but that the ancestors of the bacterial and of the archaeal
domains were (hyper)thermophilic organisms. Extant
mesophilic microorganisms would therefore have had a thermophilic domain ancestor and a, yet more distant, mesophilic
universal ancestor, LUCA.
Valuable information is also provided by experimental
palaeobiochemistry, a discipline aimed at characterising
macromolecules from extinct organisms. For example,
Gaucher and colleagues (2003) conducted a statistical reconstruction of the sequence of the elongation factor EF-Tu (an
essential protein in the translation process) in the last common ancestor of Bacteria. They then synthesised the
corresponding gene in vitro and produced the enzyme by
cloning its gene in an expression vector. Finally, they determined that the optimum temperature of the enzyme activity
is 73
C, suggesting that the last common ancestor of bacteria was thermophilic.
The various arguments that have been presented above
concerning the temperature at which LUCA lived show that
the debate on this issue is far from over.
4.1.7 Molecular Structure of Membrane
Lipids in LUCA
The membranes of contemporary cells consist mainly of
lipids arranged in a double layer or, in hyperthermophilic
Archaea, in single layer. In Bacteria and in Eucarya, the
lipid bilayer is formed by phospholipids, that is, glycerol-3phosphate (G3P) molecules linked to fatty acid molecules by
ester bonds (Fig. 4.5a). In Archaea, a glycerol-1-phosphate
(G1P, a stereoisomer of glycerol 3-phosphate) is connected
to isoprenoid chains by an ether bond (Fig. 4.5b).
The above description of lipids of the Archaea on the one
hand and of the Eucarya/Bacteria on the other hand is not
without exceptions. Indeed, lipids with an ether linkage have
been described in Eucarya and in some thermophilic Bacteria, whereas side chains composed of fatty acids have been
identified in Archaea. Homologues of genes involved in the
biosynthesis of fatty acids were found in the genomes of
archaea. However, to date no exception has been found in
the glycerol-phosphate stereochemistry (G1P in archaea vs.
G3P in bacteria and eukaryotes).
The enzymes responsible for the synthesis of G1P and
G3P from dihydroxyacetone phosphate, G1PDH and
G3PDH, are nonhomologous (i.e. have different evolutionary origins) and belong to different families of proteins
showing no structural similarity. The important question is,
what was the membrane lipid stereochemistry of LUCA?
Several models have been proposed. One of them, for example, assumes that G1P and G3P were used interchangeably in
the membranes of the first cells. The homochiral membrane
would have appeared secondarily and independently in
archaea, bacteria and eukaryotes following the acquisition
of G1PDH and G3PDH (Lombard et al. 2012).
4.1.8 Metabolism in LUCA
It is generally accepted that the early atmosphere at the time
when LUCA lived was largely anoxic. Its energy metabolism was thus either fermentative, or based on anaerobic
respiration, or based on anoxygenic photosynthesis. If
some oxygen was present in the environment, even in trace
amounts, LUCA could have adopted aerobic respiration.
This second hypothesis would imply the occurrence of respiration before oxygenic photosynthesis, an evolutionary
scenario that, although surprising, cannot be completely
ruled out (see Sect. 4.4).
4.1.9 LUCA Prokaryote, Eukaryote
or Something Else?
The most widely defended (and taught) hypothesis is that
LUCA had a cellular prokaryotic organisation, since the
prokaryotic cell has a simpler organisation than the eukaryotic cell. This assumption is reflected in the names
prokaryotes (the ‘pro-’ prefix means before; the ‘caryos’
root means nucleus) and eukaryotes (‘eu-’ means true),
which imply that the latter derived from the former. Alternatively, it was suggested that both prokaryotic and eukaryotic
modern organisms were derived from a proto-eukaryotic
ancestral structure.
The prokaryotic organisation by its own qualities – simplicity and fast cell division, metabolic flexibility, gene
exchange capacity and limited nutritional needs – has experienced extraordinary evolutionary success, irreversibly
invading the primitive biosphere and resisting all the ecological upheavals that have marked the history of our planet.
The success of the ‘eukaryotic’ approach would be equivalent, but using a different evolutionary strategy.
4.1.10 The Emergence of Three Domains
4.1.10.1 The Root of the Universal Tree of Life
Which among the Archaea, Bacteria and Eucarya came
first? This issue is still hotly debated in the scientific community. In order to know in what order the three domains of
life diverged, it would be necessary to:
1. Reconstruct the universal tree of life (i.e. based on a
molecular marker present in all living organisms)
2. Root this tree (that is to say, define the direction of
evolutionary time along tree branches)
4 For Three Billion Years, Microorganisms Were the Only Inhabitants of the Earth
83
domains were (hyper)thermophilic organisms. Extant
mesophilic microorganisms would therefore have had a thermophilic domain ancestor and a, yet more distant, mesophilic
universal ancestor, LUCA.
Valuable information is also provided by experimental
palaeobiochemistry, a discipline aimed at characterising
macromolecules from extinct organisms. For example,
Gaucher and colleagues (2003) conducted a statistical reconstruction of the sequence of the elongation factor EF-Tu (an
essential protein in the translation process) in the last common ancestor of Bacteria. They then synthesised the
corresponding gene in vitro and produced the enzyme by
cloning its gene in an expression vector. Finally, they determined that the optimum temperature of the enzyme activity
is 73
C, suggesting that the last common ancestor of bacteria was thermophilic.
The various arguments that have been presented above
concerning the temperature at which LUCA lived show that
the debate on this issue is far from over.
4.1.7 Molecular Structure of Membrane
Lipids in LUCA
The membranes of contemporary cells consist mainly of
lipids arranged in a double layer or, in hyperthermophilic
Archaea, in single layer. In Bacteria and in Eucarya, the
lipid bilayer is formed by phospholipids, that is, glycerol-3phosphate (G3P) molecules linked to fatty acid molecules by
ester bonds (Fig. 4.5a). In Archaea, a glycerol-1-phosphate
(G1P, a stereoisomer of glycerol 3-phosphate) is connected
to isoprenoid chains by an ether bond (Fig. 4.5b).
The above description of lipids of the Archaea on the one
hand and of the Eucarya/Bacteria on the other hand is not
without exceptions. Indeed, lipids with an ether linkage have
been described in Eucarya and in some thermophilic Bacteria, whereas side chains composed of fatty acids have been
identified in Archaea. Homologues of genes involved in the
biosynthesis of fatty acids were found in the genomes of
archaea. However, to date no exception has been found in
the glycerol-phosphate stereochemistry (G1P in archaea vs.
G3P in bacteria and eukaryotes).
The enzymes responsible for the synthesis of G1P and
G3P from dihydroxyacetone phosphate, G1PDH and
G3PDH, are nonhomologous (i.e. have different evolutionary origins) and belong to different families of proteins
showing no structural similarity. The important question is,
what was the membrane lipid stereochemistry of LUCA?
Several models have been proposed. One of them, for example, assumes that G1P and G3P were used interchangeably in
the membranes of the first cells. The homochiral membrane
would have appeared secondarily and independently in
archaea, bacteria and eukaryotes following the acquisition
of G1PDH and G3PDH (Lombard et al. 2012).
4.1.8 Metabolism in LUCA
It is generally accepted that the early atmosphere at the time
when LUCA lived was largely anoxic. Its energy metabolism was thus either fermentative, or based on anaerobic
respiration, or based on anoxygenic photosynthesis. If
some oxygen was present in the environment, even in trace
amounts, LUCA could have adopted aerobic respiration.
This second hypothesis would imply the occurrence of respiration before oxygenic photosynthesis, an evolutionary
scenario that, although surprising, cannot be completely
ruled out (see Sect. 4.4).
4.1.9 LUCA Prokaryote, Eukaryote
or Something Else?
The most widely defended (and taught) hypothesis is that
LUCA had a cellular prokaryotic organisation, since the
prokaryotic cell has a simpler organisation than the eukaryotic cell. This assumption is reflected in the names
prokaryotes (the ‘pro-’ prefix means before; the ‘caryos’
root means nucleus) and eukaryotes (‘eu-’ means true),
which imply that the latter derived from the former. Alternatively, it was suggested that both prokaryotic and eukaryotic
modern organisms were derived from a proto-eukaryotic
ancestral structure.
The prokaryotic organisation by its own qualities – simplicity and fast cell division, metabolic flexibility, gene
exchange capacity and limited nutritional needs – has experienced extraordinary evolutionary success, irreversibly
invading the primitive biosphere and resisting all the ecological upheavals that have marked the history of our planet.
The success of the ‘eukaryotic’ approach would be equivalent, but using a different evolutionary strategy.
4.1.10 The Emergence of Three Domains
4.1.10.1 The Root of the Universal Tree of Life
Which among the Archaea, Bacteria and Eucarya came
first? This issue is still hotly debated in the scientific community. In order to know in what order the three domains of
life diverged, it would be necessary to:
1. Reconstruct the universal tree of life (i.e. based on a
molecular marker present in all living organisms)
2. Root this tree (that is to say, define the direction of
evolutionary time along tree branches)
4 For Three Billion Years, Microorganisms Were the Only Inhabitants of the Earth
83