Prediction of the archaeal exosome and its connections with the proteasomeand the translation and transcription machineries by a comparative-genomicapproach

By comparing the gene order in the completely sequenced archaeal genomes co mplemented by sequence profile analysis, we predict the existence and prote in composition of the archaeal counterpart of the eukaryotic exosome, a com plex of RNAses, RNA-binding proteins, and helicases that mediates processin g and 3'->5' degradation of a variety of RNA species. The majority of the p redicted archaeal exosome subunits are encoded in what appears to be a prev iously undetected superoperon. In Methanobacterium thermoautotrophicum, thi s predicted superoperon consists of 15 genes; in the Crenarchaea, Sulfolobu s solfataricus and Aeropyrum pernix, one and two of the genes From the supe roperon, respectively, are relocated ill the genome, whereas in other Eurya rchaeota, the superoperon is split into a variable number of predicted oper ons and solitary genes. Methanococcus jannaschii partially retains the supe roperon, but lacks the three core exosome subunits, and in Halobacterium sp ., the superoperon is divided into two predicted operons, with the same thr ee exosome subunits missing. This suggests concerted gene loss and an alter ation of the structure and function of the predicted exosome in the Methano coccus and Halobacterium lineages. Additional potential components of the e xosome are encoded by partially conserved predicted small operons. Along wi th the orthologs of eukaryotic exosome subunits, namely an RNase PH and two RNA-binding proteins, the predicted archaeal exosomal superoperon also enc odes orthologs of two protein subunits of RNase P. This suggests a function al and possibly a physical interaction between RNase P and the postulated a rchaeal exosome, a connection that has not been reported in eukaryotes. In a pattern of apparent gene loss complementary to that seen in Methanococcus and Halobacterium, Thermoplasma acidophilum lacks the RNase P subunits. Un expectedly, the identified exosomal superoperon, in addition to the predict ed exosome components, encodes the catalytic subunits of the archaeal prote asome, two ribosomal proteins and a DNA-directed RNA polymerase subunit. Th ese observations suggest that in archaea, a tight Functional coupling exist s between translation, RNA processing and degradation, (apparently mediated by the predicted exosome) and protein degradation (mediated by the proteas ome], and may have implications for cross-talk between these processes in e ukaryotes.