Genetically Enhanced Archaean Challenges Three-Domain Evolutionary Tree

Researchers have discovered two related gene fragments and one almost-whole genome that, when metagenomically reconstructed, reveal a previously unknown complex archaeon. This particular archaeon appears to be the closest living relative of eukaryotes—cells with enclosed nuclei and internal power-generating organelles that make up all currently known fungi, plants, and animals on Earth today. This finding represents a serious challenge to the traditional three-domain tree of life composed of Bacteria, Archaea and Eukaryota—all similarly primordial—and strongly favors a twodomain evolutionary tree in which eukaryotes are placed together with a diverse group of archaea in the TACK (Thaumarchaeota, Aigarchaeota, Crenarchaeota, and Korarchaeota) superphylum from which they are thought to have evolved. Simonetta Gribaldo, at Institut Pasteur in Paris, whose work supports the two-domain tree, says this latest discovery has “very important consequences because it shows that an organism with characteristics of a modern archaeon could be the starting point for eukaryogenesis.” Thijs Ettema, at Uppsala University in Sweden, who led the discovery team that identified what he describes as a quintessential archaeon with a “whole bunch of eukaryotic genes,” named it Lokiarchaeum, after Loki’s Castle, the field of deep-sea volcanic vents between Greenland and Norway where evidence of its existence was found. “In Norse mythology, the shape-shifting deity Loki is described as complex and confusing; thus, Lokiarchaeota is a very fitting name for our typical prokaryotic that encodes a variety of important eukaryotic proteins, including actin, [which] enables present-day amoeba to stalk and engulf their prey,” Ettema says. The hunt is now on for living Lokiarchaeota and proof that they can hunt down and ingest other cells. Meanwhile, Ettema speculates that actin might have given a long-ago ancestor a way to internalize that one special alpha-proteobacterium that evolved into a mitochondrion that eventually gave eukaryotes enough internal power to become multicellular. What Ettema and colleagues do say without reservation in their recent Nature article is that “the genes in Lokiarchaeota, especially those enabling membrane remodeling and intracellular trafficking, indicate that the onset of cellular complexity was already underway before the acquisition of a mitochondrial endosymbiont.” They also argue that the advanced genetic talents found in Lokiarchaeum provided the archaeal ancestor of eukaryotes with the “starter kit” for cellular complexity. Not surprisingly, the concept of a tworather than the traditional three-domain tree of life has stirred much controversy among microbial evolutionists. In contrast to Gribaldo, for example, Norm Pace and his colleagues at the University of Colorado, in Boulder, strongly support the threebranched tree developed by Carl Woese, the founder of modern evolutionary microbiology. Woese and collaborators invented ribosomal RNA (rRNA) typing, proved that archaea were not bacterial, and gave them a domain of their own in his tree of life. Archaea, in fact, appear more biochemically akin to eukaryotes than they do to bacteria. However, they differ from eukaryotes in a number of critical properties, says Pace. “One of the most telling differences is in membrane lipid chemistry: Eukaryotes use bacterial-like ester-linked and archaea ether-linked lipids,” he explains. “The enzymatic machineries behind membrane biosynthesis in eukaryotes and archaea are also distinct, implying distinct evolutionary origins as well,” according to Pace’s colleagues Charles Robertson and J. Kirk Harris, who also defend the three-domain universal tree, which separates the eukaryotic and archaeal lines prior to archaeal radiation. Therefore, eukaryotes could not be derived from archaea, they add. “Woese’s rRNA-based phylogeny is likely to be correct,” wrote the late Christian deDuve in his 2005 book Singularities. “This is not just a case of beginner’s luck, but the outcome of a perceptive choice. Ribosomal RNAs go back to the very beginnings of life, they are highly conserved and, as parts of a complex interlocked machinery of fundamental importance, they are likely to have been transferred exclusively by direct, vertical inheritance.” Emphasizing the importance of this discussion, microbial evolutionist J. Jeffrey Morris at the University of Alabama, at Birmingham, says that “knowing how bacteria, archaea, and eukaryotes are related will allow us to ‘root’ the tree of life, and that, in turn, will help us understand what sort of organism (or preorganismal entity) the last universal common ancestor of all living things was. In other words, it could help us understand what life was like in the world’s earliest days.”