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11 The Last Common Ancestor of Modern Cells
David Moreira and Purificación López-Garcı́a
11.1 The Last Common Ancestor, the Cenancestor,
LUCA: What’s in a Name?
All living beings share a number of essential features pertaining to their biochemistry and fundamental processes. Some of these features are so complex (an
outstanding example is the genetic code) that their probability to have appeared
several times independently is almost negligible. This authorizes the concept of
a common ancestor to all living beings that possessed these traits, and from
which diversification occurred, leading to the emergence of the three domains
of life that we recognize today, Archaea, Bacteria, and Eucarya. Nevertheless,
the concept of a common ancestor was born well before these universal features
were even identified, mostly on the basis of purely philosophical and theoretical
11.1.1 Some Historical Grounds
The idea that all living beings are linked by a natural process has influenced
the scientific thought for a long time. For example in his 1686 Discourse on
Metaphysics, the German philosopher Leibniz explicitly states the existence of
intermediate species between those that are distant, implying that all living beings are related in a great chain, which is intrinsic to the harmony of the universe.
Following this inspiration, many scientists have tried to identify the source of
diversity and the nature of the process unifying the different species. Darwin’s
concept of descent with modification and natural selection provided the solid
grounds to explain the patterns of similarity and difference among species that
have served as a general framework for biology until present days. In The Origin
of Species, Darwin concluded that a logical outcome of the premises of descent
with modification and natural selection is that probably all the organic beings,
which have ever lived on this earth have descended from some one primordial
form, into which life was first breathed (Darwin 1859). The concept of a common
ancestor for all life forms was born.
This idea received strong support during the last century, thanks to the
spectacular development of biochemistry and, especially, of molecular biology.
Bacteria, eukaryotes and the recently discovered archaea (Woese and Fox 1977a)
David Moreira and Purificación López-Garcı́a, The Last Common Ancestor of Modern Cells.
In: Muriel Gargaud et al. (Eds.), Lectures in Astrobiology, Vol. II, Adv. Astrobiol. Biogeophys., pp. 305–317 (2007)
DOI 10.1007/10913314 11
Springer-Verlag Berlin Heidelberg 2007
David Moreira, Purificación López-Garcı́a
share the basic structural constituents of the cell and the most fundamental
metabolic reactions. All life is based on common biochemical themes (Kornberg
2000; Pace 2001).
11.1.2 The Hypothesis of a Cenancestor
This hypothetical ancestral organism to all living beings has been baptized with
different names according to different authors. The most popular are the last
common ancestor, the cenancestor (from the Greek kainos meaning recent and
koinos meaning common) (Fitch and Upper 1987) and the last universal common ancestor or LUCA (Forterre and Philippe 1999). Although all evolutionary
biologists agree that some type of cenancestor existed, its nature is a matter of
intense and highly speculative debates. Most authors favor the idea that the cenancestor was a single organism, an individual cell that existed at a given time
and that possessed most of the features (and genes encoding them) that are
common to all contemporary organisms. From this single ancestor, the different
domains of life would have diverged (Fig 11.1A–D). Others, on the contrary,
envisage a population of cells that, as a whole, possessed all those genes, although no single individual did (Kandler 1994; Woese 1998; Woese 2000). This
implies that the level of gene exchange and spreading in this population was
very high. At some point, however, a particular successful combination of genes
occurred in a subpopulation that became isolated and gave rise to a whole line
of descent. Kandler, for instance, proposed in his pre-cell theory that bacteria,
archaea, and eukaryotes emerged sequentially in this way (Fig 11.1E) (Kandler
1994; Wächtershäuser 2003).
Single cell or population, all researchers agree that the cenancestor was already quite complex, having evolved from simpler entities, and that there was
a more or less long evolutionary path from the origin of life to the cenancestor
stage. Both, the origin of life and the nature of the cenancestor are different
evolutionary questions. Nonetheless, despite the general agreement that the cenancestor was already quite complex, the level of complexity attributed to it
varies depending on the model. For Woese, the cenancestor was a relatively primitive entity, which he called a “progenote”, that had not completely evolved the
link between genotype and phenotype (Woese and Fox 1977b). For others, the
progenote state occurred prior to the cenancestor, which was nearly a modern
cell (see review in Doolittle 2000a).
Given their universality, a ribosome-based protein synthesis (translation),
a well-developed transcription machinery for the synthesis of structural and messenger RNAs, and an energy-obtaining process based on the generation of a proton gradient across membranes (Gogarten et al. 1989), were among the features
that the cenancestor certainly possessed. Other cenancestor properties are, however, much more controversial, such as the existence of a DNA-based genome or
even the possession of lipid-based membranes. The occurrence in the cenancestor
of these properties was initially deduced mostly from biochemistry and molecular
11 The Last Common Ancestor of Modern Cells
Fig. 11.1. Current hypotheses for the evolution of the three domains of life from
a last common ancestor or cenancestor. The cenancestor stage is indicated by a blue
sphere. Models A to D envisage that all the properties attributed to the cenancestor
co-existed in the same cell, whereas in E, they were present collectively in a population
of primitive cells
David Moreira, Purificación López-Garcı́a
biology studies. Obviously, many genes (and proteins) were involved in these ancestral machineries and processes. At present, the most powerful tools to infer in
more detail which were the genes and proteins already present in the cenancestor are comparative genomics and molecular phylogeny. This type of analysis
is greatly facilitated by the increasing number of complete genome sequences
available for very different organisms. Although several problems, in particular
horizontal gene transfer and differential gene loss, make the reconstruction of
the ancestral gene content troublesome (Koonin 2003). We briefly discuss these
aspects in the following sections.
11.2 How Did the Cenancestor Make Proteins?
Prokaryotic (archaeal and bacterial) species contain approximately between 500
and 10 000 genes, whereas eukaryotic species contain approximately between
2000 and 30 000 genes. Nevertheless, when the gene content of all available
genomes is compared, only ∼60 genes are found to be common to all of them.
This set of genes is almost entirely integrated by genes encoding ribosomal RNA
and ribosomal proteins as well as other proteins involved in translation (especially aminoacyl-tRNA synthetases and translation factors) (Koonin 2003). This
implies that these genes are ancestral, and provide strong evidence that the cenancestor possessed a fully developed ribosomal-based translation machinery for
protein synthesis that was comparable to the one found in modern organisms.
Protein synthesis by ribosomes is, therefore, the most universally conserved process. Furthermore, the level of conservation appears so high that the process of
protein synthesis has remained practically unchanged for, likely, more than three
billion years.
A few of the ∼60 genes that conform the universal core encode RNA polymerase subunits. RNA polymerase is responsible for the synthesis of messenger
and other RNAs from genes (DNA templates) (Koonin 2003). As in the case of
translation, this implies that the cenancestor possessed at least part of the transcription machinery found in contemporary organisms. Nevertheless, the degree
of conservation of the transcription machinery is not as high, since several RNA
polymerase subunits and transcription factors are not universally distributed.
Transcription and translation are among the most conserved processes in
cells, and can be traced back to the cenancestor. The fact that both processes
depend primarily on structural and catalytic RNA molecules, e.g., the ribosomal
RNAs, indicates that RNA played an essential role since very early in cell evolution. This and the recent discovery of ribozymes (small catalytic RNAs) have
been important elements leading to the proposal of an “RNA!world” (for review,
see Joyce 2002). According to this model, there was a very early evolutionary
stage when RNA carried both, information-storing and catalytic functions, which
are performed today by DNA and proteins, respectively. While being broadly accepted, this model remains, however, purely hypothetical.
11 The Last Common Ancestor of Modern Cells
11.3 What Was the Nature of the Genetic Material?
Despite the fact that, in all contemporary cells, DNA is the molecule where genetic information is stored, only three out of the ∼60 universal genes are related
to DNA replication and/or repair. These are one DNA polymerase subunit, one
exonuclease and one topoisomerase (Koonin 2003). From all the genes known to
be involved in DNA replication in organisms of the three domains of life, many
are shared by archaea and eukaryotes but are absent from bacteria. The latter
apparently possesses completely unrelated genes encoding the proteins that perform the equivalent functions. Various hypotheses have been proposed to explain
the profound differences between the bacterial and archaeal/eukaryotic replication machineries. One of them even postulates that the cenancestor did not
possess a DNA genome at all. According to this model, the cenancestor would
have had an RNA genome, and DNA replication would have evolved twice independently, once in the bacterial line of descent and other in the lineage leading to
archaea and eukaryotes (Forterre 2002; Leipe et al. 1999). However, this model
is contested by different lines of evidence that, put together, suggest that the
cenancestor already possessed a DNA genome. First, although few, universally
conserved proteins and protein domains involved in DNA metabolism indeed
exist (Giraldo 2003). Second, RNA is much more error-prone than DNA due to
its higher mutation rate, so that single RNA molecules cannot exceed a certain
size (Eigen limit) without falling into replicative catastrophe (Eigen 1971, 2002).
This limit is so small, ∼30– 50kb, that an RNA molecule could contain only a few
dozen genes. Recent estimates suggest that the, already quite complex, cenancestor may have had probably more than 600 genes (Koonin 2003). If its genome
was made of RNA, many RNA molecules would have been required to contain
all those genes, which poses a serious problem of stability during replication and
partition among daughter cells. The existence of this problem is attested by the
characteristics of DNA and RNA viruses today. Whereas DNA viruses can have
genomes that reach very large sizes, up to ∼1 Mbp (Raoult et al. 2004), RNA
viruses’ genomes do not exceed ∼30kb (Domingo and Holland 1997).
The remaining models propose that the cenancestor had a DNA-based
genome. One of these explains the dichotomy of DNA replication in bacteria
and archaea/eukaryotes by stating that, whereas transcription and translation
were already well developed in the cenancestor, DNA replication was still very
primitive. DNA replication would have been improved and refined after, or simultaneously to, the separation of the two lines of descent leading to the bacteria and
to the archaea/eukaryotes (Olsen and Woese 1997). A contrasting model could
be that the cenancestor had a highly complex DNA-based metabolism and contained the ancestral versions of the proteins found today in both the bacterial
and the archaeal/eukaryotic replication machineries. One set of proteins would
be involved in replication, whereas the other would be specialized in DNA repair.
During the speciation of the two lines, only one set of proteins would have been
retained in each line of descent. Another proposal suggests that the replication
machinery was already well developed in the cenancestor, but that it evolved
David Moreira, Purificación López-Garcı́a
very fast in one or the two lineages descending from the cenancestor to the point
that the similarity between the homologous genes in both lines is no longer
recognizable (Moreira 2000; Olsen and Woese 1997). Finally, an additional hypothesis suggests that archaea and eukaryotes have retained the ancestral DNA
replication system, whereas the bacteria have seen their machinery replaced by
genes imported from viruses (Forterre 1999). However, there is no evidence for
this hypothesis but, on the contrary, many examples of the opposite, i.e., numerous acquisitions of replication-related genes by viruses from the genome of their
cellular hosts (Moreira 2000). In conclusion, although still a matter of debate,
it appears likely that the cenancestor had a DNA genome. However, the mechanism for its replication and the early divergence of the replication machineries
in the bacteria and the archaea/eukaryotes remain a mystery.
11.4 What Did the Cellular Metabolism Look Like?
The question of how metabolism looked in the cenancestor is a difficult and
complex one, and hence, is generally put aside in descriptions of a putative
ancestor. The theoretical proposal of a cenancestor is fundamentally based on
conserved genes related to the storage, expression and transmission of the genetic information present in all contemporary organisms (for recent reviews, see
Doolittle 2000a, 2000b; Koonin 2003). However, genes involved in energy and
carbon metabolism not only display a patchy distribution in organisms of the
three domains of life, but they very often belong to large multigenic families
whose members have been recruited for different functions in various metabolic
pathways. Furthermore, horizontal gene transfer is known to affect preferentially
metabolic genes, since they may confer an immediate adaptive advantage. Therefore, the reconstruction of ancestral metabolic pathways is frequently masked by
a complex history of gene duplication and differential enzyme recruitment (Castresana and Moreira 1999).
Discussions and controversies about early metabolism do take place, but they
concern the very first metabolism at the time when life arose rather than the
metabolic traits in a more evolved cenancestor. These discussions are modeldependent. If the first living beings were heterotrophs feeding upon an organic
prebiotic soup as proposed classically (Oparin 1938), then fermentation, which
is mechanistically simple, may have been the first way of gaining energy (Broda
1970), while cell building blocks were directly uptaken from the soup. If the first
living beings were chemolithoautotrophs initially developed on pyritic (FeS2 )
surfaces (Wächtershäusser 1988) or in iron monosulfide (FeS) tridimensional
compartments (Russell and Hall 1997), energy was derived from redox reactions
involving inorganic molecules such as H2 S, H2 and FeS. In this case, organic
molecules were synthesized de novo from CO2 or CO by an ancestral, yet undetermined, metabolic pathway. Today, four different pathways of autotrophic
carbon fixation are known (revised in Peretó et al. 1999). The Calvin–Benson
11 The Last Common Ancestor of Modern Cells
cycle (reductive pentose-phosphate pathway) is found in oxygenic photosynthesizers such as cyanobacteria and plants, but also in other autotrophic prokaryotes. The Arnon cycle (reductive citric acid pathway) is found in several bacteria and archaea. The Wood–Ljundahl cycle (reductive acetyl-CoA pathway) is
found in acetogenic and sulfate-reducing bacteria and methanogenic archaea. Finally, the hydroxypropionate pathway is found in the green non-sulfur bacterium
Chloroflexus sp. and a few thermophilic archaea. There is general agreement to
consider that the Calvin–Benson cycle appeared relatively late during bacterial
evolution. However, which of the other three is older is a matter of debate. The
Arnon cycle is proposed to be older by Wächtershäuser and other adherents of
the pyrite-based chemoautotrophic origin of life because of its wide distribution
in bacteria and archaea (Wächtershäuser 1990). Nevertheless, a reductive acetylCoA pathway is proposed to be the primordial autotrophic pathway because of
its higher simplicity (acetate, a two-carbon molecule is synthesized) and its exergonic (energy-releasing) nature under certain hydrothermal conditions (Russell
and Martin 2004). Finally, although less known, the hydroxypropionate pathway
is also very simple and has been proposed to be the fist autotrophic pathway at
least in phototrophic bacteria (Peretó et al. 1999).
Although the metabolic properties of the cenancestor are not generally discussed, if any or several of these pathways had developed in earlier times, the
cenancestor must have possessed them. In any case, the presence of a universal
highly conserved membrane-bound ATPase indicates that the cenancestor was
able to produce energy in the form of ATP by generating a proton gradient across
the cell membrane. What is unclear is the type of electron donors and acceptors
required to generate this proton gradient, although it might have been able to
use a variety of oxidized inorganic molecules as electron acceptors. It is also likely
that the cenancestor was able to carry out a simple heterotrophic metabolism,
at least some type of fermentation, but whether it was a full autotroph or not
remains an open question.
11.5 Was the Cenancestor Membrane-Bounded?
All contemporary cells are surrounded by a plasma membrane that is made
out of phospholipids generally organized in bilayers. However, as in the case
of replication, there exist profound differences between, this time, the membrane lipids of archaea and the membrane lipids of bacteria and eukaryotes.
In archaea, phospholipids are made out of generally isoprenoid lateral chains
that are bounded by ether linkages to glycerol-1-phosphate, whereas in bacteria and eukaryotes phospholipids are made out of fatty acids bounded by ester
linkages to glycerol-3-phosphate. From these differences, the most fundamental
is the opposite stereochemistry of the glycerol-phosphate, since some bacteria
and eukaryotes make ether linkages under certain circumstances, and since archaea do make fatty acid ether phospholipids as well (Peretó et al. 2004). The
David Moreira, Purificación López-Garcı́a
enzymes responsible for the synthesis of glycerol-1-phosphate and glycerol-3phosphate are not homologous in archaea and bacteria/eukaryotes, but belong
to two different enzymatic families. This difference is so hard to explain that
some authors have proposed that the cenancestor had not yet reached a cellular stage. Membrane lipids, and cells simultaneously, would have evolved independently from a non-enzymatic lipid synthesis pathway to generate bacteria
and archaea (Koga et al. 1998). Other authors propose that the cenancestor
did not possess a lipid membrane at all, and that membrane lipids (and their
biosynthetic pathways) were invented twice, in each one of the lineages that diverged from the cenancestor leading to the bacteria and to the archaea. Instead
of lipids, the cenancestor would have been endowed with a mineral membrane
made out of iron monosulfide; cells would be mineral compartments in a particular kind of hydrothermal chimneys (Martin and Russell 2003). Finally, another,
less radical option, is that the cenancestor had a lipid membrane, but that it was
heterochiral, i.e., it was composed by a mixture of lipids built upon glycerol-1phosphate and glycerol-3-phosphate (Wächtershäuser 2003). A subsequent specialization of the biosynthetic pathways to yield the two types of homochiral
membranes would have accompanied the speciation of archaea and bacteria. Recent phylogenetic analyses of the enzymes involved in the synthesis of glycerol
phosphate strongly suggest that the cenancestor possessed a non-stereospecific
pathway of phospholipid biosynthesis and was therefore endowed with heterochiral membranes (Peretó et al. 2004). A cenancestor endowed with a lipid membrane would be in agreement with the occurrence of several membrane-bound
proteins extremely well conserved, notably the proton-pump ATPases (Gogarten et al. 1989) and the signal recognition particle, SRP (Gribaldo and Cammarano 1998).
11.6 Other Unresolved Questions
As we have seen above, some properties of the hypothetical cenancestor appear
more or less well-defined, such as the possession of a quite modern transcription and translation machinery and, most likely, the existence of phospholipid
membranes. Other features remain obscure, such as the type of carbon and energy metabolism or the replication of the genetic material. However, there are
additional questions that remain open and that have been the subject of lively
debates. Among these, whether the cenancestor was hyperthermophilic or not,
and whether it was simple or complex.
The proposal of a hyperthermophilic cenancestor is linked to the discovery of hyperthermophilic bacteria and archaea growing optimally at >80 ◦ C,
and to the first proposals of a hot, autotrophic origin of life in a warmer early
Earth with extended hydrothermal activity (Achenbach-Richter et al. 1987; Pace
1991). The most important argument used was that hyperthermophilic prokaryotes branched at the most basal positions in phylogenetic trees (Stetter 1996).
The first criticisms to a hot origin of life derived from the fact that RNA and
11 The Last Common Ancestor of Modern Cells
other important biomolecules have relatively short life-times at high temperatures (Lazcano and Miller 1996). However, as mentioned before, the origin
of life and the cenancestor were separated in time, and might have occurred
in different environmental conditions (Arrhenius et al. 1999). Thus, some authors propose that the cenancestor was hyperthermophilic, and that the origin
of life might have taken place at much lower temperatures, but only hyperthermophiles could survive the late heavy meteorite bombardment ∼3.9Ga ago
(Gogarten-Boekels et al. 1995). However, the most important criticism to a hypothetical hyperthermophilic ancestor derives from recent phylogenetic analyses. On the one hand, computer reconstruction of ancestral ribosomal RNA
sequences suggests that the content of guanine and cytosine in the cenancestor’s RNA was incompatible with life at >80 ◦ C (Galtier et al. 1999). However, the analysis of the same datasets using other methods questions this conclusion favoring, on the contrary, a hyperthermophilic cenancestor (Di Giulio
2000). On the other hand, refined phylogenetic analyses of ribosomal RNA sequences suggest that the basal emergence of hyperthermophilic bacteria was
an artifact of phylogenetic tree reconstruction and favor the idea that they
adapted secondarily to hyperthermophily (Brochier and Philippe 2002). However, as in the previous case, the use of other phylogenetic methods comes
up with opposite results (Di Giulio 2003). At any rate, although the situation in bacteria is highly controversial, there is general agreement that the
ancestor of the archaea was indeed hyperthermophilic (Forterre et al. 2002).
Therefore, if the bacterial ancestor was also a hyperthermophile, then the
most parsimonious conclusion is that the cenancestor was hyperthermophilic.
If the bacterial ancestor was not hyperthermophilic, then it will be very difficult to infer the type of environmental conditions in which the cenancestor thrived. At any rate, all the current analyses and proposals appear compatible with the occurrence of a thermophilic (60– 80 ◦ C) cenancestor (LópezGarcı́a 1999).
Another controversial issue concerns the level of complexity that the cenancestor possessed. As stated above, it is clear that it was already very
complex. Even the authors that call it simple, envisage that its genome contained several hundred genes (∼600– 1000), which is in the range of the simplest present-day prokaryotes (Koonin 2003). Most authors imagine an ancestor that was also structurally simple, i.e., with a cellular organization resembling that of today’s prokaryotes. An ancestor of this type would have the
genetic material directly immersed in the cytoplasm, where the replication,
transcription and translation would take place. This type of ancestor is supported by the widely accepted bacterial rooting of the tree of life, i.e., that the
root of the tree of life lies between the bacteria and the archaea/eukaryotes
(Fig. 11.1A) (Woese et al. 1990), but would be also compatible with two alternative tree topologies (Fig. 11.1B,C). However, this has been challenged by
authors that propose a eukaryotic rooting of the tree of life, i.e., that the root
lies in between the eukaryotes and a branch leading to the two prokaryotic
David Moreira, Purificación López-Garcı́a
domains (Fig. 11.1D) (Brinkmann and Philippe 1999; Philippe and Forterre
1999). This eukaryotic rooting would still be compatible with a prokaryotelike cenancestor, but it opens the possibility that the cenancestor had some
of the traits that characterize modern eukaryotes, in particular the presence of
a membrane-bound nucleus and of many small RNA molecules claimed to be
relics of a hypothetical RNA world (Poole et al. 1999). In this model, prokaryotes would be derived by a reductive process from more complex eukaryotic-like
ancestors. However, although the position of the root is indeed an open question, models proposing a eukaryotic-like cenancestor do not explain how such
a complex entity was built from the prebiotic world. In this sense, a simpler,
prokaryotic-like cenancestor appears much more parsimonious in evolutionary
11.7 Perspectives
Obviously many questions have to be answered before achieving an accurate
picture of the putative cenancestor. Fortunately, it seems likely that a number of
these questions can be addressed thanks to the increasing amount of data derived
from comparative genomics. Nonetheless, a crucial issue will be to determine
the impact of horizontal gene transfer in evolution because, if horizontal gene
transfer has been rampant all along life history as some authors suggest (Doolittle
2000b), it would then be very difficult or even impossible to reconstruct any
ancestor. In a scenario of frequent or even massive horizontal gene transfer,
a single cenancestor that contained all the genes ancestral to those shared among
the three domains of life did not likely exist. Rather, these ancestral genes were
probably present in different organisms and at different times (Zhaxybayeva and
Gogarten 2004). The application of population genetics methods to the study
of gene emergence and extinction over long timescales may shed some light into
this problem.
Another open question concerns the origin and evolution of viruses, and how
these have affected cellular evolution. For instance, they may have contributed
significantly to horizontal gene transfer serving as vehicles of gene exchange.
They may have also helped to increase the evolutionary rate of many genes thus
contributing to the development of novel gene functions.
An alternative source of information to reconstruct a model portrait of the
cenancestor may come from the generation of more accurate models of the
early Earth. This could help to delineate the environmental conditions where
life arose and first evolved, giving clues, for instance, as to the putative hyperthermophilic nature of the cenancestor, and/or to the most likely metabolic
pathways it utilized. Similarly, resolving the controversies that currently exist
on the earliest microfossils and increasing the number of unambiguous fossil
data will be most helpful to establish a likely chronology of early life evolution.
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