Of Archaeal Periplasm & Iconoclasm

by Elio

Rough work, iconoclasm, but the only way to get at truth.
            Oliver Wendell Holmes

A thin section of Ignicoccus hospitalis under
the EM. C = cytoplasm. CM = "cytoplasmic"
membrane. P = periplasm. OS = outer sheath
(membrane). Bar = 0.5 µm. Source.

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. They do this by having cytochromes inserted in the outer membrane where they carry out a process known as extracellular electron transfer. This ability stands the organisms in good stead, allowing them to utilize metals in rocks as electron acceptors.

Localization of A₁A_O ATP synthase on I. hospitalis cells in ultrathin sections. (A) Labeling
with antibodies against the purified ATPase complex, (B) Labeling with antibodies against the
membrane-bound subunit a. For both images the secondary antibody with ultrasmall gold
particles is visualized. C = cytoplasm. IM = inner membrane. V = vesicles in the periplasm.
OM = outer membrane. Bar = 1 µm. Source.

First of all, 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, which revealed that ATP synthase and H₂:sulfur oxidoreductase are located entirely 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. This introduces the question: which is the cytoplasmic membrane in this organism? The figure tells you something about the rare structural complexity of this organism. Note that the two membrane system is different from that of ordinary Gram-negatives, as here the outer membrane is not known to contain LPS or porins.

Co-culture of Ignicoccus spec. (green) and
Nanoarchaeum equitans (red). ss rRNA sequence-
specific fluorescence staining. Bar = 1 µm. Source.

Is the Ignicoccus story relevant to other prokaryotes? Who’s to say at this point. Ignicoccus is mightily idiosyncratic, e.g., it’s unique among archaea in having a two-membrane system. 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.

Research Blogging Citation
Kuper, U., Meyer, C., Muller, V., Rachel, R., & Huber, H. (2010). Energized outer membrane and spatial separation of metabolic processes in the hyperthermophilic Archaeon Ignicoccus hospitalis Proceedings of the National Academy of Sciences DOI: 10.1073/pnas.0911711107

Comments

[Moselio Schaechter]

Re: [Small Things Considered] Mike Gray submitted a comment to Of Archaeal Periplasm Iconoclasm

You zeroed in on a point that is discussed in the paper. Have a look and see what they say. Let em know if you cant access it.

Elio

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A new comment from Mike Gray was received on the post Of Archaeal Periplasm Iconoclasm http://schaechter.asmblog.org/schaechter/2010/02/of-archaeal-periplasm-iconoclasm.html?cid=6a00d8341c5e1453ef0120a89e0567970b#comment-6a00d8341c5e1453ef0120a89e0567970b of the blog Small Things Considered http://schaechter.asmblog.org/schaechter/ . Comment:
Thats really cool. At what point do we have to discard the Gram negative analogy for Ignicoccus membranes? Could you argue that the outer membrane is the cytoplasmic membrane and the inner membrane is more of a nuclear membrane? Or are the cellular compartments of Ignicoccus different enough that we need new names for them?
Commenter name: Mike Gray
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Enjoy!

[Mike Gray]

That's really cool. At what point do we have to discard the Gram negative analogy for Ignicoccus membranes? Could you argue that the outer membrane is the "cytoplasmic membrane" and the inner membrane is more of a "nuclear membrane"? Or are the cellular compartments of Ignicoccus different enough that we need new names for them?