy on the outer membrane and sending it to the cytoplasm, is not part of the old belief. Yet it's been known for some time that a goodly number of bacteria can energize their outer membrane, having cytochromes inserted in the outer membrane where they carry out extracellular electron transfer. This ability allows these organisms to utilize metals in rocks as electron acceptors.

Dual membrane systems have not be found in archaea other than Ignicoccus. What are the new conclusions about power generation in its outer membrane based on? Mainly on immunoelectron microscopy of sections using gold-labeled antibodies and immunofluorescence showing ATP synthase and H2:sulfur oxidoreductase located in the outer membrane. These two enzymes are required for energizing membranes and for ATP production. Thus, ATP can be expected be made in the outer membrane and released into the periplasm (which in this organism is huge-larger than the cytoplasm). You may ask, are these two enzymes also found in the inner membrane? The answer is no. Since the periplasm is so large and the two membranes so far apart, enzyme localization to one membrane or the other can be readily discerned. So, which is the cytoplasmic membrane in this organism? Note that this two membrane system is different from that of ordinary Gram-negatives, as here the outer membrane is not known to contain LPS or porins.

Is the Ignicoccus story relevant to other prokaryotes? Who's to say at this point. Ignicoccus is mightily idiosyncratic. Not only does it grow at very high temperature and use reduction of elemental sulfur as its main energy source, but it also lives in intimate association with another archaeon, the smaller Nanoarchaeum equitans, which has a reduced genome and apparently gets its energy from its larger partner. The unusual ignicoccal ability to make ATP within its periplasm may help it to supply ATP to its associates across the outer membrane.

The authors propose a tantalizing notion: if the eukaryotic cell arose by an archaeon having swallowed a bacterium (hold on, we're not getting into that discussion right now), then Ignicoccus or something like it would have been the ideal ancestor, able as it appears to be to donate ATP to anyone residing within its boundaries. True or not, one should further respect the outliers in the biological scheme of things as potential sources of novel and deeper relationships.

Kuper, U., C. Meyer, V. Muller, R. Rachel, H. Huber. 2010. Energized outer membrane and spatial separation of metabolic processes in the hyperthermophilic Archaeon Ignicoccus hospitalis. Proc. Natl. Acad. Sci. USA 107(7):3152-3156.