Sir

In the Connections Essay 'Disappearing act' (Nature 446, 983; 2007), James A. Lake discusses the evolution of the eukaryotic cell from the perspective of the origin of the eukaryotic gene content. As he points out, there are two main gene classes in prokaryotes (archaea and bacteria): operational genes, for “day-to-day processes of cell maintenance”; and informational genes, that “convert information from DNA into proteins”. Eukaryotes are derived from archaea and bacteria, but curiously, archaeal operational genes and bacterial informational genes are almost completely absent from the eukaryotic genome. Lake suggests that “because two types of ribosomal genes cannot exist in the same nucleus, the archaebacterial ribosome may simply have been the lucky survivor when one of the components in the eubacterial ribosome was inactivated.” But, Lake asks his readers, why were the archaebacterial operational genes eliminated?

One hypothesis is that the archaeal and bacterial cells that merged to form the eukaryotic cell were 'metabolically incompatible', and consequently their merger resulted in the elimination of the archaeal operational genes. But what, then, was the basis for this 'metabolic incompatibility' and for the bacterial genes to finally get the upper hand? David Valentine has suggested that adaptations to energy stress dictate the ecology and evolution of archaea (Nature Rev. Microbiol. 5, 316–323; 2007). The biochemical mechanisms enabling archaea to cope with chronic energy stress include structural (a less ion-permeable membrane) and metabolic (pathways highly adapted to niches with low energy availability) components.

We suggest that during eukaryogenesis, the bacterial endosymbiont, which gradually became the mitochondrion, ended the chronic energy stress in the proto-eukaryote. In contrast to the anaerobic archaeal host, the aerobic bacterial endosymbiont was able to maximize the availability of energy and gradually become an efficient energy-converting organelle, the 'powerhouse' of the eukaryotic cell. The proto-eukaryotic metabolism had to be reorganized accordingly. The unique archaeal adaptations to chronic energy stress were no longer advantageous, and were out-competed by the 'higher energy'-adapted bacterial metabolism. Lateral gene transfer from organisms other than the two founders certainly contributed to the eukaryotic gene repertoire, but we think that operational genes mostly originated from bacterial donors because the archaeal genes were incompatible with the energy-rich environment of the eukaryotic cell.

To return to Lake's Essay, the two faces of the eukaryotic gene content (the Janus paradox) might reflect two types of incompatibilities between its two prokaryotic founders: structural incompatibility between the informational systems; and environmental (or ecological) incompatibility between the metabolic systems. These eventually led to the synergetic, two-faced, chimaeric result — the eukaryotic cell.