Archaeal Histones, Nucleosomes, and Transcription Initiation

Abstract

Methanobacterium thermoautotrophicum and Methanobacterium formicicum, and five in Methanococcus and Charles J. Daniels Department of Microbiology jannaschii, two of which are plasmid-encoded (Bult et al., 1996;Grayling et al., 1996). In most cases, the pri-Ohio State University Columbus, Ohio 43210 mary sequences of the archaeal histones within one species are more similar to each other than to the sequences of histones in other Archaea, indicating that the original histone gene has undergone different num-The packaging of nuclear DNA by histones into nucleobers of duplications during the divergence of different somes and chromatin is a feature as definitive of the euryarchaeal lineages. To date, only histone-like DNA-Eucarya as the nuclear membrane, and determining how binding proteins have been identified in members of the eucaryal RNA polymerases access promoters buried Crenarchaeota (Grayling et al., 1996). Fifteen complete within nucleosomes and initiate transcription is currently archaeal histone sequences are available, and the resi-an area of considerable research interest. Bacteria condues on the interacting hydrophobic faces of their ␣ tain "histone-like" proteins (Schmid, 1990), but despite helix 2s are very highly conserved (-A15---L14A15--L12---this designation, these are not histone-like and do not A 13 --I 12 A 13 --A 14 V 13 --A 15 --A 15 -[hyphens indicate amino acid form DNA-protein complexes structurally related to the residues between the identified residues; see Figure 1]), nucleosome. Bacterial RNA polymerases do not, theresuggesting that all homodimer and heterodimer partner-fore, appear to face the same promoter-access problem, ships may still be possible, although some partnerships and bacterial RNA polymerases are structurally simpler may be preferred, or may even have been fixed. The than their eucaryal counterparts. What about Archaea?residues at these positions in the eucaryal core histones As detailed below, although Archaea lack a nuclear are hydrophobic, but they are more variable and gener-membrane, they do contain histones that compact DNA ally bulkier, and space and interaction constraints iminto nucleosome-related structures, and archaeal RNA posed by these different R groups presumably direct polymerases have the multisubunit complexity of eucarthe correct eucaryal histone heterodimerization and pre-yal RNA polymerases (Langer et al., 1995). They also clude homodimerization. require the participation of homologs of eucaryal TATA-Histone-fold domains do not occur exclusively in his-binding protein (TBP) and transcription initiation factor tones but have also been identified in both positive and IIB (TFIIB) to initiate transcription.negative transcription regulators (Burley et al., 1997). Histone sequences and the structure of the nucleo-The subunits of the CCAAT-binding transcriptional actisome are universally conserved in Eucarya, and histones vators, CBF-A (HAP3 in yeast) and CBFC (HAP5), associ-and their method of DNA compaction must therefore ate through histone-fold pairin...

The transcriptional activator GvpE for the halobacterial gas vesicle genes resembles a basic region leucine-zipper regulatory protein

“…This is in accord with the ®nding that the basic transcription machinery and promoter sequences of archaea closely resemble their eukaryal counterparts (Reeve et al, 1997). The study of archaeal gene regulation is still in its infancy, but as more regulatory factors are identi®ed, the more we will learn about the phylogenetic development of the eukaryal transcription machinery.…”

“…In addition, archaeal promoters contain a TATA-box sequence located approximately 27 nucleotides upstream of the transcription initiation site (Hain et al, 1992;Langer et al, 1995). Like in eukarya, transcription initiation involves the action of TATA-box binding proteins (TBP) and transcription factors (TFII), but the mechanism appears to be somewhat simpler, since the archaeal system requires only the homologs of the eukaryal TBP and TFII B for accurate initiation, and the TFII E and TFII H required for eukaryal transcription initiation are not present (Thomm, 1996;Reeve et al, 1997;Qureshi et al, 1997). While the basic archaeal transcription machinery has been investigated in some detail, insight into the regulation of gene expression in archaea is still scarce.…”

On the origins of cells: a hypothesis for the evolutionary transitions from abiotic geochemistry to chemoautotrophic prokaryotes, and from prokaryotes to nucleated cells

“…Another change is that histones, which are present in methanogens and relatives (Reeve et al 1997;Fahrner et al 2001) as well as in eukaryotes, are sketched onto the host's chromosomes. Another change is that inventions specific to the eukaryotic lineage are symbolized as green dots.…”

The neomuran origin of archaebacteria, the negibacterial root of the universal tree and bacterial megaclassification.

“…In eukaryotes, which ancestrally had four core histones and H1, supercoiling is negative. Archaebacteria probably never had more than two core histones (Reeve et al, 1997). The archaebacterial cenancestor took the extra step into hyperthermophily, further modifying its chromatin.…”