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Biochemical Society Transactions (2011) Volume 39, part 1
Nucleoid-associated proteins in Crenarchaea
Rosalie P.C. Driessen and Remus Th. Dame1
Leiden Institute of Chemistry, Gorlaeus Laboratories, Laboratory of Molecular Genetics and Cell Observatory, Leiden University, P.O. Box 9502, 2300 RA
Leiden, The Netherlands
Abstract
Architectural proteins play an important role in compacting and organizing the chromosomal DNA in all
three kingdoms of life (Eukarya, Bacteria and Archaea). These proteins are generally not conserved at
the amino acid sequence level, but the mechanisms by which they modulate the genome do seem to be
functionally conserved across kingdoms. On a generic level, architectural proteins can be classified based
on their structural effect as DNA benders, DNA bridgers or DNA wrappers. Although chromatin organization
in archaea has not been studied extensively, quite a number of architectural proteins have been identified.
In the present paper, we summarize the knowledge currently available on these proteins in Crenarchaea.
By the type of architectural proteins available, the crenarchaeal nucleoid shows similarities with that of
Bacteria. It relies on the action of a large set of small, abundant and generally basic proteins to compact
and organize their genome and to modulate its activity.
Introduction
Organisms of all three kingdoms of life (Bacteria, Archaea
and Eukarya) need to organize and compact their genomic
DNA to reduce its dimensions below that of a cell or a
nucleus. Yet the genetic material needs to be flexibly and
dynamically organized to permit DNA-based processes such
as transcription, replication and repair.
Genome compaction in archaea is currently poorly
understood. The size of the archaeal genome is in the order
of megabases, comparable with that of bacteria, and also the
micrometre-sized dimensions of the cell are shared. Archaea
compact their genomic DNA into a structure generally
referred to as the nucleoid, which is not membrane-enclosed.
Compaction is achieved by a diverse set of architectural
proteins associated with the nucleoid. None of these proteins
is conserved among all archaeal species, and most of the ones
identified to date have a limited phylogenetic distribution
(Figure 1).
The two main archaeal phyla, Euryarchaea and Crenarchaea, employ mechanistically different approaches to
organize and compact their genome. Euryarchaea synthesize
histone homologues, which, by wrapping DNA, form
nucleosomal beads-on-a-string-like structures in vitro [1].
Therefore compaction of the genome in species of this
phylum is considered to be similar to that in eukaryotes. In
eukaryotes, these nucleosomal filaments arrange into 30 nm
fibres, which are subject to further higher-order compaction.
Crenarchaea do not synthesize histone homologues (with
rare exceptions), but instead employ a wide array of small
NAPs (nucleoid-associated proteins). Genome organization
Key words: Archaea, architectural protein, chromatin, Crenarchaea, nucleoid, nucleoid-associated
protein.
Abbreviations used: Alba, acetylation lowers binding affinity; CC1, crenarchaeal chromatin
protein 1; EM, electron microscopy; MCM, minichromosome maintenance; NAP, nucleoidassociated protein.
1
To whom correspondence should be addressed (email [email protected]).
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Authors Journal compilation in these species is considered to be similar to that of bacteria.
In bacteria, NAPs organize the genome predominantly
by bending or bridging DNA [2]. The DNA-bridging
activity is likely to be involved in forming higherorder looped structures representing topologically isolated
domains. The DNA within these domains is additionally
compacted because of the presence of supercoils [3]. Hardly
anything is known about higher-order organization in
archaea. However, considering the functional conservation
of chromatin proteins with homologues from both bacteria
and eukaryotes, it is likely to show similarities in higher-order
structures as well.
Architectural proteins in general modulate the spatial path
of the DNA by wrapping, bridging or bending it. These
properties, rather than sequence homology, appear to be
conserved among kingdoms [3]. Not only do the architectural
properties of these proteins explain compaction, they also
provide a framework for understanding how different
proteins can work together in providing a dynamic genome.
The delicate interplay between architectural proteins (e.g.
related to their differential expression in different conditions)
permits them to modulate the degree of compaction and
thereby regulate the accessibility of the genomic DNA for
different DNA-based processes.
A few words on euryarchaeal histones
Although covering euryarchaeal nucleoid organization and
compaction in detail is not the scope of the present review,
some key aspects are given in this section. This information
will aid the reader in grasping the differences in the archaeal
kingdom and the similarities of the euryarchaeal phylum to
eukaryotes in genome compaction. Euryarchaea encode two
homologues of eukaryotic core histones. Whereas eukaryotic
histones assemble as octamers, archaeal histones arrange
themselves into tetrameric structures, composed of two
Biochem. Soc. Trans. (2011) 39, 116–121; doi:10.1042/BST0390116
Molecular Biology of Archaea II
Figure 1 Phylogenetic distribution of the main chromatin
Alba
proteins in Archaea
Besides Sac10a, homologues of this protein (such as Sso10a) are
The most widely distributed NAP in Crenarchaea is
Alba (acetylation lowers binding affinity). It has been
identified in all crenarchaeal species sequenced so far. In
addition, homologues of the Alba family are found in most
euryarchaeal species. This protein was originally identified
in Sulfolobus acidocaldarius and Sulfolobus solfataricus as
Sac10b and Sso10b respectively, but later renamed to Alba.
Alba is a small (10 kDa) basic protein, highly abundant
in these species, comprising ∼5 % of cellular proteins,
corresponding roughly to one Alba dimer per 5 bp. Alba
exists as a dimer (Figure 2A) in solution and binds cooperatively without apparent specificity to DNA. Models of
Alba binding to DNA predict interaction of the body
of the dimer with the major groove, flanked by additional
interactions of the individual β-hairpins of the monomers
with the minor groove [11]. EM (electron microscopy)
studies have shown the formation of two structurally
different types of Alba–DNA complexes depending on
the concentration of the protein. At low and intermediate
concentrations, Alba bridges DNA duplexes, resulting in
compaction because of the formation of looped structures.
At high protein concentrations, the protein coats DNA fully,
giving rise to stiff filaments [12,13], which, at first sight, do
not seem to be involved in compaction.
Binding of Alba to DNA can be modulated by its
acetylation/deacetylation at a single residue, Lys16 , situated at
the DNA-binding surface (hence the name Alba). Acetylation
of Alba by acetyltransferase Pat [14], reducing the positive
charge of the binding surface, decreases the binding affinity
to DNA approx. 30-fold [11,15]. The action of Sir2 leads to
deacetylation of this residue and restores the DNA-binding
affinity of Alba. It has been suggested that binding of
Alba represses transcription. Switching of the acetylation
status at Lys16 could provide a mechanism to regulate the
binding affinity of the protein and thus its ability to repress
transcription. Indeed, acetylation of Alba relieves repression
of transcription and deacetylation restores it in vitro [14,15].
In addition to hindering transcription, binding of Alba to
DNA probably affects any other DNA-based processes.
For instance, Alba possibly interferes with replication. It
has been shown that progression of the helicase MCM
(minichromosome maintenance) is impeded on Alba–DNA
complexes in vitro. Also, in this case, acetylation of Alba
reduces its binding to DNA and therefore allows MCM to
unwind DNA [16]. The switching of the acetylation status of
Alba thus emerges as an important mechanism in modulating
DNA accessibility.
A number of archaeal species encode two Alba homologues. For instance, S. solfataricus expresses Alba1, which
is highly conserved, and Alba2, which is less conserved.
Alba2 is expressed at levels 20-fold lower than that
of Alba1 [13]. The exact role of Alba2 is not known, but
the data currently available suggest that it modulates the
activity of Alba1. At physiological conditions, Alba2 is found
uniquely as heterodimer with Alba1. These heterodimers
only form bridged DNA–protein complexes, and even at
represented in the same Sac10a division.
dimers [4]. The tetramer assembled on the DNA wraps
approx. 90 bp of DNA around its surface [5], in contrast
with the ∼150 bp found in eukaryotic nucleosomes [6].
Archaeal histones lack the N- and C-terminal tails that are
subject to post-translational modifications in their eukaryotic
counterparts [7,8]. Such modifications are key to modulating
chromatin compaction in eukaryotes in relation to gene
expression. In Euryarchaea, the same could be accomplished
by varying the stoichiometry of the two expressed histone
proteins in the tetramer. As the composition of the tetramers
affects the DNA-binding affinity, varying expression levels
of individual histone monomers provides a mechanism to
regulate transcription. Indeed, in some species, the expression
level of the different histone proteins is dependent on growth
conditions [9].
NAPs in Crenarchaea
Crenarchaea encode a variety of small, abundant and
generally basic architectural proteins that modulate their
genome [10]. Although these proteins are not universally
conserved among all Crenarchaea, each species contains at
least two NAPs (generally a bender and a bridger) to jointly
compact the genomic DNA and modulate the accessibility
of the genome. In this section, we give an overview of the
proteins identified and, if known, of their architectural and
biochemical properties. Unfortunately, data regarding the
in vivo functionality of these proteins are scarce.
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Biochemical Society Transactions (2011) Volume 39, part 1
Figure 2 Structures of crenarchaeal nucleoid-associated proteins
(A) Crystal structure of an Alba homodimer. Lys16 residues are depicted as spheres. (B) Crystal structure of a Sso10a dimer.
(C) Co-crystal structure of Sul7 with an 8 bp DNA fragment. (D) Co-crystal structure of Cren7 with an 8 bp DNA fragment.
Images were prepared using PyMOL (DeLano Scientific; http://www.pymol.org) and PDB codes 1H0X, 1XSX, 1AZQ and 3LWH
respectively.
high concentrations do not assemble into the coated DNA
filaments seen with Alba1 homodimers. These differences
in DNA binding observed for the Alba heterodimer and
homodimer can probably be attributed to changes in dimer–
dimer interactions. The likely interaction surface is highly
conserved in Alba1, but not in Alba2. Similar to the effects
seen with Alba2, a substitution in the Alba1 dimer/dimer
interface (Phe60 to Ala) leads to a decrease in effective DNAbinding affinity [17]. These results underline the important
role of dimer–dimer interactions in formation of densely
packed protein–DNA filaments. Changing the ratios of Alba1
and Alba2 might be another mechanism by which to regulate
gene expression next to Alba1 acetylation.
Several Alba homologues that lack the key residue in modulating Alba binding to DNA (Lys16 ) have been identified.
Ape10b2 from Aeropyrum pernix and Mma10b from the
euryarchaeal Methanococcus maripaludis are the only ones
characterized [18,19]. Owing to the absence of Lys16 , the
DNA-binding affinity of these Alba homologues cannot be
modulated by changing the acetylation status at this site.
Interestingly, Mma10b exhibits a preference for sequencespecific binding to DNA; its binding site corresponds to
an AT-rich palindrome of 18 bp [18]. It is less abundant
(∼0.01 % of total cellular proteins) than other architectural
proteins and has a low affinity for generic DNA. It has been
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Authors Journal compilation shown in ChIP-chip (chromatin immunoprecipitation on
chip) studies that Mma10b-binding sites locate within genes.
Deletion mutants of Mma10b in this species show up/downregulation of some 15 genes, similar to Mvo10b-deletion
mutants in Methanococcus voltae [20]. The relatively low
expression levels of Mma10b compared with Alba, together
with its sequence-specific binding, suggest that Mma10b
has evolved towards a more specific role in transcription
regulation deviating from the primary role of Alba proteins
in genome compaction.
Sac10a
Sac10a homologues are widely distributed among Crenarchaea and also encoded in some euryarchaeal species.
Similarly to Alba, this protein has been shown to facilitate
DNA bridging in EM studies [12]. Little is known
about Sac10a at the biochemical level and about how
it contributes to genome compaction. However, some
characteristic features are evident in the structure of the
protein. The protein exists in solution as homodimer and its
dimerization occurs via an antiparallel coiled coil (Figure 2B).
The DNA-binding winged helix structures are on opposite
sides of the coiled coil [21,22]. This arrangement of the dimer
probably facilitates the DNA bridging observed [12].
Molecular Biology of Archaea II
Sul7
Sulfolobus species express a number of highly conserved
architectural proteins of ∼7 kDa, which are collectively
referred to as Sul7 proteins. Every species encodes one to
three genes (resulting from gene duplications) for Sul7. Sul7
proteins are expressed at high levels (up to 5 % of the total
cellular protein). They are highly basic and bind to DNA
without apparent sequence specificity.
Sul7 is a simple protein, consisting of two antiparallel βsheets and a C-terminal α-helix [23]. It exists as a monomer in
solution and the monomer is also the form in which it binds
to DNA (Figure 2C). Binding of Sul7 to DNA is facilitated
by insertion of one of the β-sheets into the minor groove with
concomitant intercalation of Val26 and Met29 . The binding of
the protein results in a DNA bend of approx. 66◦ [23,24].
The binding of Sul7 also affects local DNA topology, as the
distortion of the DNA results in the constraint of negative
supercoiling [25].
Sul7 is subject to post-translational modifications. It is
methylated on several lysine residues. Differently from Alba,
these modifications do not change the DNA-binding affinity
of the protein. Instead, this modification might help to protect
the protein from thermal denaturation, as Sul7 methylation is
found to increase after heat shock [26]. Sul7 can also protect
DNA from thermal denaturation, as DNA–Sul7 complexes
have an increased melting temperature compared with bare
DNA [27]. This protection is relevant in the light of the
hyperthermophilic natural habitat of Sulfolobus species.
Some additional functions have been proposed for Sul7.
In addition to protecting itself from denaturation, Sul7 has
been shown to ensure integrity and activity of other proteins
in vitro. Sul7 is able to disaggregate proteins that have
been denatured by high temperatures in an ATP-hydrolysisdependent manner [28,29]. Sul7 has also been shown to be
able to repair UV-induced damage. Upon exposure to UV, a
conserved tryptophan residue at the DNA-binding interface
is oxidized and acts as an electron donor. This electron can
subsequently be transferred to a thymidine dimer, which leads
to the reversal and thus repair of the thymidine dimer [30].
It remains to be shown whether either of these activities is
relevant in vivo.
Cren7
Cren7 is an architectural protein found in almost all
crenarchaeal species. It is interesting to note that Cren7 is
absent from only the few crenarchaeal species that encode
histone proteins (e.g. Thermofilum pendens [31,32]). It was
discovered only recently as a gene product co-purifying with
Sul7 [33]. The two proteins are completely different at the
level of amino acid sequence, yet very similar in structure and,
not unexpectedly, in biochemical properties. As many other
architectural proteins, Cren7 is abundantly expressed (1 %
of cellular protein) and has no apparent sequence specificity.
Since Cren7 is highly conserved in crenarchaea, it is likely
to play a key role in chromatin organization and gene
regulation.
As mentioned, the structure of Cren7 resembles that of
Sul7. It contains two antiparallel β-sheets and an extended
flexible loop (Figure 2D). The major differences between
Cren7 and Sul7 are the C-terminal α-helix unique to Sul7
and the aforementioned loop present only in Cren7.
Cren7 binds to DNA through one of the β-sheets and the
flexible loop. Its DNA binding is similar to that of Sul7 with
the β-sheet inserted into the minor groove and Leu28 and
Val36 intercalating. As a consequence, binding of Cren7 to
DNA induces a bend of approx. 53◦ . Binding of Cren7 also
constrains negative supercoils, yet twice as efficiently as Sul7
[32].
CC1 (crenarchaeal chromatin protein 1)
CC1 is yet another small (6 kDa) basic DNA-binding protein.
It was discovered in a search for single-stranded-DNAbinding proteins in archaeal species and found to bind singlestranded and double-stranded DNA with equal affinities [34].
CC1 and its homologues have been found in a limited number
of species: Thermoproteus tenax, Pyrobaculum aerophilum
and Aeropyrum pernix. It exists in solution and binds to DNA
as a monomer. The only structural information available
is that CC1 is rich in β-sheet structure. It is unknown
how this protein binds to DNA, but it constrains negative
supercoiling and increases the melting temperature of duplex
DNA [19].
Future prospects
It is fair to say that our understanding of the archaeal
nucleoid is limited. It is based mostly on data from in vitro
experiments and extrapolation from our knowledge of the
bacterial nucleoid and eukaryotic chromatin. Nevertheless,
together, this provides a good framework for building structural models of archaeal nucleoid organization. Currently,
such models cannot go much further than incorporating
the activities of individual NAPs on DNA. Evidently, there
is a need for more information regarding the action of
these proteins in vivo, in vitro and in silico. The questions
that await an answer in the close future are related to the
interplay of different NAPs in modulating genome structure
and accessibility, and the possible existence of higher-order
structures.
A thorough understanding can only be reached if an
integrated approach is taken where knowledge obtained at
different scales is combined. With the advent of singlemolecule techniques, such as optical or magnetic tweezers, it
is now possible to identify the general architectural properties
of a chromatin protein, such as bending, bridging or
wrapping the DNA, in a straightforward manner [35]. For instance, the force–extension curve of a protein–DNA complex
(the typical outcome of a micromanipulation experiment)
provides a ‘signature’ of such generic properties (Figure 3)
[36–38]. In addition, the data obtained from such studies can
give detailed quantitative kinetic information about protein–
DNA interactions. A first level of added complexity, and
the first step to understanding in vivo genome dynamics, is
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Biochemical Society Transactions (2011) Volume 39, part 1
Figure 3 Simulations of force–extension curves: signatures of DNA–protein complexes corresponding to ‘model representatives’ from
the three classes of architectural proteins
The worm-like chain model [39] was used with a DNA persistence length, lP , of 50 nm and a DNA contour length,
l0 , of 16 μm for bare DNA (dashed curves). The DNA extension is expressed relative to the DNA contour length (x/l0 ).
(A) DNA-bending proteins condense DNA by inducing localized bends, causing a decrease in effective persistence length. (lP =
35 nm, dotted curve; lP = 20 nm, continuous curve). Note that dense packing of chromatin proteins on DNA can result
in an opposite effect and stiffen the DNA, resulting in a shift of the force–extension curve towards larger extensions.
(B) DNA-bridging proteins form looped structures along the DNA, compacting the molecule by decreasing the effective
contour length. Exerting a force on the DNA results in disruption of the loops (in these simulations, with sizes of 350, 70,
100 and 80 nm respectively). (C) DNA-wrapping proteins wrap DNA around their surface. The force–extension curve displays
seven DNA-wrapping proteins [in these simulations, each wrapping 100 bp (34 nm)], which are released from the DNA
molecule at a critical force of 20 pN. (D) Schematic overview of the three classes of architectural proteins: DNA benders,
DNA bridgers and DNA wrappers.
to study the joint action of multiple architectural proteins
using these methods. The detailed knowledge obtained at the
single-molecule level alone is not sufficient. It is essential
to obtain direct information on the situation in vivo. This
can be achieved by using microarray or deep-sequencingbased techniques that probe genome-wide binding and
gene activity. Modern high-resolution imaging techniques
can yield important information of nucleoid structure at
the single-cell level. Evidently, each of these techniques
relies heavily on the availability of tools to manipulate
the genetic material in the archaeal species of interest.
Structural and kinetic information, integrated with twodimensional and three-dimensional position information of
(sets of) architectural proteins will form the basis of accurate
predictive models of spatial genome organization.
C The
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Authors Journal compilation Acknowledgments
We are grateful to Mariliis Tark-Dame and Nora Goosen for
comments and a critical reading of the paper. We apologize to those
people whose interesting publications could not be cited owing to
the defined scope of this work and size constraints.
Funding
This work was financially supported by NWO (Netherlands
Organization for Scientific Research) through a Vidi grant to R.T.D.
[grant number 864.08.001].
Molecular Biology of Archaea II
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Received 16 August 2010
doi:10.1042/BST0390116
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