Molecular Biology of Archaea 3
From archaeon to eukaryote: the evolutionary
dark ages of the eukaryotic cell
Joran Martijn and Thijs J.G. Ettema1
Department of Cell and Molecular Biology, Science for Life Laboratory, Uppsala University, Husargatan 3, SE-75 237, Uppsala, Sweden
Abstract
The evolutionary origin of the eukaryotic cell represents an enigmatic, yet largely incomplete, puzzle. Several
mutually incompatible scenarios have been proposed to explain how the eukaryotic domain of life could
have emerged. To date, convincing evidence for these scenarios in the form of intermediate stages of the
proposed eukaryogenesis trajectories is lacking, presenting the emergence of the complex features of the
eukaryotic cell as an evolutionary deus ex machina. However, recent advances in the field of phylogenomics
have started to lend support for a model that places a cellular fusion event at the basis of the origin
of eukaryotes (symbiogenesis), involving the merger of an as yet unknown archaeal lineage that most
probably belongs to the recently proposed ‘TACK superphylum’ (comprising Thaumarchaeota, Aigarchaeota,
Crenarchaeota and Korarchaeota) with an alphaproteobacterium (the protomitochondrion). Interestingly,
an increasing number of so-called ESPs (eukaryotic signature proteins) is being discovered in recently
sequenced archaeal genomes, indicating that the archaeal ancestor of the eukaryotic cell might have been
more eukaryotic in nature than presumed previously, and might, for example, have comprised primitive
phagocytotic capabilities. In the present paper, we review the evolutionary transition from archaeon to
eukaryote, and propose a new model for the emergence of the eukaryotic cell, the ‘PhAT (phagocytosing
archaeon theory)’, which explains the emergence of the cellular and genomic features of eukaryotes in the
light of a transiently complex phagocytosing archaeon.
Introduction
The evolutionary origin of the eukaryotic cell represents an
enigmatic, yet largely incomplete, puzzle. Despite the large
number of mutually incompatible scenarios that have been
proposed to explain its origin (for a recent overview, see [1]),
some consensus has been reached about the following points
[2]: first, the LECA (last eukaryotic common ancestor) most
probably contained the mitochondrial progenitor derived
from endosymbiosis with an alphaproteobacterium and,
secondly, eukaryotic genomes have a chimaeric nature: genes
for information storage and processing are archaea-related,
and genes for metabolic or ‘operational’ processes are mostly
bacterial in nature (but not necessarily derived from the
mitochondrial progenitor). Finally, a significant fraction of
the eukaryotic genes encode proteins that are restricted
to eukaryotes, the so-called ESPs (eukaryotic signature
proteins). Beyond this, the picture gets blurry. Currently, two
major questions are of interest: (i) what was the nature of the
host that took up the alphaproteobacterium, and (ii) when did
eukaryotic complexity arise, before (‘mitochondria-late’) or
after (‘mitochondria-early’) the endosymbiotic event that led
Key words: Archaea, eukaryogeneois, horizontal gene transfer (HGT), last eukaryotic common
ancestor (LECA), phagocytosing archaeon theory (PhAT).
Abbreviations used: CRISPR, cluster of regularly interspaced palindromic repeats; ESP, eukaryotic
signature protein; HGT, horizontal gene transfer; LECA, last eukaryotic common ancestor; PhAT,
phagocytosing archaeon theory.
1
To whom correspondence should be addressed (email [email protected]).
Biochem. Soc. Trans. (2013) 41, 451–457; doi:10.1042/BST20120292
to the establishment of the mitochondrion? Mitochondrialate models, of which the Archezoa model [3] is its main
protagonist, argue that eukaryotes gradually evolved from
a lineage devoid of mitochondria (the proposed Archezoa)
and eventually acquired mitochondria (Figures 1A and 1B).
Hence such scenarios are compatible with the classical threepronged classification of the domains of life [4]. In contrast,
mitochondria-early models argue that the eukaryotic lineage
emerged from a symbiosis between an archaeon and
a bacterium (the mitochondrial ancestor), and that this
‘symbiogenesis/fusion’ subsequently triggered the evolution
of typical eukaryotic features [5,6] (Figures 1C and 1D).
Although both models provide a fairly complete explanation, a smoking gun is missing: cellular intermediates that
would support either scenario are unknown to biology thus
far [7]. The previously presumed amitochondriate eukaryotes
(‘archezoans’) were shown to have once contained mitochondria in their evolutionary past [5,8]. Conversely, evidence
for the existence of intermediate cellular entities that would
support fusion-like scenarios is also lacking [7]. Obviously,
in the absence of intermediate stages of eukaryotic evolution,
the gap between extant prokaryotic and eukaryotic cell
types remains puzzlingly large [2], and we can at best guess
about the forces that supposedly triggered the emergence of
cellular complexity that is characteristic for eukaryotes.
Despite apparent methodological complications [9], the
most recent efforts to shed light on this issue from
a phylogenomics point of view seemingly lend support
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Figure 1 The evolutionary relationships between the three
domains of life
(A) Schematic phylogenetic tree that displays the classical ‘three
domains’ view of life [4], in which the Archaea (red) and Eukarya
(green) appear as sister lineages, sharing a common branch in the
tree of life. Such a view is most compatible with scenarios in which the
alphaproteobacterial progenitor of mitochondria was acquired relatively
late in eukaryotic evolution (B), that is, after the emergence of the
cellular complexity that is typical for eukaryotes. Hence the host in
these ‘mitochondria-late’ scenarios, such as the Archezoa theory [3],
is envisaged to have been a complex amitochondriate eukaryote (the
‘archezoan’). (C) Schematic phylogenetic tree displaying a fusion-like
origin for the eukaryotic domain of life. In this case, the fusion
partner is envisaged to have been a ‘garden variety’ archaeon [2]
that took up the alphaproteobacterial progenitor of mitochondria via a
hitherto unknown endosymbiotic interaction (D). After a brief period of
popularity, support for ‘mitochondria-late’ scenarios has been decreasing
due to the detection of mitochondria-derived organelles in all presumed
for transport) proteins [18–20], ubiquitin protein modifier
system components [21], as well as several eukaryotetype transcription and translation factors (see [14] for an
overview).
Another argument in favour of such a scenario comes from
an energetic viewpoint: the acquisition of the mitochondria
is believed to have alleviated the eukaryotic progenitor from
the bioenergetic constraints to which bacterial and archaeal
cells are subjected, and allowed for the immense expansion in
the number of genes, and hence allow for the emergence of
cellular complexity [22]. In the present paper, we elaborate on
these theories, and integrate recent insights to propose a new
variant of the fusion model to explain the emergence of the
eukaryotic cell. Yet, before we do so, we first zoom in on the
genomic differences between prokaryotes and eukaryotes,
as these might reveal clues about the processes that have
occurred during the evolutionary ‘dark ages’ of the eukaryotic
cell.
amitochondriate eukaryotes [8].
The evolutionary ‘dark ages’ of the
eukaryotic cell
On the basis of comparative analyses of genome sequence
data that have become available during the last decade, it
has become increasingly clear that the evolutionary gap
between prokaryotes and eukaryotes remains extremely
large. Irrespective of the available hypotheses to explain
this observation, the LECA is inferred to have been highly
complex. LECA is inferred to have contained most of
the typical eukaryotic features, which, due to the lack of
evidence for pre-existing intermediate eukaryotic life forms,
seems to have arisen within a relatively short timeframe.
Despite the fact that little is known about the period during
which the prokaryote-to-eukaryote transition was established, it is clear that three evolutionary forces, i.e. gene
duplication, HGT (horizontal gene transfer) and gene genesis,
have played a major role in the emergence of eukaryotes. In
this section, we briefly discuss these forces.
Massive gene duplication at the basis of the
eukaryotic emergence
to symbiogenesis/fusion-like scenarios at the base of the
eukaryotic origin. These studies are largely consistent with an
extended version of the eocyte theory [10,11], which suggest
that eukaryotes have emerged from within the archaeal
domain of life [12,13] or more specifically from the recently
proposed ‘TACK superphylum’ (comprising Thaumarchaeota, Aigarchaeota, Crenarchaeota and Korarchaeota) [14,15].
This idea is supported further by the fact that members of
this archaeal group uniquely share a number of presumed
ESPs [14], including bona fide orthologues of actin [16],
tubulin [17], ESCRT (endosomal sorting complex required
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Authors Journal compilation Gene duplication is widely considered to be a crucial
mechanism for evolutionary innovation [23]. The existence
of a large amount of pan-eukaryotic paralogues suggests that
gene duplication has been a major driving force in eukaryotic
evolution. For example, whereas many components of the
eukaryotic core machinery comprise two or more gene
copies, their prokaryotic counterparts mostly contain only
a single gene. A detailed reconstruction of eukaryotic
genome content has identified three important lessons [24].
First, the ancestral eukaryotic gene repertoire seems to
have approximately doubled in size before the onset of
the major eukaryotic radiations. Secondly, gene duplication
seems to have played a primordial role in the emergence of
eukaryotic features, as functional classes that affiliated with
‘typical’ eukaryotic processes (protein fate, superstructure
Molecular Biology of Archaea 3
forming proteins, etc.) have been subjected to extensive
duplications. Thirdly, a significant part of the paralogous
gene content of the ancestral eukaryotic gene content seems
to be a result of lateral gene transfer, which, at least in
part, was acquired via the endosymbiosis that gave rise to
the emergence of the mitochondrion (see below). A telling
example of how duplication has shaped eukaryotic gene
content is depicted by the evolution of the Ras superfamily
of small GTPases that play pivotal roles in the process of
cellular compartmentalization in eukaryotes [25,26]. This
superfamily is characterized by several ancient duplication
and gene-transfer events. The latter is exemplified by the
Rho family of GTPases, which are ubiquitous regulators of
phagocytosis in eukaryotes, and which most probably have a
bacterial origin [27].
The origin of bacterial genes in eukaryotes
In addition to gene duplication, HGT events have played a
major role in the emergence of the eukaryotic cell, as is evident
by the significant amount of genes that clearly are of bacterial
origin that reside on eukaryotic genomes. On the basis of
phylogenetic studies, part of these bacterial genes can be
readily attributed to the alphaproteobacterial endosymbiont
from which mitochondria evolved [28]. Yet, the origin of the
remaining set of bacterial genes in eukaryotic genomes, which
seemingly lacks phylogenetic coherence, is a matter of debate
[2]. Whereas some try to explain that these genes have been
the result of additional gene-transfer events [2], for example,
by means of additional transient endosymbiotic partners,
or a result of gene influx via predation [29] or parasitism
[30], others envisage that HGT between prokaryotic lineages
before [31] and after [1,32] the origin of mitochondria
can readily explain the mosaic nature of bacterial genes in
eukaryotes. Hence, whereas both lines of thought explicitly
imply a major role for HGT in eukaryotic evolution, the
main dispute centres on the question of whether it was a
single event (the mitochondrial endosymbiosis) or multiple
events that gave rise to these bacterial genes. Importantly, each
of these scenarios does not necessarily exclude one another,
therefore it is tempting to think that each of them might have
played their part in the emergence of eukaryotes.
Eukaryotic innovations at the basis of
eukaryogenesis
Eukaryotes have evolved cellular structures and systems that
lack a functional counterpart in prokaryotes. Examples of
these include the characteristic endomembrane systems in
eukaryotes, such as the nucleus, endoplasmatic reticulum and
Golgi apparatus, and the existence of a cytoskeleton that
facilitates higher-order processes such as cellular motility,
phagocytosis and vesicular trafficking. Many of the proteins
that are involved in these processes (although not exclusively,
e.g. [27,33]), are dominated by ESPs [34], which generally
comprise up to one-third of the gene content of extant
eukaryotes. Whereas in the past it has been proposed that
such proteins might have been contributed by an extinct
donor lineage [34], this is not likely, as ESPs are involved
in a wide variety of eukaryotic processes. Moreover, ESPs are
continually being discovered in prokarytotic genomes that
have recently been sequenced.
Rather, the emergence of ESPs has been proposed to be the
result of molecular innovation events that can be classified
into three categories [35]: (i) reuse of prokaryotic proteins
and domains for the same biochemical function, but in a
different context; (ii) emergence of new biochemical functions
and protein superfamilies, but within existing protein
folds; and (iii) domains with bona fide new folds, ‘invented’
during the early stages of eukaryotic evolution. The first category includes proteins for which prokaryotic homologues
can be readily detected using sensitive sequence or structural
homology detection algorithms, and is characterized by a
drastic acceleration of sequence divergence. For the third
category, it was found that many new domains either had
α-helical or metal-chelated supported structure. Because such
structures are less dependent on the complex hydrogenbonding for their stability, it was hypothesized that domains
that harbour them are more susceptible for evolution of new
folds [35].
The ‘PhAT’ (phagocytosing archaeon
theory) scenario for the origin of
eukaryotic complexity
As outlined above, the lack of information about the
early stages of eukaryotic evolution currently precludes
the rationalization of detailed hypotheses to explain the
emergence of the eukaryotic cell in its full complexity.
Yet, in the light of continuous discovery of new pieces of
this enigmatic puzzle, a revision of previous hypotheses
seems justified. In this section, we propose the PhAT for
the emergence of the eukaryotic cell, which differs from
previous hypotheses in that it involves the emergence of a
relatively sophisticated archaeal lineage that stands at the
basis of the process of eukaryogenesis. Our hypothesis
provides: (i) a rational explanation for the highly mosaic
prokaryotic genome content of extant eukaryotes, (ii) an
explanation for the significant evolutionary distance between
archaeal and eukaryotic orthologous genes as opposed to
that of Alphaproteobacteria and mitochondria, and (iii) an
alternative explanation for the origin of the nucleus. The
hypothesis can be broken down into a number of stages
(Figure 2) as follows.
1. A transient TACK archaeon
The starting point of the envisioned scenario is an ancestral
archaeal lineage, probably belonging to the recently proposed
‘TACK superphylum’ [14] that is supposed to have contained
the full collection of ESPs that have currently been identified
in archaea, such as actin [16,27], tubulin [17], the ubiquitin
protein modifier machinery [21] and several proteins involved
in transcription and translation. It is possible that this archaeal
lineage was only transient [36].
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Figure 2 The PhAT scenario for the origin of the eukaryotic cell
2. Loss of cell wall
Schematic step-wise overview of the crucial steps of the proposed
PhAT (see the text for details), comprising the following stages: (1) A
flexible actin-based cytoskeleton, which supported the formation of
cellular protrusions. (3) The archaeon’s cytoskeleton matures into a
primitive phagocytotic machinery, and the uptake and digestion of other
Subsequently, this ancient TACK lineage is envisaged to have
lost its proteinacious cell wall, allowing for the evolution of
a more flexible actin-based cytoskeleton, such as observed in
plasma-like organisms. Ancient duplications of the archaeal
actin gene could have been the basis of the emergence
of this flexibility [27,37], allowing for the formation of
branched actin polymers. Such actin-based structures could
have facilitated the formation of cellular protrusions.
prokaryotic cells exposes the archaeon to increasing amounts of ‘foreign’
genomic DNA. The resulting elevated rates of HGT destabilize the
archaeal host genome, which causes the genetic material to evolve at
3. Primitive phagocytosis causing rampant HGT
‘garden variety’ archaeon, probably belonging to the recently proposed
‘TACK superphylum’ contains an actin-based cytoskeleton (blue). (2)
After losing its proteinacious cell wall, the archaeon evolves a more
accelerated rates, forming the basis of the gene innovation processes.
(4) A protective membrane boundary is formed to protect the genetic
integrity of the host cell genome via invagination events, giving rise
to a primitive karyotic cell type. The protective membrane structure
restabilizes the host genome and restores the evolutionary rates.
An ancient alphaproteobacterium is taken up, but not digested, and
establishes an endosymbiotic interaction with the ‘parakaryotic’ host cell.
Conceivably, the symbiotic interaction was already established before
the ingestion of this protomitochondrial cell type. (5) The transition
of the alphaproteobacterial endosymbiont into an energy-producing
mitochondrion forms the basis of the emergence of cellular complexity
typical for eukaryotes. The surplus of energy facilitates the maturation of
the nucleus and additional endomembrane systems and allows the host
genome to expand. This relaxed genomic stringency further accelerates
genomic innovations via gene duplication events, recombination of
existing genes and gene genesis events. In addition, with energy
production now taking place at the mitochondrial membranes rather
than the outer membrane, the volume of the cell is no longer restricted
to typical prokaryotic dimensions.
Next, the cytoskeleton matured into a primitive phagocytosis
machinery. Critically, the primordial uptake and digestion of
other prokaryotic cells exposes the phagocytosing archaeon
to increasing amounts of genomic DNA of the ingested
cells. The latter would have resulted in rampant HGT
to the archaeal genome, causing the emergence of a
highly mosaic host genome. As a consequence of the high
prevalence of HGT, the host genome destabilizes, for example
due to detrimental gene dosage effects [38], causing the
genetic material to evolve at accelerated rates. Moreover,
the ephemeral elevation of evolutionary rates of sequence
evolution also explains why the similarity between eukaryotic
and archaeal genes is generally weak as compared with those
between Alphaproteobacteria and mitochondria [7], as the
latter genes have not been exposed to such rate acceleration.
4. Evolution of a primitive nucleus to protect
genomic integrity
In order to protect the genetic integrity of the host cell
genome from further phagocytosed genetic material, a
protective membrane boundary is formed via invagination
events, giving rise to a primitive karyotic cell type.
The protective membrane structure stabilizes the host
genome and restores the evolutionary rates to normal.
Now that phagocytosis has become an integrated part
of its lifestyle, the organism continues to take up
prokaryotic cells. One particular cell, probably an ancient
alphaproteobacterium, is phagocytosed, but not digested,
and establishes a endosymbiotic interaction with the host
cell, similar to those that are often observed in microbial
eukaryotes (e.g. amoebae or ciliates) [39]. Conceivably, the
symbiotic interaction was already established before
the ingestion of this protomitochondrial cell type.
5. Energy-induced genome expansion and
innovation
Finally, the alphaproteobacterial endosymbiont reductively
evolves into an ATP-generating organelle: the mitochondrion. In contrast with genes from ingested cells, the stable
endosymbiotic interaction between the mitochondrion and
host cell allows organelle–host gene transfer events. The
newly provided surplus of energy allows the host cell to
evolve cellular complexity [22], such as the maturation of
the nucleus and additional endomembrane systems. Released
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from the evolutionary pressure to retain a small compact
genome, the host genome is allowed to expand. This relaxed
genomic stringency allows for genomic rearrangements
and results in a playground for genomic innovation via
recombination of existing genes, gene duplications and gene
genesis events, allowing for the expansion of existing protein
families and for the emergence of novel protein folds. In
addition, with energy production now taking place at the
mitochondrial membranes rather than the outer membrane,
the volume of the cell is no longer restricted to typical
prokaryotic dimensions.
Discussion
In the present paper, we present a scenario (PhAT) for
the origin of the eukaryotic cell, which has a primitive
phagocytosing archaeon at its basis. Although this idea has
been suggested before [27,40], PhAT represents the first
explicit model that implements archaeal phagocytosis at the
basis of the process of eukaryogenesis, as it provides an
explanation for the origin of the nucleus and mitochondria,
as well as for the mosaic bacterial gene content in eukaryotes.
Although thought-provoking, the current model is as
plausible (or implausible) as any other theory for the
emergence of a eukaryotic cell that has been proposed in
the past with respect to the lack of supporting evidence for
intermediate eukaryotic life forms.
Whereas phylogenomic support for fusion-like origin of
the eukaryotic cell is growing steadily [12–15], the mosaic
bacterial gene content in eukaryotic genomes is seemingly at
odds with such models. In the past, this anomaly has been
explained: (i) by the existence of multiple endosymbiotic
partners, each of which contributed genetic material to the
host cell [2,41], or (ii) by HGT among prokaryotes before
[31], and after [1,32], the single ancient acquisition of the
alphaproteobacterial ancestor of mitochondria. Although
we acknowledge that HGT is a major driving force in
prokaryotic genome evolution, we do not believe that
the bacterial ‘pot-pourri’ of genes in eukaryotic genomes
can be explained by a single ancient acquisition event
(i.e. the mitochondrial ancestor). Indeed, differential losses
notwithstanding, approximately 20% of ancestral eukaryotic
genes present in LECA show signatures of multiple bacterial
and archaeal origins [1]. For example, several eukaryotic genes
involved in key functions, such as glycolysis [42], central
anaerobic metabolism [43] and mitochondrial translation
[44], do not display phylogenetic affiliation with currently
sequenced Alphaproteobacteria. Hence, rather than invoking
a single acquisition event, we propose that a significant part
of these bacterial genes originate from phagocytotic ingestion of prokaryotes, similar to the ‘you are what you eat’
concept proposed by Doolittle [29]. It should be noted,
however, that in Doolittle’s scenario, the phagocytosing cell
was envisaged to be a fully fledged eukaryote, rather than an
archaeon as in the PhAT scenario.
Traditionally, the origin of the nucleus has been explained
via an endosymbiosis event, such as in certain variants of
the eocyte theory [10]) or via membrane invagination events
(‘autogenous karyogenesis’). The best-known autogenous
model is the endokaryotic hypothesis [45], which envisages
that the nucleus was formed to decouple the process of
transcription from translation as a defence mechanism against
an invasion of self-splicing introns. Under the PhAT scenario,
we propose another variant of the autogenous model,
which entails the emergence of the nucleus as a defence
mechanism against phagocytosis-induced HGT. Prokaryotes
have evolved several mechanisms to both promote (e.g.
conjugation, gene transfer agents, DNA-containing vesicles)
and counter [CRISPR (cluster of regularly interspaced
palindromic repeats) and restriction-modification systems]
the exchange of genetic material. Apart from the fact that the
efficacy of CRISPR-based systems is thus far restricted to
defence against viral and plasmid sequences, we envisage
that the available defence systems were insufficient to
protect the host cell against the destabilizing effects
of phagocytosis-induced HGT, prompting the emergence of
an alternative mechanism. Indeed, the fact that eukaryotic
genomes do not encode these prokaryotic defence systems
seems to support this idea, as does the notion that rates
of HGT from prokaryotes to eukaryotes are much lower
than between prokaryotes. Archaeal genomes, in particular
those of members of the TACK superphylum, encode a
number of eukaryotic proteins that have the ability to affect
membrane bending [46], and we envisage that such proteins
have been instrumental in the initial formation of nucleuslike compartments. Although seemingly far-fetched, the
formation of ‘higher-order’ intracellular membrane systems
has occurred several times independently in evolution, and
is not restricted to eukaryotes: several prokaryotic lineages,
including cyanobacteria (thylakoid membranes), members
of the Planctomycetes–Chlamydia–Verrucomicrobiae superphylum (possibly also including Poribacteria) [47], and, most
recently, Archaea [48], are known to contain membrane
structures, each equipped with specific functions. Therefore
the emergence of the nucleus as a protective barrier against
excessive HGT in the primitive phagocytosing archaeon
should not be rendered implausible on these grounds.
Arguably, despite its costs, phagocytosis is obviously a highly
profitable activity, as is evident from by the plethora of
phagocytic protists that exist in Nature.
Outlook
The evolutionary transition from prokaryote to eukaryote
has been a complex journey in which non-tree-like processes
have probably played a decisive role [22,36]. Unfortunately,
we are currently lacking the resolution that is needed to
distinguish the processes that have been instrumental in this
transition from the ephemeral ones. Still, with the recent
advances in next-generation sequencing technologies, as well
as in high-throughput techniques that allow for the genomic
exploration of the vast uncharacterized microbial diversity
(e.g. single-cell genomics, metagenomics), the coming years
will see a vast expansion of new and exciting genomic data
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that will help us obtaining this resolution. In addition,
the genomic characterization of presumed intermediates in
eukaryotic evolution, such as the recently discovered illusive
‘Myojin parakaryote’ [49], will undoubtedly shed new light
on the dark ages of the eukaryotic cell.
Acknowledgements
We apologize to those authors whose work we could not refer to
owing to space constraints.
Funding
The work in T.E.’s laboratory is supported by the Swedish Research
Council [grant number 621-2009-4813], and by European
Research Council (ERC) [grant number 310039-PUZZLE_CELL] and
Marie Curie European Reintegration Grant (ERG) [grant number
268259-RICKOCHET] grants from the European Union.
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Received 1 November 2012
doi:10.1042/BST20120292
C The
C 2013 Biochemical Society
Authors Journal compilation 457