4.4.2 Appearance of Oxygenic Photosynthesis
and Its Consequences
4.4.2.1 Modification of the Atmospheric
Composition
During the evolution of the usage of solar energy as an
energy source, a major step was taken with the appearance
of cyanobacteria capable of oxygenic photosynthesis. They
acquired the ability to use an energy source (solar energy)
and an electron donor (water) that were available in inexhaustible quantities in the environment. In evolutionary
terms, their appearance represents a major innovation
and cyanobacteria experienced considerable expansion.
Massively producing dioxygen through time, they profoundly changed the composition of the atmosphere of the
planet, allowing the development of aerobic respiration.
Without cyanobacteria, eukaryotes and especially multicellular organisms, as currently known, would have probably
never appeared. The appearance of dioxygen upset the
biogeochemical cycles of many elements including iron,
which, spontaneously oxidised in the presence of dioxygen,
precipitates as in mineral form and becomes a life-limiting
factor in the oceans.
It is difficult to estimate with precision the evolution of
the concentration of dioxygen in the atmosphere (Fig. 4.11).
It seems clear that the activity of cyanobacteria in the oceans
is the source of almost all atmospheric O 2 , whose content
greatly increased around 2.3 Ga ago to reach its current
value more than a billion years later. However, the production of O 2 by cyanobacteria could have started much earlier.
The time lag between dioxygen production by cyanobacteria
and its accumulation in the atmosphere could be explained
by the oxygenation of the multitude of reduced mineral
species, such as iron, and by the oxygenation of the oceans.
The transformation of ferrous iron to ferric iron led to the
formation of deposits called ‘banded iron formations’ (BIF)
that are today an important source of iron ore. After the
complete conversion of ferrous iron to ferric iron precipitate,
the oceans would have gradually become saturated in
dioxygen, which subsequently diffused into the atmosphere
to reach its present concentration.
The atmospheric dioxygen content before 2 billion years
is hotly debated. For most scientists, the primitive atmosphere and oceans were predominantly anoxic. For others,
the O 2 content would have been sufficient to allow the
emergence of a form of aerobic life. It has also been
suggested that the presence in the oceans and in shallow
lagoon systems of ‘oases’, powered by relatively intense
photosynthesis, could have promoted the emergence of an
aerobic metabolism before the overall oxygenation of the
atmosphere.
The dioxygen produced by cyanobacteria, which gradually invaded all terrestrial and aquatic habitats, could have
been a dangerous poison for all forms of prokaryotic or
eukaryotic anaerobic life. This is because, although
dioxygen itself is not toxic, its radical derivatives called
‘free radicals’ (the superoxide ion hydrogen peroxide) are
highly reactive, toxic chemical species. However, the
increase of dioxygen in the atmosphere and in the oceans
did not occur abruptly, as described above. Very likely, in
parallel to the gradual increase of the O 2 concentration,
some organisms developed defence systems to eliminate
these free radicals (appearance of enzymes such as superoxide dismutase, catalase and peroxidase).
4.4.2.2 Appearance of a Protective Ozone Layer
Another consequence of increased dioxygen was the formation of an ozone (O 3 ) layer, which is a very effective barrier
against ultraviolet radiation of short wavelength, lethal to all
living organisms.
As this kind of radiation is efficiently attenuated by water
(a few tens of centimetres to several metres of water suffice),
ocean life could develop even in the absence of an ozone
layer. The appearance of a protective ozone layer could
allow the expansion of microorganisms to the land surface.
4.4.2.3 Emergence of New Pathways
in Biogeochemical Cycles
The oxygenation of the atmosphere completely modified the
functioning of biogeochemical cycles: aerobic biodegradation of organic matter, oxidation of ammonium into nitrate
and of hydrogen sulphide to sulphate, etc. (See Chap. 14).
4.4.2.4 Dioxygen Is Used as a Terminal Electron
Acceptor: The Appearance of Aerobic
Respiration
The generally accepted paradigm, which was previously
presented in this chapter, posits that oxygenic photosynthesis predated aerobic respiration. Aerobic respiration would
have appeared either from the evolution of electron transport
chains of the photosynthetic apparatus or from the respiratory chain of denitrifying microorganisms (Saraste and
Castresana 1994). One possible explanation for the success
of aerobic respiration is the higher energetic efficiency than
possible with anaerobic respiration.
The emergence of oxygenic photosynthesis before that of
aerobic respiration is however not unanimously accepted.
Indeed, for some scientists, aerobic respiration predated
oxygenic photosynthesis. Their hypothesis is based on
phylogenetic analyses suggesting that LUCA could have
possessed at least one cytochrome oxidase, an enzyme
reducing dioxygen in H 2 O and, therefore, could have been
an aerobic organism (Castresana 2004). If aerobic respiration actually predated the onset of oxygenic photosynthesis,
the question of the origin of respired dioxygen arises.
One possibility is its production by abiotic reactions such
4 For Three Billion Years, Microorganisms Were the Only Inhabitants of the Earth
103
and Its Consequences
4.4.2.1 Modification of the Atmospheric
Composition
During the evolution of the usage of solar energy as an
energy source, a major step was taken with the appearance
of cyanobacteria capable of oxygenic photosynthesis. They
acquired the ability to use an energy source (solar energy)
and an electron donor (water) that were available in inexhaustible quantities in the environment. In evolutionary
terms, their appearance represents a major innovation
and cyanobacteria experienced considerable expansion.
Massively producing dioxygen through time, they profoundly changed the composition of the atmosphere of the
planet, allowing the development of aerobic respiration.
Without cyanobacteria, eukaryotes and especially multicellular organisms, as currently known, would have probably
never appeared. The appearance of dioxygen upset the
biogeochemical cycles of many elements including iron,
which, spontaneously oxidised in the presence of dioxygen,
precipitates as in mineral form and becomes a life-limiting
factor in the oceans.
It is difficult to estimate with precision the evolution of
the concentration of dioxygen in the atmosphere (Fig. 4.11).
It seems clear that the activity of cyanobacteria in the oceans
is the source of almost all atmospheric O 2 , whose content
greatly increased around 2.3 Ga ago to reach its current
value more than a billion years later. However, the production of O 2 by cyanobacteria could have started much earlier.
The time lag between dioxygen production by cyanobacteria
and its accumulation in the atmosphere could be explained
by the oxygenation of the multitude of reduced mineral
species, such as iron, and by the oxygenation of the oceans.
The transformation of ferrous iron to ferric iron led to the
formation of deposits called ‘banded iron formations’ (BIF)
that are today an important source of iron ore. After the
complete conversion of ferrous iron to ferric iron precipitate,
the oceans would have gradually become saturated in
dioxygen, which subsequently diffused into the atmosphere
to reach its present concentration.
The atmospheric dioxygen content before 2 billion years
is hotly debated. For most scientists, the primitive atmosphere and oceans were predominantly anoxic. For others,
the O 2 content would have been sufficient to allow the
emergence of a form of aerobic life. It has also been
suggested that the presence in the oceans and in shallow
lagoon systems of ‘oases’, powered by relatively intense
photosynthesis, could have promoted the emergence of an
aerobic metabolism before the overall oxygenation of the
atmosphere.
The dioxygen produced by cyanobacteria, which gradually invaded all terrestrial and aquatic habitats, could have
been a dangerous poison for all forms of prokaryotic or
eukaryotic anaerobic life. This is because, although
dioxygen itself is not toxic, its radical derivatives called
‘free radicals’ (the superoxide ion hydrogen peroxide) are
highly reactive, toxic chemical species. However, the
increase of dioxygen in the atmosphere and in the oceans
did not occur abruptly, as described above. Very likely, in
parallel to the gradual increase of the O 2 concentration,
some organisms developed defence systems to eliminate
these free radicals (appearance of enzymes such as superoxide dismutase, catalase and peroxidase).
4.4.2.2 Appearance of a Protective Ozone Layer
Another consequence of increased dioxygen was the formation of an ozone (O 3 ) layer, which is a very effective barrier
against ultraviolet radiation of short wavelength, lethal to all
living organisms.
As this kind of radiation is efficiently attenuated by water
(a few tens of centimetres to several metres of water suffice),
ocean life could develop even in the absence of an ozone
layer. The appearance of a protective ozone layer could
allow the expansion of microorganisms to the land surface.
4.4.2.3 Emergence of New Pathways
in Biogeochemical Cycles
The oxygenation of the atmosphere completely modified the
functioning of biogeochemical cycles: aerobic biodegradation of organic matter, oxidation of ammonium into nitrate
and of hydrogen sulphide to sulphate, etc. (See Chap. 14).
4.4.2.4 Dioxygen Is Used as a Terminal Electron
Acceptor: The Appearance of Aerobic
Respiration
The generally accepted paradigm, which was previously
presented in this chapter, posits that oxygenic photosynthesis predated aerobic respiration. Aerobic respiration would
have appeared either from the evolution of electron transport
chains of the photosynthetic apparatus or from the respiratory chain of denitrifying microorganisms (Saraste and
Castresana 1994). One possible explanation for the success
of aerobic respiration is the higher energetic efficiency than
possible with anaerobic respiration.
The emergence of oxygenic photosynthesis before that of
aerobic respiration is however not unanimously accepted.
Indeed, for some scientists, aerobic respiration predated
oxygenic photosynthesis. Their hypothesis is based on
phylogenetic analyses suggesting that LUCA could have
possessed at least one cytochrome oxidase, an enzyme
reducing dioxygen in H 2 O and, therefore, could have been
an aerobic organism (Castresana 2004). If aerobic respiration actually predated the onset of oxygenic photosynthesis,
the question of the origin of respired dioxygen arises.
One possibility is its production by abiotic reactions such
4 For Three Billion Years, Microorganisms Were the Only Inhabitants of the Earth
103