Archaebacterial DNA-dependent RNA polymerases testify to the evolution of the eukaryotic nuclear genome.

Abstract

Genes for DNA-dependent RNA polymerase components B, A, and C from the archaebacterium Sulfolobus acidocaldarius and for components B", B', A, and C from the archaebacterium Halobacterium halobium were cloned and sequenced. They are organized in gene clusters in the order above, which corresponds to the order of the homologous rpoB and IpoC genes in the corresponding operon of the Escherichia coli genome. Derived amino acid sequences of archaebacterial components A and C were aligned with each other and with the sequences of corresponding (largest) subunits from the archaebacterium Methanobacterium thermoautotrophicum, with sequences of various eukaryotic nuclear RNA polymerases I, 1, and Ill, and with the sequence ofthe 1' component from E. coli Phylogenetic relations between the primary kingdoms of life have been established using rRNA as an evolutionary chronometer (1, 2). RNA polymerase appears to be an appropriate alternative because it is ubiquitous, highly conserved, and a complex macromolecule. We have cloned and sequenced the genes for the large RNA polymerase components of two phylogenetically distant archaebacteria: the sulfur-dependent extreme thermophile Sulfolobus acidocaldarius (Su. acidocaldarius) and the extreme halophile Halobacterium halobium. Eukaryotes possess three specialized nuclear RNA polymerases (pol I, II, and III) thought to be derived from one ancestral "urkaryotic" enzyme by diversification (3). Archaebacteria should provide an independent outside reference, in addition to eubacteria, for elucidating the origin of the eukaryotic lineage.DNA-dependent RNA polymerases from archaebacteria are of two types (4, 5). The BAC type (largest subunits arranged in order of decreasing size) is found in the sulfurdependent extreme thermophiles (6), including the Thermococcales (7), and in the genus Thermoplasma, which belongs to the second major branch of the archaebacterial kingdom (1). The AB'B"C type, characterized by a split B component, is common to the methanogens and extreme halophiles, other representatives of the second major branch. Immunochemical cross-reactivity indicates that the two (or three) largest components of eubacterial, eukaryotic nuclear, and archaebacterial RNA polymerases are homologous (4, 8). Interkingdom homologies between smaller components, including the archaebacterial C subunits, have not yet been ascertained.The complex component patterns of archaebacterial RNA polymerases, comprising around 10 subunits each, resemble those of the nuclear eukaryotic rather than the more streamlined eubacterial enzymes. Accordingly, immunochemical cross-reactivity was larger between archaebacterial and eukaryotic components than between archaebacterial and eubacterial components (8), and the consensus sequences of putative promoters of archaebacterial stable RNA and protein genes (9, 10) are strikingly similar to those of eukaryotic promoters for RNA polymerase II (11).Here we compare the derived amino acid sequences of components A and C from three archaebacteria with eac...

The complete genome of the crenarchaeon Sulfolobus solfataricus P2

“…64). The archaeal and eukaryal polymerases are closely related in subunit complexity and sequence (65,66). Fourteen RNA polymerase subunits are encoded by 8 loci: rpoDN (Sso0071, 5140), rpoHB-ЈBЈЈAAЈЈ(Sso5468, 0227, 3254, 0225, 0223), rpoG (Sso0277; ortholog of S. acidocaldarius RpoG) (67), rpoL (Sso5577), rpoEЈEЈЈ (Sso0415, 5798), rpoF (Sso0751; ortholog of M. thermoautotrophicum rpoF) (68), rpoK (Sso6768) and rpoP (Sso5865; ortholog of M. thermoautotrophicum rpoP) (68).…”

Evolution of the RNA polymerase II C-terminal domain

“…The largest of these subunits contains eight highly conserved domains, designated regions A through H (2), which are common to all prokaryotic and eukaryotic homologues (3). Unlike all other members of this protein family, however, the largest subunit of eukaryotic RNA pol II has an additional C-terminal domain (CTD), comprising a varied number of tandemly repeated heptapeptides with the consensus sequence Tyr-1-Ser-2-Pro-3-Thr-4 -Ser-5-Pro-6 -Ser-7 (4).…”

Lineage‐specific partitions in archaeal transcription

“…Evidence from sequence similarity studies between RNA polymerases suggests that archaeal transcription shared certain components with that of the Eukarya (Puhler et al 1989), a conclusion further supported by the discovery of TFIIB in Pyrococcus furiosus (Ouzounis and Sander 1992) and TBP in P. woesei (Rowlands et al 1994). The strong similarity of archaeal transcription initiation factors with their eukaryotic counterparts has reinforced the concept that these domains shared an ancestral transcriptional apparatus.…”

“…Furthermore, these analyses may reveal how archaea respond to environmental challenges, in particular, given their possible association with various aspects of human disease (Eckburg et al 2003). Several previous studies have shown that the RNA polymerase core enzyme exhibits structural similarity between the Archaea and the Eukaryota (Puhler et al 1989). Moreover, the minimal set of factors required for in vitro transcription initiation in archaea consists of TATA-box binding protein (TBP), TFIIB and RNA polymerase II (Werner and Weinzierl 2002).…”

“…Moreover, the minimal set of factors required for in vitro transcription initiation in archaea consists of TATA-box binding protein (TBP), TFIIB and RNA polymerase II (Werner and Weinzierl 2002). In bacteria, however, the process appears to be fundamentally different (Struhl 1999), with regulation accomplished by an entirely different set of proteins (Gralla 1996).Evidence from sequence similarity studies between RNA polymerases suggests that archaeal transcription shared certain components with that of the Eukarya (Puhler et al 1989), a conclusion further supported by the discovery of TFIIB in Pyrococcus furiosus (Ouzounis and Sander 1992) and TBP in P. woesei (Rowlands et al 1994). The strong similarity of archaeal transcription initiation factors with their eukaryotic counterparts has reinforced the concept that these domains shared an ancestral transcriptional apparatus.…”