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Molecular Biology of Archaea II
Bacterial and eukaryotic systems collide in the
three Rs of Methanococcus
Richard P. Parker, Alison D. Walters and James P.J. Chong1
Department of Biology (Area 5), University of York, York YO10 5DD, U.K.
Abstract
Methanococcus maripaludis S2 is a methanogenic archaeon with a well-developed genetic system. Its
mesophilic nature offers a simple system in which to perform complementation using bacterial and
eukaryotic genes. Although information-processing systems in archaea are generally more similar to those
in eukaryotes than those in bacteria, the order Methanococcales has a unique complement of DNA
replication proteins, with multiple MCM (minichromosome maintenance) proteins and no obvious originbinding protein. A search for homologues of recombination and repair proteins in M. maripaludis has revealed
a mixture of bacterial, eukaryotic and some archaeal-specific homologues. Some repair pathways appear to
be completely absent, but it is possible that archaeal-specific proteins could carry out these functions. The
replication, recombination and repair systems in M. maripaludis are an interesting mixture of eukaryotic
and bacterial homologues and could provide a system for uncovering novel interactions between proteins
from different domains of life.
Introduction
The chimaeric nature of archaeal genomes has been
commented on at some length. In general, the informationprocessing pathways in these organisms are perceived as
simplified versions of their eukaryotic counterparts. DNA
replication, repair and recombination (‘the three Rs’) have
all been examined using archaea as models for the equivalent
eukaryotic processes [1]. A requirement to manipulate DNA
has inevitably resulted in a level of similarity between how the
three Rs occur in all domains of life. However, it is clear that
the proteins and mechanisms involved in these processes are
generally more similar between archaea and eukaryotes. For
example, key DNA replication proteins have little sequence
or structural similarity between eukaryotic and bacterial
equivalents. Archaeal models have undoubtedly increased
our understanding of eukaryotic information-processing
pathways. However, with the accumulation of results, it
is becoming increasingly difficult to generalize about these
pathways even within the archaea. Differences at the species
level are presumably due to horizontal transfer. Variation in
the components of the three Rs is particularly striking in the
order Methanococcales, which provide a good illustration of
the innate plasticity of DNA-processing pathways.
Key words: archaeon, DNA repair, DNA replication, Methanococcales, recombination.
Abbreviations used: AP, apurinic/apyrimidinic; ATM, ataxia telangiectasia mutated; BER, base
excision repair; DSB, double-strand break; GGR, global genome repair; Hj, Holliday junction;
HR, homologous recombination; MCM, minichromosome maintenance; MMR, mismatch repair;
NER, nucleotide excision repair; NHEJ, non-homologous end-joining; ss, single-stranded; PCNA,
proliferating-cell nuclear antigen; RFC, replication factor C; TCR, transcription-coupled repair; XP,
xeroderma pigmentosum complementation group.
1
To whom correspondence should be addressed (email [email protected]).
Biochem. Soc. Trans. (2011) 39, 111–115; doi:10.1042/BST0390111
How do the Methanococcales replicate
their DNA?
Methanococcales are an extreme example of the variation
noted in DNA replication in archaea. Flow cytometric
studies have indicated that the DNA content in these
cells is atypical of archaea, and more similar to what is
seen in bacteria [2,3]. Consistent with this observation,
there is no clear archaeal/eukaryotic Cdc6/ORC (origin
recognition complex)-like protein in these species, which
recognizes and binds origins of replication. Equally, there
is nothing that looks like the bacterial equivalent (DnaA).
The Methanococcales are also unusual among archaea in
possessing multiple MCM (minichromosome maintenance)
homologues [4,5]. MCMs are functionally equivalent to
the bacterial DnaB helicase, and form the replicative
helicase in both eukaryotes and archaea. Eukaryotic MCM
complexes consist of heterohexamers with six different, but
related, subunits. All archaea examined to date possess a
single MCM homologue that forms homohexamers. These
simplified complexes have provided mechanistic insight into
how the eukaryotic MCM complex is likely to function.
Unusually, Methanococcus maripaludis S2 possesses four
MCM homologues, all of which contain the motifs that have
so far been identified as being essential for function as a DNA
helicase [4,5].
All four M. maripaludis MCMs co-purified when coexpressed, indicating that they form a heteromeric complex
in vitro [5]. This system may provide insights into subunit–
subunit interactions and specializations associated with
individual MCMs in the eukaryotic complex. Two of the
four M. maripaludis MCMs appear to have arisen via an
ancient duplication event and are conserved throughout
the Methanococcales. The other two MCM homologues in
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M. maripaludis appear to have arisen via a duplication
involving mobile elements [5,6]. Whether the MCMs in this
organism have evolved specific roles in the helicase complex
remains to be established.
Repair, recombination and how these pathways interact
with the replication machinery in the Methanococcales have
not been studied. There are no obvious homologues of
damage-induced checkpoint triggers such as the eukaryotic
ATM (ataxia telangiectasia mutated)/ATR (ATM- and Rad3related) genes in M. maripaludis, so how damage is recognized
and whether DNA damage checkpoint mechanisms exist is
currently unknown. M. maripaludis has been reported to be
highly sensitive to UV damage [7], suggesting that some
repair pathways may be compromised. Given that these
organisms are strict anaerobes, and therefore unlikely to
encounter direct sunlight, loss of these pathways should not
be surprising. On the other hand, Methanococcales exist at
a wide range of temperatures, and therefore general DNA
damage repair mechanisms must exist.
We have undertaken a search for M. maripaludis S2
genes involved in recombination and repair (Table 1).
We have identified a mixture of both bacterial and
eukaryotic homologues. Some repair pathways, notably
MMR (mismatch repair), are apparently absent in most
archaea, although it is possible that completely different
proteins fulfil the same functions. Some pathways appear
to consist of a mixture of bacterial and eukaryotic proteins,
suggesting that studying these systems could reveal novel
interactions. The fact that such a melange of proteins might
function together is illustrative of the plasticity likely to
be inherent in DNA-processing mechanisms. Understanding
what changes need to be made to bacterial and eukaryotic
proteins so that different systems can interact with each
other and how these repair mechanisms are co-ordinated with
replication systems remains to be determined.
NHEJ (non-homologous end-joining)
NHEJ is a process by which DSBs (double-stranded breaks)
in DNA can be repaired and was first identified in eukaryotes
(for a review, see [8]). It is the major pathway of DSB repair
during G1 -phase of the cell cycle in eukaryotes, when HR
(homologous recombination) is not possible because only
a single copy of each chromosome is present. NHEJ can
result in both error-free and mutagenic repair, depending
on whether DNA ends are re-ligated with or without any
processing. Two highly conserved proteins, Ku70 and Ku80,
recognize and bind to DNA ends at DSBs and act as a
platform to recruit other proteins required for repair [9,10].
NHEJ pathways have been identified in some bacteria and
appear to only require two proteins, Ku and LigD [11,12]. As
in eukaryotes, Ku binds to DNA ends at DSBs and recruits
LigD, which possesses exonuclease, gap-filling polymerase
and DNA-ligase activities and allows completion of repair
[13]. We have been unable to identify any Ku homologues
within the genome of M. maripaludis. In fact, with the
exception of Archaeoglobus fulgidus, Ku appears to be absent
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protein could play the role of Ku, or perhaps Mre11/Rad50
homologues are involved in DNA-binding to allow NHEJ. It
is also possible that, as in many bacteria, the NHEJ pathway
is absent from M. maripaludis, perhaps because multiple
chromosomes are present in the cell throughout the cell cycle,
allowing the more accurate process of HR to be used to repair
DSBs.
NER (nucleotide excision repair)
The NER pathway recognizes and repairs damaged DNA
bases and it is a major pathway for the repair of UVinduced damage in both bacteria and eukaryotes (for
a review, see [6]). Damaged bases are recognized by
proteins that detect distortions in DNA. The most common
types of DNA damage caused by UV light are CPDs
(cyclobutane–pyrimidine dimers) and 6–4 photoproducts.
In both eukaryotes and bacteria, there are two types of
NER: GGR (global genome repair) and TCR (transcriptioncoupled repair) [14]. GGR is a genome-wide process, whereas
TCR only occurs at sites where DNA is being transcribed
[15]. GGR and TCR differ only in the proteins used to
recognize DNA damage, with the processes downstream of
damage recognition being carried out by the same set of
proteins [16].
In bacterial GGR, damage recognition is carried out by the
UvrA/B proteins (for a review, see [17]). In bacterial TCR,
stalled RNA polymerase is detected by Mfd, a protein which
modulates RNA polymerase activity to allow binding of
UvrA/B to the site of damage [18]. After damage recognition,
TCR and GGR processes are identical, with UvrB/C cutting
the single strand of DNA either side of the damage to allow
excision, which involves the DNA helicase UvrD [19]. DNA
polymerase I then fills the gap and DNA ligase A completes
repair. The process of NER in eukaryotes occurs by the same
basic mechanism as in bacteria, but many more proteins are
involved [20].
M. maripaludis possesses homologues of bacterial proteins
Mfd and UvrA, B and C, suggesting that damage recognition
and incision of DNA could occur via a bacterial-like process.
However, M. maripaludis does not possess a homologue of
UvrD, the bacterial DNA helicase required for excision of ss
(single-stranded) DNA. Furthermore, the UvrA/B/C genes
are present in M. maripaludis in an operon that does not
contain any helicase homologues that could substitute for
UvrD. Interestingly, M. maripaludis also has homologues
of eukaryotic NER proteins, including the endonucleases
XPF (where XP is xeroderma pigmentation complementation
group) and XPG, and the DNA helicase XPD. PCNA
(proliferating-cell nuclear antigen), RFC (replication factor
C) and ligase I are involved in the gap-filling and ligation
steps at the end of NER in eukaryotes, and homologues of
all of these proteins exist in M. maripaludis. However, the
polymerase involved in NER in Methanococcus is probably
archaeal-specific, as none of the eukaryotic or bacterial
Molecular Biology of Archaea II
Table 1 Repair and recombination homologues in M. maripaludis S2
Proteins/pathways that are apparently missing in M. maripaludis are in bold. E, eukaryotic; B, bacterial; U, universal; A, archaeal.
Best match
Pathway
Domain
Gene
M. maripaludis gene
Role
Notes
NER
B
B
B
UvrA
UvrB
UvrC
MMP0729
MMP0727
MMP0728
Damage recognition
Damage recognition/DNA cleavage
DNA cleavage
B
B
UvrD
Mfd
–
MMP1284
Helicase
RNA polymerase modulation
E
E
XPD
XPF
MMP1219
MMP1395
5 →3 helicase
5 endonuclease
E
E
XPG
RFC
MMP1313
MMP1711
3 endonuclease
DNA synthesis
E
E
U
PCNA
Lig1
MutS
MMP322
MMP970
–
DNA synthesis
Ligation
Damage recognition
Missing
U
U
E
MutL
Nth1
APE1; APE2
–
MMP0537
MMP1012
Strand resectioning
Damage recognition
AP endonuclease (forms ss breaks)
Missing
Similarity to MutY (E)
APE1 is major AP
Missing
Specific for
transcription-coupled
repair
MMR
BER
B
RecBCD
–
DNA helicase/nuclease
endonuclease (E),
similarity to ExoA (B)
Missing
E
E
E
Mre11
Rad50
Nbs1
MMP1340
MMP1341
–
End processing
End processing
End processing
Missing
A
B
B
Hel308
RecF
RecO
MMP0890
MMP0332
–
Replication fork remodelling
Single-strand gap processing
Single-strand gap processing
Missing
B
B
B
RecR
RecQ
RecJ
–
MMP0457
MMP1314
Single-strand gap processing
Single-strand gap processing
Single-strand gap processing
U
U
RadA
RadB
MMP1222
MMP0617
Strand invasion
B
B
B
RuvA
RuvB
RuvC
–
MMP0176
–
Branch migration
Missing
Hj resolution
Missing
NHEJ
A
A
–
Hjc
Hef
–
MMP0336
MMP1395
–
Hj resolution/replication fork remodelling
–
Missing? No homologues
Other components
Replication fork
B
E
ExoVII
MMP0731; MMP0732
Exonuclease
HR
Missing
of Ku-like proteins
polymerases involved in NER have homologues in M.
maripaludis.
The mixture of bacterial and eukaryotic homologues
in M. maripaludis implies that NER could occur via
several different pathways. Although damage recognition
occurs via bacterial-like proteins, the downstream process
of repair could utilize a mixture of bacterial and eukaryotic
homologues (Figure 1). Perhaps the eukaryotic DNA helicase
See [20]
XPD is able to substitute for UvrD and interacts with
UvrA/B/C. Alternatively, XPD could act with XPG and
XPF in a separate pathway, with another unidentified helicase
acting with UvrA/B/C. Another possibility is that the NER
pathway in M. maripaludis is not functional. M. maripaludis
has been reported previously to be unusually sensitive to UV
damage [7], perhaps implying that such damage cannot be
repaired efficiently, if at all, by the chimaeric mixture of NER
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Figure 1 A mixture of bacterial and eukaryotic homologues of
NER proteins are present in M. maripaludis
Shaded boxes indicate bacterial homologues; white boxes indicate
eukaryotic homologues. The DNA polymerase involved in gap-filling is
probably archaeal- or Methanococcales-specific (white text).
archaea [23]. Perhaps MMR has been replaced in these
organisms by an alternative system.
Base excision repair
DNA is susceptible to damage from spontaneous base
changes due to oxidation, methylation or hydrolysis. The
BER (base excision repair) pathway is largely responsible for
repairing this type of damage [24]. Removal of the damaged
base is the first step in this process and is catalysed by a
DNA glycosylase. There are various DNA glycosylases, each
specific for a particular type of damaged base. The remaining
sugar phosphate is removed by an AP (apurinic/apyrimidinic)
endonuclease. This leaves a single nucleotide gap in one
strand, which can be filled by a DNA polymerase and sealed
by a DNA ligase.
It appears that the M. maripaludis BER system is made up
of homologues of eukaryotic components. Methanococcus
encodes a glycosylase/lyase of the bifunctional Nth family,
which cleaves the phosphodiester backbone at the same time
as removing the base [25]. This leaves an aldehyde residue
blocking the 3 -terminus of the damaged strand, which still
has to be processed by an AP endonuclease. Methanococcus
encodes an AP endonuclease of the APE1 type.
Homologous recombination
genes present in this organism. M. maripaludis also lacks a
photolyase homologue, which is required for light-activated
repair of UV-induced damage. This could explain further the
high sensitivity of M. maripaludis to UV light.
Mismatch repair
The strand-directed MMR system is a mechanism for
identifying DNA replication errors that proofreading
polymerase may have missed [21]. An important feature is
the ability to recognize the newly synthesized strand and
repair it to match the original template. At the core of MMR
are two proteins called MutS and MutL found in bacterial and
eukaryotic cells. MutS binds specifically to the mismatched
base pair and recruits MutL. MutL searches nearby DNA
for a nick (indicative of the newly synthesized strand) and
degrades the nicked strand back through the mismatch. The
ss gap can then be repaired by a polymerase and a ligase. In
bacteria, an additional protein called MutH creates nicks at
unmethylated (newly replicated) GATC sites.
We were unable to identify MutS, L or H in M. maripaludis.
In fact, these genes are absent from all class I methanogens
(Methanococcales, Methanobacteriales and Methanopyrales)
[22]. Interestingly, they are also lacking in hyperthermophilic
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Authors Journal compilation HR allows the exchange of genetic material between two
DNA duplexes of the same, or similar sequence [26]. It
is an essential process and its importance is illustrated
by universal conservation of the key RecA family of
recombinases (RecA in bacteria, Rad51 in eukaryotes and
RadA in archaea). An important function of HR is to
rescue stalled replication forks and repair DNA DSBs
without any loss of information. Once a DSB is detected,
an exonuclease degrades 5 -nucleotides leaving an ss 3 overhang. This process is performed by the RecBCD complex
in bacteria and by the MRN (Mre11/Rad50/Nbs1) complex in
mammals. RecA proteins bind co-operatively to the ssDNA,
forming a nucleoprotein filament that can intertwine with the
recipient duplex. HR can also be used to repair ss breaks. In
bacteria, the RecFOR pathway works in conjugation with
the RecQ helicase and RecJ exonuclease to prepare the gap
for RecA binding and filament formation. Strand exchange is
a key step in HR, where the RecA-coated strand interacts
with the recipient duplex DNA until a complementary
region is located and a heteroduplex can be formed. The
heteroduplex is then extended by branch migration, forming
an Hj (Holliday junction). In bacteria, RuvA specifically
recognizes Hj structures and recruits hexameric RuvB to
move the branch point using ATP. The final step in HR is
to cut two of the four strands, resolving the Hj and releasing
two separate duplexes. The Hj resolvase is RuvC in bacteria
and GEN1 in eukaryotes.
HR in M. maripaludis appears to be carried out by
a mixture of universal, bacterial, eukaryotic and archaealspecific proteins. M. maripaludis possesses clear homologues
of eukaryotic DSB-recognition and end-processing proteins
Molecular Biology of Archaea II
Mre11 and Rad50, although Nbs1 homologues could not
be identified. M. maripaludis does not have homologues
of RecBCD, but does have homologues of some of the ss
break-processing components RecF, RecQ and RecJ. Another
protein thought to act early on in HR is Hel308, which
may remodel stalled forks [27]. Nucleoprotein filaments
are formed in archaea by RadA, which is more similar to
eukaryotic Rad51 than bacterial RecA. Euryarchaeota also
have a RadA paralogue called RadB, which does not cause
strand invasion by itself, but stabilizes RadA on DNA [28].
Branch migration in Methanococcus may be performed by a
homologue of RuvB, although RuvA and C are lacking. M.
maripaludis also possesses the archaeal Hj resolvase called
Hjc, which is unrelated to bacterial RuvC or eukaryotic
GEN1 [29]. Methanococcus also has a homologue of a protein
called Hef found in Euryarchaeota that was first identified in
Pyrococcus furiosus [30]. Interestingly, Haloferax volcanii Hef
was recently shown to have dual roles in HR: (i) as a nuclease
to resolve Hjs (such as Hjc); and (ii) as a helicase to reverse
stalled replication forks and expose the causative lesion for
repair by another pathway (e.g. BER) [31].
Conclusions
In M. maripaludis S2, on the basis purely of the presence
or absence of known DNA repair proteins, MMR is lacking
and BER is more similar to the eukaryotic pathway, whereas
NER and HR combine components found in bacteria and
eukaryotes with archaeal-specific proteins. All three domains
of life suffer the same types of DNA damage, so perhaps it is
not surprising that the enzymes that repair them are relatively
transferable. However, those enzymes also have to interact
with each other, and M. maripaludis may provide a useful
model for studying what changes are needed to accommodate
these interactions.
Funding
Work in our laboratory is supported by Cancer Research UK [grant
number C23949/A7771].
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Received 25 August 2010
doi:10.1042/BST0390111
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