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Correspondence
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The nucleolar
proteome and the
(endosymbiotic)
origin of the
nucleus
Sir,
Nucleoli are essential regions of the eukaryotic nuclei
where the ribosomes are assembled. The human nucleolar
proteome has been studied in the last two years, leading to the
identification of several hundreds of proteins.(1,2) In a recent
Bioessays’ article, Staub et al.(3) characterise a large set of
conserved domains in these nucleolar proteins. The search of
these domains in other organisms revealed a complex pattern.
Many exist in archaea, arguing for an archaeal origin of the
nucleolar ‘‘core’’ machinery. A substantial bacterial contribution is also identified, while several domains are exclusively
eukaryotic. These results support a chimeric origin of the
nucleolus, with an ancestral core of archaeal origin supplemented with certain bacterial proteins and several proteins
invented during the eukaryotic evolution. This mixed heritage
is compatible with the diverse hypotheses that propose the
amalgamation of archaea and bacteria to give rise to the first
eukaryotes. However, these hypotheses differ in the mechanism explaining the merging of the archaeal and bacterial
partners. Some propose an unspecified fusion(4) or the engulfment of an archaeon by a bacterium.(5,6) The most elaborate
invoke symbioses between archaea and bacteria.(7–11)
Another fundamental difference concerns the origin of the
nucleus: is it a remnant of endosymbiotic archaea(5,6,10–12) or
just an idiosyncratic eukaryotic invention?(7,9,13,14)
Staub et al. try to answer this question using the nucleolar
proteome information. They conclude that the ribosomes and
the components involved in the maturation and assembly of
their constituents are of archaeal origin, which excludes a
bacterial endosymbiotic origin of the nucleus.(3) However,
all modern hypotheses for the origin of the nucleus involve
symbiotic or endosymbiotic archaea, not endosymbiotic
bacteria.(5,6,10 –12) Hence, despite their claim, Staub et al.’s
results are fully compatible with these hypotheses. They are
reluctant to accept an origin of the nucleus from an
1144
BioEssays 26.10
Stephen J. Gaunt
Department of Development & Genetics
Babraham Institute, Babraham
Cambridge, CB2 4AT, U.K.
E-mail: [email protected]
DOI 10.1002/bies.20116
Published online in Wiley InterScience (www.interscience.wiley.com).
endosymbiotic archaeal ancestor, but they support their view
with arguments other than the nucleolar protein domain
analysis. Are their arguments sufficiently sound? The first
concerns the co-existence of three different genomes and
protein synthesis machineries in early eukaryotes and the
problems eventually derived from the interferences between
them. However, this problem is not exclusive for the hypotheses proposing an endosymbiotic origin of the nucleus.
Indeed, the study of the nucleolar proteome supports a
chimeric origin of eukaryotes involving at least an archaeon
and a bacterium, that is, two genomes and two different protein
synthesis machineries. This is not necessarily problematic,
as revealed by the evolutionary history of eukaryotes. All
contemporary eukaryotes have or have had mitochondria with
their own genome and protein synthesis machinery. Moreover,
photosynthetic eukaryotes also contain chloroplasts, derived
from cyanobacterial endosymbionts with a genome and
protein synthesis machinery. In the most complex cases,
cryptophyte and chlorarachniophyte algae, chloroplasts derive from endosymbiotic eukaryotic algae, which possess a
reduced but functional nucleus (the ‘‘nucleomorph’’). In these
algae, four different genomes and protein synthesis machineries co-exist: nuclear-, mitochondrial-, chloroplast- and
nucleomorph-encoded. This extreme complexity (CavalierSmith called these organisms ‘‘meta-algae’’)(15) eloquently
demonstrates that the co-existence of different genomes and
protein synthesis machineries is possible and can have a great
evolutionary success.
The second argument evoked by Staub et al. is that the
available theories do not explain the energetic advantages for
an endosymbiotic origin of the nucleus. Several hypotheses do
not discuss any selective advantage (energetic or other) for
the establishment of the endosymbiosis.(5,6) However, we
have already advanced a model, the ‘‘syntrophy hypothesis’’,(10,11) starting with the establishment of a metabolic
symbiosis (‘‘syntrophy’’ meaning ‘‘eating together’’) sustained
by interspecies hydrogen transfer between facultative sulfatereducing proteobacteria and methanogenic archaea, a frequent symbiosis in anoxic environments.(16) For us, the
ancestral nucleus (derived from the methanogen) was
originally a metabolic compartment, which lost methanogenesis during its evolution. The hypothesis preferred by Staub
et al. to explain eukaryogenesis, the ‘‘hydrogen hypothesis’’,(9)
is also based on a hydrogen-transfer syntrophy between
BioEssays 26:1144–1145, ß 2004 Wiley Periodicals, Inc.
Correspondence
archaea and bacteria, but it does not advance any energyrelated explanation for the origin of the nucleus.
A third argument deals with structural characteristics of the
nuclear membrane. As Staub et al. posit ‘‘no free-living
prokaryote is separated from the environment in the same
manner in which the nucleus is separated from the cytoplasm’’.
This is true, but the question is also whether we should expect,
after many hundred millions years of evolution, to find a
nuclear membrane remaining identical to that of a free-living
prokaryote. We think this is highly improbable. On the contrary,
during the huge time span of eukaryotic evolution important
structural changes and innovations have occurred (a clear
example are the nuclear pores). Innovations exist for the
mitochondria and chloroplasts (for example, specific membrane transport systems)(15,17) but they do not refute their
endosymbiotic origin. No free-living algae are separated from
the environment as cryptophyte and chlorarachniophyte fourmembrane chloroplasts do, but their endosymbiotic origin is
beyond any doubt. Endosymbiotic hypotheses need to explain
the structural peculiarities of the nuclear membrane, but the
origin of the nuclear membrane and its selective advantages
are also puzzling for non-endosymbiotic supporters.
Finally, Staub et al. argue that nucleus replication involves
membrane disintegration, something that obviously does not
occur in prokaryotes. However, whilst several eukaryotic
groups break down their nuclear membrane during mitosis
(the so-called ‘‘open mitosis’’), many others do not (‘‘closed
mitosis’’, more similar to the replication of a prokaryotic cell).(18)
In some groups (e.g. green algae), both mitosis forms exist. The
key question is to know which mitosis type, open or closed, is
ancestral. Since both types are widespread in the eukaryotic
tree, a simple inspection of their distribution across the
eukaryotic phyla does not provide a clear answer. Interestingly,
most hypotheses to explain the evolution of mitosis based on
the characteristics of the closed and open mechanisms state
that the closed mitosis predated the open one, an idea
consistent with an endosymbiotic origin of the nucleus.(18)
In summary, Staub et al. have carried out a very interesting
analysis that sheds light on the origin and evolution of the
nucleolus, but their results are compatible with very different
hypotheses for the origin of the nucleus, including the
endosymbiotic theories. Their arguments against a possible
endosymbiotic origin can be debated and are disconnected
from their observations concerning the nucleolus. The origin of
the nucleus remains an open question.
References
Response to Moreira et al.
called ‘‘hydrogen hypothesis’’.(1,2) We cannot (and did not)
rule out other hypotheses but, in the following, we will explain
in more detail why we favour the ‘‘hydrogen hypothesis’’ from
the standpoint of nucleolus evolution.
Moreira et al.’s description of our main results is partly
correct: the core nucleolar protein machinery is of archaeal
Sir,
In our recent article about the nucleolar protein domain
repertoire, we embedded a plausible scenario for nucleolus
evolution into a hypothesis on eukaryote evolution, the so-
BioEssays 26:1145–1147, ß 2004 Wiley Periodicals, Inc.
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David Moreira
Louis Ranjard
Purificación López-Garcia
Unité d’Ecologie, Systématique et Evolution
UMR CNRS 8079, Université Paris-Sud
bâtiment 360, 91405 Osay Cedex
France
E-mail: [email protected]
DOI 10.1002/bies.20122
Published online in Wiley InterScience (www.interscience. wiley.com).
BioEssays 26.10
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