Mol Gen Genet (1988) 212:382-385
© Springer-Verlag 1988
An unlinked 5 S ribosomal RNA gene
in the archaebacterium, Thermococcus celer
Doreen E. Culham and Ross N. Nazar
Department of Molecular Biology and Genetics, University of Guelph, Gueph, Ontario, Canada N1G 2Wt
Summary. We have determined the nucleotide sequence of
an unlinked 5 S rRNA gene region from a thermophilic
archaebacterium, Thermococcus celer. This 5 S rRNA gene
is flanked by a single tRNA Asp sequence and appears to
be transcribed as part of a very short operon consisting
of only two gene sequences. Comparative studies indicate
features in the 5' and 3' flanking sequences, which bear
similarity with promoter and termination signals in eubac-
teria, but also reflect unusual features found in at least
some archaebacteria. The evolution of this unlinked operon
and the unusual features are discussed.
Key words: Thermococcus celer - Unlinked 5 S rDNA
Nucleotide sequence
In all organisms, the mature large ribosomal RNA compo-
nents (16-18 and 23~8 S rRNAs) are cleaved from a com-
mon precursor molecule. In eubacteria, the 5 S RNA se-
quence is also transcribed as part of this common precursor
(see Nomura and Post 1980) but the 5 S RNA of the eukar-
yotic cytoplasmic ribosome is transcribed from a separate
gene by an alternative RNA polymerase III (see Nazar
1982). Although not co-transcribed, in lower eukaryotes
such as Saccharomyces, the 5 S genes remain linked to the
rDNA as part of the same repeating DNA unit; in higher
eukaryotes this association is entirely absent. Because these
evolutionary changes are both substantial and intriguing
they are the subject of considerable speculation. Since alter-
native 5 S genes are activated during different states of de-
velopment in at least some eukaryotes (see Brown and
Schlissel 1985) the possibility exists that some of these evo-
lutionary changes may be directed towards cellular regula-
tion.
Recent studies (Jarsch et al. 1983; Neumann et al. 1983;
Wich et al. 1984) on the organization of ribosomal RNA
genes in archaebacteria have revealed at least three organ-
isms; Methanococcus, Sulfolobus and Thermococcus, with
extra, apparently unlinked, 5 S rRNA genes. As these could
represent early examples in the evolution of unlinked 5 S
RNA genes further study has been undertaken. In two
strains of Methanococcus, DNA cloning and sequencing
(Wich et al. 1984, 1987) has shown that the unlinked gene
is localized in a cluster of tRNA gene sequences and may
Offprint requests to. R.N. Nazar
E H X U S X P P C SX X C X P T AA H C T S E
T Y V ¥ T Y ~r ¥ Y YT ¥ ¥ ¥ Y Y VY ¥ ¥ y y Y
I ID ii
i D 11 I , ~ : I It
0 2 0.4 0 0.SKb
Fig. 1. Determination of the nucleotide sequence for an unlinked
5 S rRNA gene region from Thermococcus celer. A 2-Kb EcoRI
(E) fragment containing the unlinked 5 S rRNA gene was isolated
by plaque hybridization from a 2 Charon 3A genomic library,
and subcloned using the pBR322 cloning vector. The nucleotide
sequence for a 1,055-base portion of this fragment was determined
by further cleaving the EeoRI fragment with restriction endonucle-
ase CfoI (C), HinfI (H), HaeIII (A), HpaII (P), SstI (S), StuI (U),
TaqI (T), or XhoI (X) and degrading it chemically by the sequenc-
ing techniques of Maxam and Gilbert (1980). The arrows indicate
the direction and extent of the sequences that were obtained
be expressed as part of a separate operon. In this study
an unlinked gene in a second genus of archaebacterium,
Thermococcus celer, has been isolated and characterized.
Sequence analyses indicate that this 5 S RNA gene is, ap-
parently, part of a much smaller operon and may be co-
transcribed with a single tRNA Asp sequence.
An earlier study on the 5 S rRNA genes of T. celer
(Neumann et al. 1983) suggested that in this organism one
type of 5 S DNA sequence was linked with the 16 and
23 S rDNAs in a very large (> 20 kb) genomic EcoRI-diges-
tion fragment while a second, unlinked copy, was present
in a much shorter 2-kb fragment. To clone this shorter
fragment specifically, DNA was extracted (Cryer et al.
1975) from Thermococcus celer cells, strain Vu13, DMS
2476 (generously provided by W. Zillig) and a ~ Charon
3A vector (Blattner et al. 1977) was used to construct a
genomic library, thereby excluding the much longer EcoRI-
digestion fragment. DNA from a complementary plaque
(2Ch 3A-TC2000) was digested with EcoRI endonuclease
and further subcloned into pBR322; colony hybridization
was used to select complementary clones (see Maniatis et al.
1982). As indicated in Fig. 1, subsequent cleavages with
restriction enzymes and hybridization analyses (Bittner
et al. 1980; Seed 1982) were used to identify complementary
fragments and prepare them for sequence determination
(Maxam and Gilbert 1980). About 1 kb of sequence was
determined (Fig. 2) including the 5 S rRNA sequence and