Extrachromosomal element capture and the evolution of multiple replication origins in archaeal chromosomes.
In all three domains of life, DNA replication begins at specialized loci termed replication origins. In bacteria, replication initiates from a single, clearly defined site. In contrast, eukaryotic organisms exploit a multitude of replication origins, dividing their genomes into an array of short contiguous units. Recently, the multiple replication origin paradigm has also been demonstrated within the archaeal domain of life, with the discovery that the hyperthermophilic archaeon Sulfolobus has three replication origins. However, the evolutionary mechanism driving the progression from single to multiple origin usage remains unclear. Here, we demonstrate that Aeropyrum pernix, a distant relative of Sulfolobus, has two origins. Comparison with the Sulfolobus origins provides evidence for evolution of replicon complexity by capture of extrachromosomal genetic elements. We additionally identify a previously unrecognized candidate archaeal initiator protein that is distantly related to eukaryotic Cdt1. Our data thus provide evidence that horizontal gene transfer, in addition to its well-established role in contributing to the information content of chromosomes, may fundamentally alter the manner in which the host chromosome is replicated.
Robinson
Nicholas P
NP
Medical Research Council Cancer Cell Unit, Hutchison Medical Research Council Research Center, Hills Road, Cambridge CB2 0XZ, United Kingdom. npr22@hutchison-mrc.cam.ac.uk
Bell
Stephen D
SD
D041522:Aeropyrum / Q000235:genetics; D000595:Amino Acid Sequence; D019843:Archaeal Proteins / Q000737:chemistry / Q000235:genetics / Q000302:isolation & purification; D001483:Base Sequence; D018797:Cell Cycle Proteins / Q000235:genetics; D019847:Chromosomes, Archaeal / Q000235:genetics*; D018983:DNA Footprinting; D004261:DNA Replication / Q000235:genetics*; D004268:DNA-Binding Proteins / Q000235:genetics; D019143:Evolution, Molecular; D005111:Extrachromosomal Inheritance / Q000235:genetics*; D019766:Genes, Archaeal; D008969:Molecular Sequence Data; D016366:Open Reading Frames / Q000235:genetics; D051738:Origin Recognition Complex; D017434:Protein Structure, Tertiary / Q000235:genetics; D018741:Replication Origin / Q000235:genetics*; D012093:Replicon / Q000235:genetics; D015183:Restriction Mapping; D029701:Saccharomyces cerevisiae Proteins / Q000235:genetics; D017386:Sequence Homology, Amino Acid; D012689:Sequence Homology, Nucleic Acid; D016945:Sulfolobus acidocaldarius / Q000235:genetics; D048229:Sulfolobus solfataricus / Q000235:genetics
D019843:Archaeal Proteins; D018797:Cell Cycle Proteins; D004268:DNA-Binding Proteins; D051738:Origin Recognition Complex; D029701:Saccharomyces cerevisiae Proteins; C499592:TAH11 protein, S cerevisiae