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Archaea. 2007 May; 2(2): 117–125. Published online 2006 November 20. | PMCID: PMC2686387 |
Copyright © 2006 Heron Publishing—Victoria, Canada Lineage-specific partitions in archaeal transcription Richard M.R. Coulson,*1 Nathalie Touboul,2 and Christos A. Ouzounis3 1 Microarray Group, The European Bioinformatics Institute, Wellcome Trust Genome Campus, Hinxton, Cambridge CB10 1SD, U.K. 2 ALCIMED, 84 boulevard Vivier Merle, 69 485 Lyon Cedex 03, France 3 Computational Genomics Unit, Institute of Agrobiotechnology, Center for Research and Technology Hellas, Thessalonica, 57001 Greece Received September 13, 2006; Accepted October 23, 2006.
The phylogenetic distribution of the components comprising the
transcriptional machinery in the crenarchaeal and euryarchaeal
lineages of the Archaea was analyzed in a systematic manner by
genome-wide profiling of transcription complements in fifteen complete
archaeal genome sequences. Initially, a reference set of
transcription-associated proteins (TAPs) consisting of sequences
functioning in all aspects of the transcriptional process, and
originating from the three domains of life, was used to query the
genomes. TAP-families were detected by sequence clustering of the TAPs
and their archaeal homologues, and through extensive database
searching, these families were assigned a function. The phylogenetic
origins of archaeal genes matching hidden Markov model profiles of
protein domains associated with transcription, and those encoding the
TAP-homologues, showed there is extensive lineage-specificity of
proteins that function as regulators of transcription: most of these
sequences are present solely in the Euryarchaeota, with nearly all of
them homologous to bacterial DNA-binding proteins. Strikingly, the
hidden Markov model profile searches revealed that archaeal chromatin
and histone-modifying enzymes also display extensive
taxon-restrictedness, both across and within the two phyla.
Keywords: genome profiling, protein families, sequence clustering, transcription-associated proteins
Transcription, a core gene expression process, involves different agents
participating in initiation, elongation, termination and regulation. The
basic principles of transcriptional regulation in the Bacteria and
Eukaryota have been outlined ( Ptashne
and Gann 1997), contrasting with the Archaea, where such
mechanisms are less well-understood. The study of the archaeal
transcriptional machinery is important to an understanding of both the
molecular mechanisms, and the evolutionary history, of transcriptional
regulation in all three domains of life. 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). 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. However, a
rigorous comparison with bacteria was not performed until entire
archaeal genomes became available. It was then shown that archaea
contain a significant proportion of bacterial transcripional regulators,
in addition to their eukaryotic-like transcription initiation factors
( Kyrpides and Ouzounis 1999), for
example Lrp ( Kyrpides and Ouzounis
1995) and sigma-70 ( Kyrpides and
Ouzounis 1997). Notably, the only transcriptional components
common to all three domains of life are the two largest RNA polymerase
subunits, SIR2, NifL and TenA ( Coulson
et al. 2001), the latter found fused with the metabolic enzyme
ThiD in eukaryotes ( Ouzounis and
Kyrpides 1997). With 15 archaeal genomes, encompassing a wider
range of genera from the two main archaeal lineages, a systematic
analysis of the archaeal transcriptional machinery would test the
robustness of the assumption that bacterial-type regulators and
eukaryotic initiation factors co-exist in the Archaea
( Bell et al.
2001a).
The reference sequence dataset of transcription-associated proteins
(TAPs) was extracted from SwissProt and TrEMBL from entries containing
the word “transcription” in their description and keyword
records, as previously described ( Coulson
and Ouzounis 2003, Coulson et al.
2004). Searching and linking database records was facilitated by
SRS ( Etzold et al. 1996). From a
total of 9874 TAP sequences, 4654 are bacterial, 4907 are eukaryotic and
313 are archaeal. Archaeal genomes were obtained from the COGENT
database ( Janssen et al. 2003).
The following fifteen fully sequenced and published archaeal genome
sequences were used (strain names after comma, COGENT identifiers in
parentheses): Archaeoglobus fulgidus, DSM4304
(AFUL-DSM-01), Aeropyrum pernix, K1 (APER-XK1-01),
Halobacterium sp., NRC-1 (HALO-NRC- 01),
Methanosarcina acetivorans, C2A (MACE-C2A-01),
Methanoccocus jannaschii, DSM 2661 (MJAN-DSM-01),
Methanopyrus kandleri, AV19 (MKAN-AV1-01),
Methanosarcina mazei, Go1 (MMAZ-GO1-01),
Methanobacterium thermoautotrophicum, deltaH
(MTHE-DEL-01), Pyrococcus abyssi, GE5 (PABY-GE5-01),
Pyrobaculum aerophilum, IM2 (PAER-IM2-01),
Pyrococcus horikoshii, OT3 (PHOR-OT3- 01),
Sulfolobus solfataricus, P2 (SSOL-XP2-01),
Sulfolobus tokodaii, Str. 7 (STOK-XX7-01),
Thermoplasma acidophilum, DSM1728 (TACI-DSM-01) and
Thermoplasma volcanium, GSS1 (TVOL-GSS-01). There is
only one complete nanoarchaeotal genome available, and its uniqueness
precluded it from the intra-lineage analyses performed in these studies.
The TAP reference dataset was compared against the fifteen archaeal
genomes (36,194 sequences) using BLASTp with an E-value
cut-off of 10 –6
( Altschul et al. 1997), after
being filtered for composition bias with CAST
( Promponas et al. 2000). For each
archaeal genome, the numbers of both the TAP-homologues and
matching-reference TAPs were recorded (see
Table 1). The 1938 archaeal
proteins and 2634 TAPs thus obtained (4572 in total) were clustered
using the TRIBE-MCL algorithm ( Enright
et al. 2002), i.e., only the TAPs matching archaeal proteins
(2634 in number) and these archaeal homologues (1938 in number) were
clustered by sequence similarity. To assess the effect of granularity,
two runs were performed with inflation values of 2.0 and 5.0, as
previously described ( Coulson and
Ouzounis 2003). The distribution of both singletons and families
across the Archaea and the reference dataset was examined (see
Table 2).
| Table 1.
BLASTp search results using the reference set to query fifteen
archaeal genomes.
|
| Table 2.
Distribution of TRIBE-MCL protein families. Shown are the number
of identified families at inflation values of 2.0 and 5.0,
corresponding to different granularities (see Methods).
|
To further establish the validity of this approach, a parallel analysis
was conducted with hidden Markov model (HMM) profiles from the Pfam
database (version 7.8) ( Bateman et al.
2004). The Pfam accession numbers associated with the 9874
reference TAPs were used to link directly to 508 unique Pfam entries.
The fifteen archaeal genomes were queried with HMM profiles, using
“hmmsearch” from the software package HMMER
( Eddy 1998). Hits were considered
significant if their score against the corresponding HMM profile was
above a trusted cut-off value, equivalent to the lowest-scoring known
member of the Pfam alignment. Of the 508 profiles, 173 have detected
homologues in archaea, of which 115 are not involved in transcription.
The remaining 58 profiles, defined as TA-HMMs, were validated by their
InterPro records to confirm that they were transcription-related.
The 9874 reference TAP sequences extracted from SWISS-PROT and TrEMBL
identified 1938 proteins in the fifteen archaeal genomes
( Table 1). On average, about 5%
of the genomes matched the reference set, with some slight variation;
the TAP matches identified by BLASTp represent about 4% of the gene
content of the Crenarchaeota, and about 6% of the gene content of the
Euryarchaeota. This observation suggests that the TAP complement of the
Crenarchaeota is more divergent from the reference set than that of the
Euryarchaeota ( Table 1). However,
in both archaeal divisions, the abundance of TAP hits appears to
increase with genome size.
The extent of sequence divergence between the detected archaeal proteins
and the sequences in the reference set was examined by sequence
clustering analyses performed on the BLASTp similarity search results.
The clustering operations were implemented at inflation values of 2.0
and 5.0, corresponding to different granularities; the lower value
produces larger clusters, containing more distantly related sequences.
With an inflation value of 2.0, clustering results in 281 families of
which 179 (64%) contain at least one TAP and one archaeal sequence
( Table 2). With an inflation
value of 5.0, clustering results in 632 families of which 179 (28%) also
contain at least one TAP and one archaeal sequence. In this second case,
243 singletons were generated (38% of all clusters,
Table 2). Hence, attention was
focused on clusters generated with an inflation value of 2.0 because
these are both more accurate and broader than clusters generated with a
larger inflation value ( Coulson and
Ouzounis 2003). Similar parameter settings have been shown to
result in a precision of >90% for InterPro, and >80% for SCOP
families ( Enright et al. 2002).
Lineage specificity and functional classification
Clusters generated by TRIBE-MCL correspond to protein families whose
members are related by common function. Thus, the 179 TAP-containing
clusters generated at an inflation value of 2.0
( Table 2), and containing at
least one TAP and one archaeal homologue, were annotated manually
based on the description records of SwissProt obtained via SRS
( Etzold et al. 1996). After
this step, 119 clusters were found to be directly related to the
transcriptional process, corresponding to 906 archaeal sequences.
These transcription-associated (TA-) clusters were examined in terms
of the role played in the transcriptional process by their TAP members
and the phylogenetic origins of both the TAP and archaeal sequences
( Table 3). The term
“phylogenetic origin” refers to the phylogenetic domain to
which a TAP belongs, and in which lineage the archaeal homologue is
observed.
| Table 3.
Functional classification and taxonomic distribution of families
containing both TAPs and their archaeal homologues. Definitions:
TAP domain = phylogenetic domain (Archaea = ARC, Bacteria = BAC,
(more ...) |
Analysis of the phylogenetic origins of the TAPs in the TA-clusters
showed that in just over 80% of the families (97 clusters) the TAPs
are found only in prokaryotic genomes
( Table 3). In ~44% (i.e., 43
out of 97 families) and ~37% (36 families) of these TA-clusters, the
TAP members of an individual cluster originate solely from either the
Archaea (A) or the Bacteria (B), respectively. TAP members in the
remaining ~19% of these TA-clusters originate from both the archaeal
and bacterial domains (AB); so, each of these 18 families contains at
least one archaeal and one bacterial TAP. Strikingly, in 89 out of the
97 families (~92%) whose TAPs are present only in prokaryotes (A, B
and AB families), the TAPs function as transcriptional regulators
(listed as ‘Regulators’ in
Table 3): in the B and AB
families, the role of every TAP member is to regulate transcription,
and in ~82% of the A families, the TAP members perform the same
regulatory role. This finding highlights the prevalence of regulators
of prokaryotic origin in the Archaea.
The above pattern contrasts with the other 22 TA-clusters, which
contain TAPs present in the Eukaryota (codes with E in
Table 3). In 10 of these
families (~46%) the TAPs comprise RNA polymerase subunits, and in six
families (~27%) they function as basal transcription factors,
corresponding to a total of 73% of families involved in transcription
initiation and synthesis. This compares with just 8% (8 out of 97) of
families of prokaryotic origin that contain TAPs of identical
function. Hence, few archaeal sequences show homology to eukaryotic
regulators of transcription and bacterial proteins associated with RNA
synthesis. However, even though a large number of archaeal sequences
exhibit homology to bacterial transcriptional regulators, there
appears to be a substantial proportion of archaeal-specific regulatory
factors represented by the archaeal families (A families in
Table 3).
The 119 TA-clusters exhibit a high degree of lineage-specificity; ~63%
(27 cases) and ~81% (29 cases) of the A and B families,
respectively—the majority of which are transcriptional
regulators—detect archaeal homologues that are unique to
Euryarchaeotal genomes ( Table
3). This contrasts with the TA-clusters containing TAPs
originating from the Eukaryota, where the opposite pattern is
observed: ~83% and ~60% of the AE and ABE families, respectively,
contain archaeal homologues present in both the Crenarchaeota and
Euryarchaeota. Furthermore, in over four fifths of these phylogenetic
classes of TA-clusters (14 out of 17 families), the TAP members
function as either subunits of RNA polymerase or basal transcription
factors.
However, among the prokaryotic (A, B and AB) families, two-thirds (64
out of 97) contain archaeal homologues present only in the
Euryarchaeota, whereas in 25 (about one-quarter) of such clusters the
TAP homologues originate from both archaeal phyla. Very few of these
families (~8%, 8 out of 97) have as members archaeal TAP homologues
that are present uniquely in the Crenarchaeota. The vast majority of
the A, B and AB families (>90%, 89 families) contain TAPs that
function as regulators and are mostly present in Euryarchaeota only.
In particular, all the TAPs in the B families are DNA-binding
proteins, and >80% of their families possess only Euryarchaeota
sequences ( Table 3). These
functional and taxonomic distribution patterns suggest that there are
either fewer (known) Crenarchaeota-specific sequences associated with
the control of transcription, or that such sequences are more diverged
from the bacterial-type regulators in the Euryarchaeota.
Protein domain representation in archaeal phyla
The TRIBE-MCL clustering analyses were complemented by querying the
archaeal genomes with 58 HMM profiles that had been validated to be
associated with the transcriptional process (TA-HMMs). A large
proportion of sequences were identified by both procedures,
corresponding to 600 proteins and 81 clusters.
( Table 4 displays for each
genome the number of TAP-homolgues detected by each method
individually, and the number detected by both methods.) Additionally,
the two methods of TRIBE-MCL clustering and HMM profile searches
uniquely detect 306 and 239 proteins, respectively
( Table 4). This degree of
overlap indicates a consistent identification of the
transcription-associated gene complement in the archaeal genomes under
consideration ( Table 4). Fewer
proteins associated with the transcriptional process were found in the
Crenarchaeota than in the Euryarchaeota (~2.40% versus ~3.39%;
Table 4). The presence of
nearly 1.5-fold more TAP-homologues in the Euryarchaeota is highly
significant ( P < 2×10 –7,
Fisher’s exact test). Furthermore, a slight,
monotonically-increasing relationship of TAP-homologue abundance with
genome size is observed ( Tables
1 and 4 and
). This correlation is
significant for the euryarchaeal genomes ( P <
0.05, Spearman rank correlation), even though M.
acetivorans, containing the highest number of
protein-encoding genes, exhibits a similar percentage to M.
thermoautotrophicum and P. abyssi, with much
smaller genomes ( Table 4 and
).
| Table 4.
TAP-homologue abundance in the Crenarchaeota and Euryarchaeota
genomes. Definitions: MCL, the number of TAP-homologues detected
by the TRIBE-MCL clustering; MCL & HMM, the number of
(more ...) |
The twenty-one TA-HMMs representing eleven of the twelve polypeptides
that constitute RNA polymerase, match approximately equivalent
abundances of genes in the Crenarchaeota and Euryarchaeota genomes
(~0.44% versus ~0.53% respectively: 49 out of 11,120 and 132 out of
25,074 sequences). Genes encoding subunits A′, A²,
B′, B², D, E, H and N are detected in all fifteen of the
archaeal species by the profile-based method (Supplementary
Table 1). Only matches to
subunits F, K and L were not observed in all genomes; F is not
detected in two of the crenarchaeal ( P. aerophilum
and S. tokodaii) and just one of the euryarchaeal
genomes ( M. kandleri), whereas L exhibits the
opposite pattern and is undetected in P. horikoshii,
T. volcanium (both euryarchaeotes) and P.
aerophilum (a crenarchaeote), with a homologue of K absent
only from P. horikoshii. This apparent absence of
only a small number of RNA polymerase subunits probably arises from
their diverged nature as genes encoding these proteins have been
observed in these species ( Brochier et
al. 2004). Furthermore, nearly identical phylogenetic
distributions are observed with the RNA polymerase families detected
by the TRIBE-MCL clustering (Supplementary
Table 2), suggesting little
sequence divergence between the RNA polymerase subunits of the
euryarchaeota and crenarchaeota.
Significantly more sequences in the Euryarchaeota match TA-HMMs of
proteins associated with the initiation complex, and transcription
elongation and termination, than in the Crenarchaeota
(): ~0.18% of genes in
crenarchaeal genomes (20 genes) and ~0.30% of genes in euryarchaeal
genomes (75 genes) encode such transcription factors
( P < 0.05, Fisher’s exact test). This
difference can mainly be accounted for by the highly amplified
TATA-box binding protein (TBP, PF00352) and TFIIB (TFB, PF00382) gene
families in Halobacterium sp.
( Baliga et al. 2000). The
Halobacterium sp. genome contains (when normalized
for genome size) ~4.5-fold and ~2.6-fold more genes encoding TBP and
TFB, respectively, than the average for this phylum (see
; namely 42.2 copies per
10,000 genes versus an average of 9.3 for TBP and 26.9 versus 10.4 for
TFB). Sequences with homology to the eukaryotic basal transcription
factor TFIIE-alpha (TFE, PF02002) are observed in every archaeal
species except Thermoplasma, and the transcription
elongation TFIIS (TFS, PF01096) is detected in all archaeal genomes
except M. kandleri, as previously noted by
Brochier et al. (2004). Hence,
there appears to be little sequence divergence of these four basal
transcription factors across the two archaeal phyla. However,
sequences homologous to bacterial transcription termination factors
are not widespread in the Archaea: the anti-termination factor NusB
(PF01029) is found in only four euryarchaeal genomes including
M. kandleri, where there are three homologues, and
NusG is found in only one crenarchaeote ( S.
solfataricus) and one euryarchaeote ( M.
thermoautotrophicum).
The lack of taxon-restrictedness exhibited by RNA polymerase subunits
and basal transcription factors contrasts sharply with proteins that
bind DNA nonspecifically and modulate chromatin structure
(). Sequences encoding
archaeal histones (PF00808) are found in all Euryarchaeota genomes
except those of T. acidophilum and T.
volcanium, where instead the bacterial histone-like HU
protein (PF00216) is present. Even though HU protein is ubiquitous and
highly conserved across the bacterial kingdom
( Sagi et al. 2004), no
homologues were observed in the other nine euryarchaeal genomes. None
of these proteins associated with compacting prokaryotic chromosomes
(archaeal histones and HU protein) are found in the Crenarchaeota.
Sequences belonging to the histone deacetylase (HDAC) family (PF00850)
are observed in the Crenarchaeota, and all of the euryarchaeal species
except Thermoplasma, resulting in the phylogenetic
distribution of these HDAC homologues being identical to that of the
TFE. None of the HDAC-matching sequences are detected by the TA-HMM
representing Sir2 (PF02146), a histone deacetylase present in all
three domains of life: the profile identifies Sir2 homologues in all
Crenarchaeota species and the four Euryarchaeota genomes that contain
homologues of NusB. Hence, the proteins that function to fold DNA, and
those that control this process, exhibit considerable diversity across
the archaeal domain.
A high degree of phylum-specificity is observed with sequences
matching the 24 transcriptional regulator TA-HMMs
(). There are 127
(~1.14%) and 396 (~1.58%) sequences in Crenarchaeota and Euryarchaeota
genomes, respectively, that match these profiles, suggesting that the
Euryarchaeota contain nearly 1.5-fold more sequences homologous to
well-characterized bacterial proteins associated with controlling gene
expression than do the Crenarchaeota ( P ≥
0.0014, Fisher’s exact test). Of the three regulator TA-HMMs
that match the highest number of archaeal genes
(), there are nearly
twice the number of euryarchaeaotal as crenarchaeotal sequences (when
genome size is accounted for) encoding metalloregulatory repressors
(ArsR, PF01022) and specific regulators of amino acid metabolism
(AsnC/Lrp, PF01037), with sequences homologous to those involved in
the bacterial two-component signal transduction system being absent
from the Crenarchaeota (response regulator receiver domain, PF00072).
In conjunction with the functional and phylogenetic analyses of the
TA-clusters ( Table 3), the
profile searches imply that the Crenarchaeota contain significantly
fewer sequences with homology to well-characterized bacterial
repressors than do the Euryarchaeota.
The pattern of elevated abundance of sequences homologous to bacterial
regulators in the Euryarchaeota () is also observed with proteins containing the LysR
(PF00126), MarR (PF01047), TetR (PF00440) and the iron-dependent
repressor (PF01325) DNA-binding domains. The only exception to this
trend is a domain (PF04014) present in the Bacillus
subtilis abrB and spoVT genes that control developmental gene
expression: curiously, twice the number of Crenarchaeotal genes
contain this domain than do Euryarchaeotal genes. The TA-HMMs detected
no bacterial transcriptional regulators with homologues confined to
the Crenarchaeota, contrasting with the Euryarchaeota where nitrogen
regulatory protein P-II (PF00543), the transcriptional regulator Phage
shock protein C (PspC, PF04024) and bacterial metalloregulatory
proteins controlling the transcription of mercury resistance operons
(MerR, PF00376) have homologues in two or more of the euryarchaeaotal
genomes.
The only eukaryotic DNA-binding domain identified in the archaeal
genomes was a variant of the C2H2-zinc finger (PF00096), that detected
a total of 17 sequences across all Crenarchaeota and six Euryarchaeota
species. However, Halobacterium—the only
non-thermophile analyzed—appears most
“bacteria-like” in its complement of transcriptional
regulators; it is the only species with homologues of cold-shock
protein (PF00313), Crp (PF00325) and region 2 of s70
(PF04542). Therefore, although nearly all the archaeal transcriptional
regulators identified are related to bacterial repressors, there is
considerable heterogeneity across, and within the two phyla in the
types of regulator families present within a particular species.
The genome-wide profiling of archaeal transcription that was performed
indicates that the Euryarchaeota have more proteins associated with the
transcriptional process than do the Crenarchaeota. Furthermore, in both
phyla, there is a trend showing that TAP-homologue abundance increases
with genome size, i.e., smaller genomes appear to contain
proportionately fewer transcription factors than larger ones. Evidence
of this type of correlation has also been observed in bacteria
( Cases et al. 2003). Although a
number of functional classes associated with RNA synthesis and
transcription initiation are shared both between and within the known
archaeal phyla, there are a number of surprising lineage-specific
patterns that have not previously been systematically characterized:
both the proteins that constitute archaeal chromatin and histone
modifying enzymes, as well as transcriptional regulators—which are
major contributors to the lineage-specificity—display extensive
sequence diversity across the archaeal domain.
Genes encoding eleven out of the twelve RNA polymerase subunits are
observed in all fifteen archaeal genomes, with a few exceptions
( Slesarev et al. 2002). Subunit F
(identified only with the profile-based method) is not observed in three
genomes; however, its eukaryotic functional and structural equivalent,
Rpb4 ( Werner et al. 2000), is not
essential for cell viability in yeast
( Woychik and Young 1989). The
other two subunits that were not found in all of the analysed genomes
are K and L, which appear to be absent only from P.
horikoshii as homologues of L are detected by the TRIBE-MCL
clustering in P. aerophilum and T.
volcanium. These data imply that RNA polymerase is very highly
conserved in the Archaea.
Transcription initiation in archaea resembles the eukaryotic process in
its requirement for TBP, TFB (the archaeal version of eukaryotic TFIIB)
( Soppa 1999,
Reeve 2003) and TFE (an archaeal
protein homologous to the N-terminal region of the a subunit of
eukaryotic TFIIE) ( Bell et al.
2001b, Hanzelka
et al. 2001). Genes encoding these three basal transcription
factors are present in all of the genomes, with the only notable absence
being that of TFE from T. acidophilum and T.
volcanium. However, no archaeal genes encoding homologues of
TAFs ( Qureshi et al. 1997) or
TFIIE (subunit b), TFIIF and TFIIH
( Ouhammouch 2004) were
identified. TBP is usually encoded by a single copy gene, though
Halobacterium sp. contains eleven copies
( Ng et al. 2000), with three
genes in M. acetivorans and M. mazei
coding for this canonical transcription factor. The
Halobacterium genome also contains multiple copies of
TFB-encoding genes (seven), as do half of the other genomes that contain
either two or three copies. Hence, the identification of multiple copies
of TBP and TFB genes in a range of archaeal species supports the
hypothesis that different types of transcriptional regulation occur in
response to environmental challenges
( Goo et al. 2004), although the
role of multiple TBPs and their relationship with multiple TFBs is not
yet clear ( Galagan et al. 2002).
The archaeal nucleosome appears to display extensive taxon variablity:
with the exception of the Thermoplasma (whose genomes
encode bacterial HU-like proteins), the Euryarchaeota use homologues of
histones H3 and H4 to assemble chromatin
( Geiduschek and Ouhammouch 2005),
contrasting with the Crenarchaeota where completely different sets of
proteins compact the genome (e.g., Alba in S.
solfataricus ( Bell et al.
2002)). It is interesting to note, given the apparent lack of
histones in Thermoplasma, that no homologues of members
of the HDAC family, Sir2 or TFE are present in the genomes of T.
acidophilum and T. volcanium. Sir2 homologues
are present in all the Crenarchaeotal genomes, but only in the same four
Euryarchaeotal genomes as NusB. This may suggest some association
between RNA chain elongation and histone deacetylation, as both TFIIE
and NusB function in the elongation process, and in eukaryotes many
factors can influence transcript elongation on chromatin templates
( Sims et al. 2004). This
heterogeneity in the constituents of archaeal chromatin is unexpected as
trypanosomatids contain the four core histones, and possess a range of
chromatin-remodeling activities, also present in mammals even though
there is considerable evolutionary distance between the two eukaryotic
taxa ( Ivens et al. 2005).
The elevated abundance in euryarchaeal genomes of proteins associated
with the transcriptional process arises, predominately, from the
increased number (when genome size is accounted for) of sequences
homologous to bacterial transcriptional regulators within these genomes
(). Members of the AsnC/Lrp
family of regulators have been shown to act as both repressors and
activators of archaeal transcription
( Geiduschek and Ouhammouch 2005),
though whether chromatin remodeling and histone modification play an
important role in the control of gene expression, as in eukaryotes, is
not known. DNA-compacting proteins and HDACs are observed in all
archaeal species except T. acidophilum and T.
volcanium, which are only distantly related to the extreme
halophilic and methanogenic euryarchaeotes
( DeLong 2000). Instead,
Thermoplasma contain the bacterial HU-protein, making
transcriptional control in this archaeal group reminiscent of Bacteria,
i.e., the genomic DNA is readily accessible to DNA-binding proteins,
resulting in the default expression state of a gene being
“on” ( Struhl 1999).
This could be in contrast to the other Euryarchaeota and the
Crenarchaeota, where the default state is “off” because of
genome compacting by chromatin.
Nearly all the Crenarchaeota studied have shown a high degree of niche
specialization (most are hyperthermophiles) and, like parasitic
protozoa, which occupy only a limited range of environments, appear to
contain far fewer proteins that regulate transcription than do organisms
adapted to a wider range of environmental conditions
( Coulson et al. 2004,
Ivens et al. 2005). At present, a
lack of experimental data makes it impossible to determine whether the
Crenarchaeota possess significant numbers of lineage-specific
transcriptional regulators or whether they just contain fewer of the
bacterial-type compared with the Euryarchaeota. Nonetheless, these
results are consistent with previous genome profiling studies of
transcriptional complements, which show that the greater the
evolutionary separation between taxa, the greater the
taxon-restrictedness of the TAP-families
( Coulson and Ouzounis 2003).
Table S1. Number of archaeal genes matching domains present in RNA polymerase subunits.
Table S2. RNA polymerase subunit gene copy number in archaeal
genomes.
R.M.R.C. and C.A.O. thank the Medical Research Council for supporting
this work through a Special Training Fellowship in Bioinformatics to
R.M.R.C.
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