fermentation and may contain DNA (see Sect. 5.4.2). It has
been now clearly demonstrated that hydrogenosomes and
mitosomes are highly derived mitochondria (Shiflett and
Johnson 2010).
These examples show that the absence of mitochondria is
not the mark of a poorly advanced cellular organisation but,
rather, the result of evolution by simplification linked to a
particular lifestyle, with loss of the mitochondrial genome as
well as of all genes of the respiratory chain. Noticeably, a
double-membraned intracellular organelle derived from
mitochondria seems to have been conserved in all extant
eukaryotic organisms.
The phenomenon of evolutionary simplification also
applies to the evolutionary history of the agents of malaria,
Plasmodium falciparum, and toxoplasmosis, Toxoplasma
gondii. Sequencing the genome of these organisms has
revealed the presence of extranuclear genomes sharing a
common evolutionary origin with chloroplast genomes of
photosynthetic eukaryotes. These genomes were localised in
cell structures that were detected in microscopy but whose
function was not previously understood. Apicomplexa, the
phylum to which Plasmodium and Toxoplasma belong, are
now seen as having a non-photosynthetic organelle, the
apicoplast, evolved by simplification of an ancestral chloroplast (see Sect. 7.8.4).
4.4
Synthetic Approach of the Evolution
of Metabolisms
What mechanisms of energy acquisition and carbon fixation
did microorganisms use during evolution?
The present state of our knowledge does not allow determining precisely the different stages of development of these
mechanisms. However, thanks to clues provided by geological, palaeontological, palaeoclimatic and phylogenetic studies and coupled with knowledge of the diversity of
contemporary microbial metabolism, it is possible to speculate about the occurrence of different metabolisms during
evolution (Nealson and Rye 2003). It is nevertheless necessary to bear in mind that this speculation says nothing (or
very little) about the metabolism of LUCA.
4.4.1 The Primordial Metabolism:
Heterotrophic or Autotrophic?
There are two hypotheses concerning the metabolism of the
first living beings (Ehrlich 2002). In the first, the primitive
metabolism would have been of the fermentative type and
would thus be heterotrophic. Given the universality of glycolysis in today’s living world, it is tempting to assume that
this, probably very ancient, mechanism was present in
LUCA and even perhaps in the first organisms. In this
view, ATP, which is the storage form of energy, was produced by substrate-level phosphorylation. Fermented
molecules would have had an abiotic origin. The fermentation products – organic acids – released into the environment
would have decreased the extracellular pH. Because the first
membranes were supposed to have been permeable to
protons, the cell must have had a proton pump consuming
a large part of the ATP produced by fermentation to maintain
its internal pH (Fig. 4.19a). Subsequently, membrane
proteins constituting rudimentary electron transfer chains
would have appeared, fuelled by non-fermentable organic
substrates present in the environment (Fig. 4.19b). The
expulsion of a proton (H
+
), possibly coupled to the activity
of the respiratory chains, would have allowed the maintenance of intracellular pH compatible with the physiology of
the cells and the creation of a membrane potential via a
proton gradient between the inside and the outside of the
cell. As the membrane became impermeable to protons, their
return within the cell would have occurred by means of an
ATP-synthesising enzyme, functionally comparable to the
ATP synthase present in extant cells (Fig. 4.19c). This
mechanism – the coupling between a proton gradient
generated by electron transfer and ATP synthesis –
corresponds to Peter Mitchell’s chemiosmotic theory.
Its presence in the three domains of life suggests that it
appeared early during evolution. Some cells (the ancestors
of future autotrophic organisms) would then have acquired
the ability to use carbon dioxide as a carbon source.
It is also possible (second hypothesis) that the first living
organisms were able, from the outset, to assimilate CO 2 ;
in this case, autotrophy would have preceded heterotrophy.
Organic molecules synthesised by autotrophic organisms
could have been a source of food for the first heterotrophic
organisms. If autotrophy appeared first, it is unclear if
it was chemolitho-autotrophy or photoautotrophy (Ehrlich
2002).
Assuming chemolitho-autotrophy preceded phototrophy,
energy needs would have been met by the use of mineral
elements present on the early Earth (dihydrogen, iron,
hydrogen sulphide, etc.). In the absence of dioxygen,
electrons produced by redox reactions would have been
transferred to a final acceptor, such as iron (Vargas et al.
1998) or elementary sulphur (Fig. 4.19d), and these
organisms would have been chemolitho-autotrophic. Data
obtained from isotopic fractionation suggest the appearance
of autotrophic CO 2 fixation around 3.8 billion years.
Similarly, sulphate-reducing organisms could have been
active around 3.47 billion years (Shen and Buick 2004).
Moreover, direct association of fossil microorganisms with
a volcanic particle substrate in similarly aged rocks is
strongly indicative of chemolithotrophy (Westall et al.
2011a, b). However, Philippot et al. (2007) suggested
sulphide could be produced by disproportionation of
elementary sulphur rather than sulphate reduction.
4 For Three Billion Years, Microorganisms Were the Only Inhabitants of the Earth
101
been now clearly demonstrated that hydrogenosomes and
mitosomes are highly derived mitochondria (Shiflett and
Johnson 2010).
These examples show that the absence of mitochondria is
not the mark of a poorly advanced cellular organisation but,
rather, the result of evolution by simplification linked to a
particular lifestyle, with loss of the mitochondrial genome as
well as of all genes of the respiratory chain. Noticeably, a
double-membraned intracellular organelle derived from
mitochondria seems to have been conserved in all extant
eukaryotic organisms.
The phenomenon of evolutionary simplification also
applies to the evolutionary history of the agents of malaria,
Plasmodium falciparum, and toxoplasmosis, Toxoplasma
gondii. Sequencing the genome of these organisms has
revealed the presence of extranuclear genomes sharing a
common evolutionary origin with chloroplast genomes of
photosynthetic eukaryotes. These genomes were localised in
cell structures that were detected in microscopy but whose
function was not previously understood. Apicomplexa, the
phylum to which Plasmodium and Toxoplasma belong, are
now seen as having a non-photosynthetic organelle, the
apicoplast, evolved by simplification of an ancestral chloroplast (see Sect. 7.8.4).
4.4
Synthetic Approach of the Evolution
of Metabolisms
What mechanisms of energy acquisition and carbon fixation
did microorganisms use during evolution?
The present state of our knowledge does not allow determining precisely the different stages of development of these
mechanisms. However, thanks to clues provided by geological, palaeontological, palaeoclimatic and phylogenetic studies and coupled with knowledge of the diversity of
contemporary microbial metabolism, it is possible to speculate about the occurrence of different metabolisms during
evolution (Nealson and Rye 2003). It is nevertheless necessary to bear in mind that this speculation says nothing (or
very little) about the metabolism of LUCA.
4.4.1 The Primordial Metabolism:
Heterotrophic or Autotrophic?
There are two hypotheses concerning the metabolism of the
first living beings (Ehrlich 2002). In the first, the primitive
metabolism would have been of the fermentative type and
would thus be heterotrophic. Given the universality of glycolysis in today’s living world, it is tempting to assume that
this, probably very ancient, mechanism was present in
LUCA and even perhaps in the first organisms. In this
view, ATP, which is the storage form of energy, was produced by substrate-level phosphorylation. Fermented
molecules would have had an abiotic origin. The fermentation products – organic acids – released into the environment
would have decreased the extracellular pH. Because the first
membranes were supposed to have been permeable to
protons, the cell must have had a proton pump consuming
a large part of the ATP produced by fermentation to maintain
its internal pH (Fig. 4.19a). Subsequently, membrane
proteins constituting rudimentary electron transfer chains
would have appeared, fuelled by non-fermentable organic
substrates present in the environment (Fig. 4.19b). The
expulsion of a proton (H
+
), possibly coupled to the activity
of the respiratory chains, would have allowed the maintenance of intracellular pH compatible with the physiology of
the cells and the creation of a membrane potential via a
proton gradient between the inside and the outside of the
cell. As the membrane became impermeable to protons, their
return within the cell would have occurred by means of an
ATP-synthesising enzyme, functionally comparable to the
ATP synthase present in extant cells (Fig. 4.19c). This
mechanism – the coupling between a proton gradient
generated by electron transfer and ATP synthesis –
corresponds to Peter Mitchell’s chemiosmotic theory.
Its presence in the three domains of life suggests that it
appeared early during evolution. Some cells (the ancestors
of future autotrophic organisms) would then have acquired
the ability to use carbon dioxide as a carbon source.
It is also possible (second hypothesis) that the first living
organisms were able, from the outset, to assimilate CO 2 ;
in this case, autotrophy would have preceded heterotrophy.
Organic molecules synthesised by autotrophic organisms
could have been a source of food for the first heterotrophic
organisms. If autotrophy appeared first, it is unclear if
it was chemolitho-autotrophy or photoautotrophy (Ehrlich
2002).
Assuming chemolitho-autotrophy preceded phototrophy,
energy needs would have been met by the use of mineral
elements present on the early Earth (dihydrogen, iron,
hydrogen sulphide, etc.). In the absence of dioxygen,
electrons produced by redox reactions would have been
transferred to a final acceptor, such as iron (Vargas et al.
1998) or elementary sulphur (Fig. 4.19d), and these
organisms would have been chemolitho-autotrophic. Data
obtained from isotopic fractionation suggest the appearance
of autotrophic CO 2 fixation around 3.8 billion years.
Similarly, sulphate-reducing organisms could have been
active around 3.47 billion years (Shen and Buick 2004).
Moreover, direct association of fossil microorganisms with
a volcanic particle substrate in similarly aged rocks is
strongly indicative of chemolithotrophy (Westall et al.
2011a, b). However, Philippot et al. (2007) suggested
sulphide could be produced by disproportionation of
elementary sulphur rather than sulphate reduction.
4 For Three Billion Years, Microorganisms Were the Only Inhabitants of the Earth
101