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The hyperthermophilic archaeon Ignicoccus hospitalis generates ATP on the inner side of its outer membrane and the energy molecules flow toward the inner membrane, according to Harald Huber at the University of Regensburg in Regensburg, Germany and his collaborators there and at the Johann Wolfgang Goethe University in Frankfurt. I. hospitalis, or an organism much like it, is an ideal ancestral candidate. Details of this research appear in the February 16 Proceedings of the National Academy of Science (107:
3152-3156).
"This most recent discovery is, to say the least, unexpected," notes Moselio Schaechter of California State University at San Diego, "even for the hyperthermophile that shattered the ancient belief that life at high temperatures is not possible." All three known species in the crenarchaeal genus Ignicoccus lack rigid cell walls, specifically, a surface layer (S layer) typical for other members of its phylum. Furthermore, also in contrast to other archaea, the inner and outer membranes of Ignicoccus enclose a compartment called the periplasmic space after the cell-wall containing periplasm of gram-negative bacteria. However, the archaeal outer membrane lacks lipopolysaccharide (LPS) and is porin-free, making it fundamentally different from that of gram-negative bacteria. Thus, I. hospitalis, along with I. islandicus and I. pacificus, have cell envelope architectures unique among archaea and unlike that of any known bacterium.
By examining the A1A0 ATP synthases of the I. hospitalis outer membrane, Huber and his team determined that this organism generates ATP within the periplasm, and that it flows inward towards the cytoplasmic membrane. In contrast, gram-negative bacteria generate ATP in their cytoplasmic membranes and transmit those molecules to the outer membrane. Because DNA and ribosomes are located in the cytoplasm of this archaeon, the researchers point out that ATP synthesis is spatially separated from information processing and protein biosynthesis. Notably, says Huber, "Neither the inner nor the outer membrane of I. hospitalis alone satisfies all the criteria of a cytoplasmic membrane." Although the outer membrane has a primary proton pump and contains ATP synthase, the inner membrane contains and surrounds the biochemical components necessary for information processing and biosynthesis. This arrangement raises the fundamental question of how to define cytoplasmic membranes generally, as well as in Ignicoccus.
Indeed, the cell structure of this archaeon is unlike that of any known bacterium but strikingly similar to that of eukaryotes. These differences make I. hospitalis a prime candidate for being a eukaryotic ancestor, one that could provide ATP and other molecules to an incorporated symbiont without the need for any interactions between the cytoplasm of either it or the host. "This work also sheds light on the interaction between I. hospitalis (‘the friendly fire sphere') and its companion archaeon, Nanoarchaeum equitans (‘the riding dwarf'), which has the smallest archaeal genome known and lacks nearly all metabolic and biosynthetic genes," says Ulf Küper, the research team's lead scientist. N. equitans grows exclusively on the surface of I. hospitalis, and the central question is how energy is transferred from host to rider. "Having ATP formation in the periplasm of I. hospitalis avoids the complex import of energy across three membranes into N. equitans," Küper says.
The need for easy energy transfer from I. hospitalis to the nanoarchaeon may even have driven the evolution of its novel cellular architecture. "Archaea are full of surprises, as would be expected from organisms with such extreme survival talents," says Schaechter, who believes that many more surprises are in store.
Marcia Stone
Marcia Stone is a science writer based in New York City. More of her work can be seen at http://www.mstoneworks.net.
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