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BCM - Seminario - I-1 - 2015 - The Origin of Modern Terrestrial Life
BCM - Seminario - I-1 - 2015 - The Origin of Modern Terrestrial Life
HFSP Journal
Institut Pasteur, 25 rue du Docteur Roux, 75015 Paris et Universit Paris-Sud, CNRS, UMR 8621,
91405, Crsay-Cedex, France
2
Institut Pasteur, 25 rue du Docteur Roux, 75015 Paris, France
Received 22 June 2007; accepted 22 June 2007; published online 25 July 2007; corrected 11 March 2008)
The study of the origin of life covers many areas of expertise and requires the
input of various scientific communities. In recent years, this research field has
often been viewed as part of a broader agenda under the name of exobiology or
astrobiology. In this review, we have somewhat narrowed this agenda, focusing
on the origin of modern terrestrial life. The adjective modern here means that
we did not speculate on different forms of life that could have possibly appeared
on our planet, but instead focus on the existing forms cells and viruses. We try
to briefly present the state of the art about alternative hypotheses discussing not
only the origin of life per se, but also how life evolved to produce the modern
biosphere through a succession of steps that we would like to characterize as
much as possible. [DOI: 10.2976/1.2759103]
CORRESPONDENCE
P. Forterre: forterre@pasteur.fr
S. Gribaldo: simo@pasteur.fr
156
Plausible mechanisms for the formation of the solar system have now been
PERSPECTIVE
Figure 1. Schematic of bottom-up and top-down approaches. Major events discussed in the text are highlighted.
emergence of life (liquid water, continental crust, atmosphere) were already in place at 4.4 4.3 Ga. However, the
habitability of the early Earth was seriously compromised by
multiple giant impacts. In particular, around 3.9 Ga the
Earth was subjected to an impressive episode of bombardment, called the late heavy bombardment (LHB) (Cohen et
al., 2000).
The Late Heavy Bombardment
HFSP Journal
Greenland) dates exactly to the end of the LHB, at 3.8 Ga. In
our opinion, it is unlikely that any forms of life, if already
present, would have survived the devastating impacts of the
LHB. If this view is correct, it implies that the path to modern life would have (re)started after 3.9 3.8 Ga. The presence of sedimentary rocks testifies that oceans had already
reformed by that time. However, putative isotopic traces of
life found in these rocks are now believed to be artifactual
(see below), consistent with the idea that modern life might
have indeed originated after the LHB.
(Kump, 2005). Oxygen and silicon isotope data from archaean cherts indicate that ancient oceans may have been
warmer than today, with temperatures as high as 70 C
around 3.3 Ga (Knauth, 1998; Robert and Chaussidon,
2006). However, the interpretation of isotopic data remains
controversial since this would imply that archaean hot and
acidic rainwater would have produced intense weathering
that is not observed in the paleoweathering record. Furthermore, a hot ocean is difficult to reconcile with a first global
glaciation that could have occurred at 2.9 and 2.4 Ga [for a
critical review of these data, see (Kasting and Howard,
2006)].
158
PERSPECTIVE
However, it is very difficult to extract kerogens from Archaean rocks, and not all lipids are equally resistant. For example, lipids from archaea are very fragile and have not been
found in rocks older than 1.8 Ga (Summons et al., 1988).
The older biomarker record regards the presence of hopanes,
lipids that today are distinctive of cyanobacteria, in 2.7 Ga
old rocks from Australia (Brocks et al., 1999). The presence
of eukaryotic-type steranes in the same ancient rocks
(Brocks et al., 1999) is more controversial since some bacteria can produce sterols as well (Pearson et al., 2003; Tippelt
et al., 1998), although not of the complexity of those found
by Brocks et al. (Summons et al., 2006).
In conclusion, the fact that the oldest traces of life that are
not controversial are only those from 2.6 Ga (Schopf, 2006)
leaves open a wide window for the origin of modern life between 3.9 (end of the LHB) and 2.7 Ga. The quest for traces
of life in this time interval is a rapidly expanding research
field. New drilling projects have now started in order to obtain novel samples of archaean rocks. Isotopic and chemical
techniques are being improved to detect the presence of organic matter with less ambiguity, and new in situ techniques
start to be applied to the analysis of putative microfossils.
Novel and more performing techniques of lipid extraction
will hopefully push back the limit of detection of biomarkers
to the early Archaean. In parallel, theoretical models for the
early Earth will surely benefit from a better description of
known metabolisms (see below) and metabolic consortia,
and their current distribution in a wide range of environmental settings.
THE ORIGIN AND EARLY EVOLUTION OF LIFE
Heterotrophic versus autotrophic theories
In the traditional prebiotic soup scenario, organic molecules would have first accumulated in the ocean or in
smaller water bodies on the early Earth, either delivered by
extraterrestrial sources (micrometeorites, dust) and/or produced by Millers type experiments (especially if the early
atmosphere was hydrogen rich, see above) (Bada and
Lazcano, 2003). The first living systems would have then
emerged from the gradual complexification of the prebiotic
broth. The authors supporting this heterotrophic theory often argue that prebiotic chemistry is the prolongation on our
planet of the cosmic chemistry, whose products (e.g., amino
acids) indeed overlap with the building blocks of life. For
them, the possibility to easily produce in prebiotic conditions
simple amino acids, purines, sugars, fatty acids, and other
small organic molecules essential to modern life is too striking to be fortuitous (de Duve, 2003). Proponents of the prebiotic soup scenario (especially the Bada and Miller school)
have in general argued in favor of a slow (gradual accumulation) and cold origin of life (essential to the long-term stability of organic matter).
As an alternative to the heterotrophic theory, 20 years
ago Wachtershauser proposed an autotrophic origin of life, in
HFSP Journal Vol. 1, September 2007
HFSP Journal
and/or in a volcanic setting may have enriched the prebiotic
arsenal of organic molecules, or else suggest that the first organics useful for life were concentrated at mineral-water interfaces and/or into porous minerals. Volcanic activity might
have been especially important for the production of phosphoric compounds that are essential for life (Yamagata et al.,
1991) (Schwartz, 2006). Indeed, the first source of phosphate
may have been polyphosphates, which are found in volcanic
condensates and hydrothermal vents produced by volcanic
activity (Yamagata et al., 1991). In order to reconcile the requirements of volcanic activity with an environment favoring molecular stability, it is tempting to suggest that life
originated in an Iceland-like setting mixing ice and fire, in
which a geothermal gradient could provide a stable and continuous energy source over long periods, whereas a cold environment could provide stability for the accumulation of organic molecules.
Both heterotrophic and autotrophic theories are faced
with the problem of ending up with a robust protometabolism that could provide the energy and monomers to establish
the RNA world (de Duve, 2003). In a first step, it is important
to consider how to transfer the energy acquired either from
the outside (heterotrophic theory) or from the reactions in
hydrothermal fluids (autotrophic theory) for further elaboration of the system inside protocells. Ferry and House (2006)
recently proposed an interesting model in which the energy
obtained from a geothermal energy flux is coupled to the formation of phosphorylated compounds. This model combines
both features of the autotrophic and heterotrophic theories
since the mechanism of energy conservation resembles those
of modern heterotrophs that metabolize reduced organic
compounds for the synthesis of adenosine triphosphate
(ATP) by substrate-level phosphorylation. A major question
is indeed whether the protometabolism can be inferred from
the metabolism of modern cells. The proponents of the heterotrophic scenario have often considered that the first organic molecules were produced by reactions completely independent from modern metabolism. In particular, Orgel
argued that the metabolisms of the RNA world would have
been completely erased by the emergence of a new metabolism based on proteinenzymes (Orgel, 2003). On the contrary, the proponents of the autotrophic theory tend to directly
link
the
protometabolism
to
modern
(hyperthermophilic) proteins via the coevolution of RNA
and peptides. In fact, as suggested by de Duve (2003) a metabolism entirely sustained by RNA catalysts can also be
linked to the modern one, if one reasons in terms of Darwinian evolution (de Duve, 2003) by assuming that a protein enzyme could have initially only replaced the function of an
existing ribozyme (i.e., transformation of a given substrate
into a given product). Similarly, if ribozymes themselves replaced the function of more ancient catalysts, the metabolism
of the RNA cells could have been built upon the more ancient
160
protometabolism, especially if the RNA world itself originated in the framework of Darwinian evolution between
competing protocells.
On the way to proto-cells
PERSPECTIVE
Figure
2.
Competition
between
vesicles in the early RNA world
adapted from Chen 2006. Lipid
vesicles containing mineral catalysts
hexagons and able to incorporate ribose
R and polyphosphate PP grow by capturing lipids from vesicles containing
amino acids AA only. The growth of
vesicles induces a proton gradient H +
that is used to facilitate the transport of
various compounds, followed by the synthesis of small RNA oligomers crosses.
After division, vesicles containing RNA
replicators red crosses grow at the expense of those containing RNA without
self-replicating activity blue crosses.
These grow further using additional RNA
green barrel to facilitate the transport of
small polar molecules.
driven by the physicochemical features of early systems. Finally, vesicle membrane growth generates a transmembrane
pH gradient (Chen and Szostak, 2004), suggesting that some
universal features of the living world could have their origin
in fundamental physicochemical features. The perspective
now would be to use such vesicles (with various mixtures of
putative catalysts, minerals, peptides, or ribozymes) to test if
they could favor to set up some form of protometabolism.
Origin of ribonucleotides
HFSP Journal
mixtures of minerals, peptides, and amino acids) that could
produce ribonucleotides (and activated ribonucleotides such
as NTP) from phosphorylated ribose and various bases, possibly inside lipid vesicles.
Origin of ribozymes
The polymerization of ribonucleotides in prebiotic conditions has only been achieved using nucleotide monophosphate activated by various amine compounds and using RNA
primers. It has been shown that clays (montmorillonite) catalyze the condensation of such activated substrates to form
RNA oligomers up to 40 50 nucleotides long [for recent reviews see (Muller, 2006) (Ferris, 2006) (Huang and Ferris,
2003)]. Importantly, the mineral catalysts increase the ratio
of 3 to 5 over 2 to 5 phosphodiester bonds. A major problem for the establishment of a robust RNA world is the instability of RNA due to the reactive oxygen in 2 of the ribose
(Forterre et al., 1995; Lazcano and Miller, 1996). RNA can
be stabilized by a high concentration of monovalent salts
(Hethke et al., 1999) (Tehei et al., 2002), but most ribozymes
absolutely require millimolar concentrations of divalent salts
(Woodson, 2005) which, in contrast, strongly increase RNA
degradation at high temperatures (Ginoza et al., 1964). To
solve this problem, Vlassov and co-workers have suggested
that RNA occurred first in cold environments, where synthesis would have been favored over degradation, an RNA
world on ice hypothesis (Vlassov et al., 2005). They reported that polymerization of nucleotides, ligation of small
RNAs, and other critical prebiotic chemical reactions are indeed stimulated by freezing [(Vlassov et al., 2004) and references therein]. Interestingly, a 3 5 linkage between
nucleotides is the major or even the only product formed under freezing conditions. Freezing probably accelerates some
chemical reactions in aqueous solution because of the organization of frozen water and the concentration of reactants.
In the RNA world on ice scenario, early ribozymes might
have survived transport to more warm and wet environments
by virtue of their synthetic power outpacing degradation
(Vlassov et al., 2004).
The next problem is the production of polymers of sufficient length to harbor catalytic activity (minimal ribozymes).
The smallest known ribozyme is a 7mer olinucleotide that
can cleave itself at 37 C [for reviews, see (Muller, 2006;
Vlassov et al., 2005)]. A mini-RNA ligase of 29 nucleotides
has also been obtained by in vitro selection (see below)
(Landweber and Pokrovskaya, 1999). This shows that small
ribozymes may support simple reactions of cleavage and ligation of other small RNAs. The production of large RNAs
by successive ligation of small RNAs would have opened the
way to the emergence of true ribozymes. The repertoire of
catalytic activities accessible to RNA has been systematically explored in several laboratories using modern enzymes
to produce libraries of random RNA oligomers. Large artificial ribozymes selected in vitro can catalyze a wide range of
At some point, one has to assume that an efficient polymerase was not only able to replicate itself, but also to replicate templates producing catalysts (either ribozymes or peptides) useful for the metabolism of the RNA cell [for reviews
and hypotheses on this period see (Jeffares et al., 1998; Poole
et al., 1998)]. It is likely that many different types of
ribozyme-catalyzed peptide synthesis arose, but that only
one survived, leading to the modern translation apparatus
with tRNA and ribosomes. Many authors have suggested that
protein synthesis first appeared as a by-product of RNA replication and was later on selected based on the expanding
chaperone and catalytic activities of longer and longer peptides (see below). For instance, by analogy with modern
RNA viruses that contain tRNA-like structures at their 3
end used to initiate the replication of viral genomes, Maizels
and Weiner (Maizels and Weiner, 1994) suggested that the
amino-acid module of tRNA with its CCA end first originated as a tag for genomic RNA replication (functioning
both as a telomer and as a marker for RNA to be replicated).
All modern tRNAs are monophyletic, i.e., they originated
from a single ancestral molecule that would have appeared in
a particular RNA-cell lineage. They are made of two modules, the amino-acid binding module and the module carrying the anticodon. The amino-acid binding module probably
originated first and was later on duplicated to produce the
anticodon module (Maizels and Weiner, 1994). From the
imagination of scientists, a great variety of scenarios have
been proposed to explain the origin of the translation machinery (Schimmel and Henderson, 1994) (Poole et al.,
1998) (Copley et al., 2005) (Taylor, 2006) (Szathmary, 1999)
(Wolf and Koonin, 2007). A detailed presentation of these
models is beyond the scope of this review. It is usually as-
162
PERSPECTIVE
sumed that the primitive genetic code was simpler (for instance with a two-nucleotide codon and less amino acids)
and expanded in the course of evolution. Two main theories
have been proposed, suggesting either that codon choice was
initiated by specific interaction between amino acids and anticodons (stereochemical theories) or that codon choice was
set up parallel with the evolution of the amino acid biosynthetic pathways (historical theories) [for reviews see (Di
Giulio, 2005; Ellington et al., 2000; Wong, 2005; Yarus et
al., 2005) (Knight and Landweber, 2000)]. In any case, the
modern genetic code is probably not a frozen accident, but
seems to be optimized to minimize the deleterious consequences of mutations (Vogel, 1998) [for review see (Freeland
et al., 2003)]. This indicates that the tendency to increase
faithful translation was the major selection pressure that directed the evolution of the genetic code, as suggested early
on by Woese (1965). Goldenfeld and co-workers have recently shown from in silico stimulation that an optimal code
might have become universal in the frame of a communal
evolution pervaded by intense horizontal gene transfer of
coding sequences and coding system components among coevolving communities with different codes (Vetsigian et al.,
2006). If correct, this suggests that mechanisms of gene
transfer were operational very early, allowing genetic exchange between RNA-protein cells. Theories about the origin of the genetic code should now also accommodate structural data obtained for modern amino-acyl tRNA synthetases
and ribosomes. For instance, from comparative structural
analysis, it has been suggested that all modern amino-acyl
tRNA synthetases evolved from two proteins whose initial
role was to chaperone the tRNA (Ribas de Pouplana and
Schimmel, 2001).
The first proteins were indeed probably short chaperonelike proteins that stabilized ribozymes and increased their
catalytic activities. They would also have facilitated the
transport of molecules (including nucleic acids) through the
membranes of the RNA cells, (Jay and Gilbert, 1987).
Longer genes and proteins may have originated by RNA recombination producing proteins of increasing size via a multistep combinatorial mechanism under the control of natural
selection (de Duve, 2003). Starting from a small number of
proteins of small size (corresponding to modern folds), this
mechanism would have allowed the extensive exploration of
the space sequence at each size level size. This period ended
up with the establishment of all modern protein superfamilies by the various combinations of protein folds. Recent advances in comparative and structural genomics have provided fascinating insights on this process [see for instance
many recent papers by the group of Koonin (Iyer et al., 2003)
(Iyer et al., 2004)]. Complex protein enzymes, such as large
RNA polymerases, ribonucleotide reductases, and thymydylate synthases, all required for the origin of DNA, likely only
originated at the end of this process.
HFSP Journal Vol. 1, September 2007
HFSP Journal
THE ORIGIN OF MODERN CELLS
Figure 3. LUCA was the last bottleneck in a long series of ancestors to the three present-day cellular domains: Archaea,
Bacteria, and Eukarya. Extinct lineages may have coexisted for
some time with the descendants of LUCA, and transferred some
features to them yellow arrows. The emergence of a universal
code in an earlier bottleneck organism may have been favored by
preferential transfer between organisms sharing the same genetic
code.
whereas others consider that LUCA was a modern-type bacterium (Cavalier-Smith, 2002) or even a primitive Eucaryote
with a nucleus (Fuerst, 2005). Thanks to the advances of
comparative genomics, some aspects of these hypotheses can
now be tested. The identification of a set of genes present in
Archaea, Bacteria, and Eukarya has led to the definition of a
minimal gene content for LUCA (Delaye et al., 2005; Harris
et al., 2003; Koonin, 2003). As expected from the universality of the genetic code, the minimal protein set includes a
core of ribosomal proteins, tRNA synthetases, and translation factors (for both initiation and elongation) indicating
that the translation apparatus was already well established in
LUCA. Importantly, the minimal set includes the components of machineries that are intimately associated with the
membrane, such as the signal recognition particle (SRP) and
the Sec systeminvolved in protein secretionand the
complex ATP synthasesthat function with a transmembrane proton gradient. These observations clearly indicate
that LUCA was a cellular organism with a membrane rather
similar to that of modern organisms (Jekely, 2006; Pereto et
al., 2004). It remains to be explained why modern lipids are
so different in Archaea compared to the classical lipids
found in Bacteria and Eukaryotes (including an opposite polarity) [for discussion see (Pereto et al., 2004) (Xu and
Glansdorff, 2002)]. Future experimental work should focus
on the study of vesicles made of the two types of lipids and to
the expression in bacteria of enzymes involved in the archaeal lipid pathway and vice versa.
Another controversial idea is that modern hyperthermophiles (i.e., organisms having an optimal growth temperature
above 80 C) could be the direct descendants of a heatloving LUCA. Hyperthermophiles indeed appear as early diverging lineages in the rRNA universal tree and have relatively short branches (Stetter, 2006). However, this position
might be due to the high guaninecytosine content of their
rRNAs, which could have reduced their rate of evolution
(leading to shorter branches and artifactual grouping) (Forterre, 1996). Several attempts have been made to determine
putative compositional biases in the rRNA, tRNA, or proteins from LUCA in order to determine the temperature at
which these molecules were functional [see, for instance
(Galtier et al., 1999) (Di Giulio, 2003)]. However, these approaches led to contradictory results and are hampered by
the difficulty of reconstructing ancient phylogenies and uncertainties concerning the root of the tree of life (see below).
In our opinion, a mesophilic LUCA fits better with the observation that hyperthermophiles are sophisticated organisms
that have evolved specific mechanisms to thrive at very high
temperatures [for a review see (Forterre and Philippe, 1999a;
Xu and Glansdorff, 2002)]. In particular, phylogenomics
analyses indeed suggest that reverse gyrase, an atypical DNA
topoisomerase present in all hyperthermophiles, was absent
in LUCA (Brochier-Armanet and Forterre, 2006; Forterre et
al., 2000) whereas hot-temperature-adapted lipids are not
164
A major goal of the top-down approaches in the origin-oflife field is to reconstruct the common ancestor of all extant
organisms to reach an intermediary stage between the origin
of life and the present biosphere. The basic principle of cell
division and membrane heredity (Cavalier-Smith, 2001) implies that all modern cells derive from a single cell. This historical entity was called the cenancestor (for common ancestor in Greek), the progenote, or the LUCA. This last term has
the advantage to be both neutral (unlike the term progenote,
which suggests a very primitive organism) and precise. It
clearly states that LUCA should not be confused with the
first cell, but was the product of a long period of evolution.
Being the last means that LUCA was preceded by a long succession of older ancestors. In this framework, a plethora of
cellular lineages that have left no descendants today may
have existed before LUCA. It is important to consider that
many of these were probably still present at the time of
LUCA, and some have probably even coexisted for some
time with its descendants, possibly contributing via horizontal gene transfer to some traits present in modern lineages
(Fig. 3).
A consensus on the nature of LUCA is far from reached.
For some authors LUCA was a very simple organism, even
possibly acellular (Woese, 1998) (Russell and Martin, 2004),
PERSPECTIVE
homologous in Archaea and Bacteria, suggesting a secondary adaptation that occurred independently in each of these
domains (Forterre and Philippe, 1999a; Xu and Glansdorff,
2002).
The minimal set of universal proteins includes a surprisingly small number of proteins that function in DNA replication, lacking in particular a DNA replicase, a primase, and a
helicase. This is not due to unrecognized homology since the
proteins performing these functions in Bacteria on one side,
and ArcheaEukaryotes on the other, belong to different protein superfamilies (Bailey et al., 2006; Leipe et al., 1999). To
explain this observation, Koonin and colleagues have suggested that LUCA had an RNA genome, but used DNA as a
replication intermediate (much like a retrovirus) (Leipe et
al., 1999). Alternatively, if LUCA had a DNA genome, the
ancestral system might have been replaced in one lineage
(probably in Bacteria) by a new system of viral origin (Forterre, 1999). Finally, if LUCA still had a bona fide RNA genome, Forterre suggested that the few universal proteins involved in DNA metabolism were independently introduced
by DNA viruses in the three cellular domains (Forterre,
2006). The idea that LUCA still had a RNA genome has been
recently boosted by the discovery of mechanisms for the repair of RNA damages and for enhancing the fidelity of RNA
transcription and replication. These findings have suggested
that RNAprotein cells may have reached a level of sophistication much more important than previously thought (Forterre, 2005; Poole and Logan, 2005).
Most authors assume that LUCA was identical to the last
common ancestor of Archaea and Bacteria, either because it
is commonly believed that the tree of life is rooted between
the ArchaeaEukaryotes on one side and Bacteria on the
other, or because of models where Eukaryotes originated
from some kind of association between Archaea and Bacteria
(Lopez-Garcia and Moreira, 1999; Martin and Muller, 1998;
Rivera and Lake, 2004; Wachtershauser, 2006). However, the
root of the bacterial tree and the origin of Eukaryotes remain
highly controversial (Forterre and Philippe, 1999b; Gribaldo
and Philippe, 2002), (Poole and Penny, 2007). If the root
turned out to be in the eucaryotic branch (Philippe and Forterre, 1999), several features now exclusively present in Eukaryotes could already have been present in LUCA, whereas
features common to Archaea and Bacteria might have originated in a common lineage to these two domains. At the moment, there is no definitive argument to conclude if the
archaealeukaryal or even the unique eucaryotic features
(e.g., the spliceosome and spliceosomal introns) are ancestral or derived. The same can be said for the features that are
common to Bacteria and Archaea, such as the superoperons
encoding ribosomal proteins. In any case, many puzzling observations that are difficult to fit in a single coherent scenario
remain to be explained. The question of the topology of the
universal tree of life is intimately linked to the problem of the
origin of the three domains. The main questions to be solved
HFSP Journal Vol. 1, September 2007
are (i) why three canonical versions of the ribosome (or other
universal traits) exist and (ii) how they are now so different
from each other, but so similar inside each domain (Woese,
1987). Many contradictory scenarios have been proposed
and are still actively debated (Lopez-Garcia and Moreira,
1999; Martin and Muller, 1998; Martin and Russell, 2003;
Rivera and Lake, 2004; Woese, 2002) (Cavalier-Smith,
2002) (Forterre, 2006). Much more work has to be done in
comparative biochemistry and molecular biology to test various evolutionary scenarios for all possible molecular machines present in modern organisms. In particular, it will be
critical to analyze in depth the history of all universal molecular machines (especially the translation apparatus).
PERSPECTIVES
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