Archaeal Genomics: An Overview

A striking feature of the M. jannaschii genome was the high fraction of genes, about 50%, that match nothing in the sequence databases. Although some of these are likely to remain unique to M. jannaschii, others should turn out to be characteristic of the Archaea as a whole or various major subgroups thereof. Currently, a number of examples are known of genes that span the phylogenetic breadth of the Archaea, but have no counterparts in the Bacteria or eukaryotes. When a full crenarchaeal genome sequence becomes available, many more such cases are expected. The large number of genes confined to Archaea attests to the group's uniqueness and to the challenge that archaeal metabolism presents to the biochemist.In the broader perspective, group-specific genes point the way to taxonomy's future. The day is ending when relationships among major taxa can be based on the phylogeny inferred for one or a few molecules (a method that all too often focuses on arcane debates over details, while failing to reinforce the remarkably broad areas of consensus). A systematics based on molecular phylogenies must cope with the facts that not all genes in an organism's genome share the same evolutionary history and that not all genes can be effectively used for phylogenetic analysis—some trees differ because the gene histories are different, others because they are merely uncertain. With full genomes, many organismal groups will be clearly defined in terms of large sets of shared unique genetic traits; organisms belonging to a taxon so defined would each possess a substantial fraction of the genes in the set, while those not within the group would possess few if any of them. In this respect, we think it improbable that the numerous genes shared by Archaea and Eucarya, but absent in Bacteria, were all present in the Universal Ancestor and subsequently lost in the ancestral bacterial stem (sometimes to be replaced by a separately invented functional analog).In the present context we have made no attempt to summarize or explain the similarities of the metabolic genes that seem to specifically unite Archaea and Bacteria. In some instances there is no recognizable homolog in the Eucarya, while in others there is simply a greater similarity of the archaeal-bacterial pair. Numerically, these Bacteria-related genes constitute a greater fraction of the M. jannaschii genome than do the genes (including most of those for replication, transcription and translation) that appear to unite the Archaea and the Eucarya. We have suggested that the former could result from the degeneration of metabolic capacity in the eukaryotic lineage (Olsen and Woese 1996xOlsen, G.J and Woese, C.R. Trends Genet. 1996; 12: 377–379Abstract | Full Text PDF | PubMed | Scopus (43)See all ReferencesOlsen and Woese 1996). It is important to ask whether this interpretation can be reconciled with our argument that the bacterial information processing system is not a simplified version of a more complex ancestral form (as seen in the Archaea and Eucarya). Most of our reasons for accepting a eukaryotic metabolic simplification, but not a bacterial informational streamlining, are that the former presents a relatively uniform, consistent picture, while the latter comprises numerous, often conflicting, vignettes. A broader, more representative sampling of genomes will be needed to resolve this issue.The evolutionary picture emerging from genomics, as we retrace our ancestry further and further back into the past, is an unsettling, yet entrancing one. Looking back toward the Universal Ancestor, the simple world of distinct organismal lineages and a robust, well-defined connection between genotype and phenotype—foundation stones of biology—loses its substance, dissolving in the turbulent evolutionary dynamic that shaped genotype, phenotype, and their connection. From the information processing systems seems to emerge a consistent, informative, and satisfying picture of cellular evolution and that of the primary lines of descent. Although far from chaotic, metabolism seems an evolutionary morass—a sure sign of conceptual revolution and enlightenment to come. In this history-laden world of microbial genomics, the evolutionary perspective necessarily changes from one of teasing ourselves with speculation to that of teasing out the grandest history of all.