Origin and subsequent evolution of the process by which light energy is used to synthesize sugars
The
evolution of photosynthesis
refers to the origin and subsequent evolution of
photosynthesis
, the process by which light energy is used to assemble
sugars
from
carbon dioxide
and a hydrogen and electron source such as water. It is believed that the pigments used for photosynthesis initially were used for protection from the harmful effects of light, particularly ultraviolet light. The process of photosynthesis was discovered by
Jan Ingenhousz
, a Dutch-born British physician and scientist, first publishing about it in 1779.
[1]
The first photosynthetic organisms probably
evolved
early in the
evolutionary history of life
and most likely used
reducing agents
such as
hydrogen
rather than water.
[2]
There are three major
metabolic pathways
by which photosynthesis is carried out:
C
3
photosynthesis
,
C
4
photosynthesis
, and
CAM photosynthesis
. C
3
photosynthesis is the oldest and most common form. A C3 plant uses the
Calvin cycle
for the initial steps that incorporate CO
2
into organic material. A C4 plant prefaces the Calvin cycle with reactions that incorporate CO
2
into four-carbon compounds. A CAM plant uses
crassulacean acid metabolism
, an adaptation for photosynthesis in arid conditions. C4 and CAM plants have special adaptations that save water.
[3]
Origin
[
edit
]
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Available evidence from geobiological studies of
Archean
(>2500 Ma)
sedimentary rocks
indicates that life existed 3500 Ma. Fossils of what are thought to be
filamentous
photosynthetic organisms have been dated at 3.4 billion years old,
[4]
[5]
consistent with recent studies of photosynthesis.
[6]
[7]
Early photosynthetic systems, such as those from
green
and
purple sulfur
and
green
and
purple nonsulfur bacteria
, are thought to have been anoxygenic, using various molecules as
electron donors
. Green and purple sulfur bacteria are thought to have used
hydrogen
and
hydrogen sulfide
as electron and hydrogen donors. Green nonsulfur bacteria used various
amino
and other
organic acids
. Purple nonsulfur bacteria used a variety of nonspecific organic and inorganic molecules.
[8]
It is suggested that photosynthesis likely originated at low-wavelength geothermal light from acidic hydrothermal vents, Zn-tetrapyrroles were the first photochemically active pigments, the photosynthetic organisms were anaerobic and relied on
H
2
S
without relying on H
2
emitted by alkaline hydrothermal vents. The divergence of anoxygenic photosynthetic organisms at the photic zone could have led to the ability to strip electrons from
H
2
S
more efficiently under ultraviolet radiation. There is geochemical evidence that suggests that anaerobic photosynthesis emerged 3.3 to 3.5 billion years ago. The organisms later developed a Chlorophyll F synthase. They could have also stripped electrons from soluble metal ions although it is unknown.
[9]
The first oxygenic photosynthetic organisms are proposed to be
H
2
S
-dependent.
[9]
It is also suggested photosynthesis originated under sunlight, using
H
2
S
emitted by volcanoes and hydrothermal vents which ended the need for scarce H
2
emitted by alkaline hydrothermal vents.
[10]
Oxygenic photosynthesis uses water as an electron donor, which is
oxidized
to molecular
oxygen
(
O
2
) in the
photosynthetic reaction center
. The biochemical capacity for oxygenic photosynthesis evolved in a
common ancestor
of extant
cyanobacteria
.
[11]
The first appearance of free oxygen in the
atmosphere
is sometimes referred to as the
oxygen catastrophe
. The geological record indicates that this transforming event took place during the
Paleoproterozoic
era at least 2450?2320 million years ago (Ma), and, it is speculated, much earlier.
[12]
[13]
A clear paleontological window on cyanobacterial
evolution
opened about 2000 Ma, revealing an already-diverse biota of blue-greens.
Cyanobacteria
remained principal
primary producers
throughout the
Proterozoic Eon
(2500?543 Ma), in part because the redox structure of the oceans favored photoautotrophs capable of
nitrogen fixation
.
[14]
Green algae
joined blue-greens as major primary producers on
continental shelves
near the end of the
Proterozoic
, but only with the
Mesozoic
(251?65 Ma) radiations of dinoflagellates, coccolithophorids, and diatoms did
primary production
in marine shelf waters take modern form. Cyanobacteria remain critical to
marine ecosystems
as primary producers in oceanic gyres, as agents of biological nitrogen fixation, and, in modified form, as the
plastids
of marine algae.
[15]
Modern photosynthesis in plants and most photosynthetic prokaryotes is oxygenic.
Timeline of photosynthesis on Earth
[
edit
]
4.6 billion years ago
|
Earth forms
|
3.4 billion years ago
|
First photosynthetic bacteria appear
|
2.7 billion years ago
|
Cyanobacteria become the first oxygen producers
|
2.4 ? 2.3 billion years ago
|
Earliest evidence (from rocks) that oxygen was in the atmosphere
|
1.2 billion years ago
|
Red and brown algae become structurally more complex than bacteria
|
0.75 billion years ago
|
Green algae outperform red and brown algae in the strong light of shallow water
|
0.475 billion years ago
|
First land plants ? mosses and liverworts
|
0.423 billion years ago
|
Vascular plants evolve
|
Source:
[16]
Symbiosis and the origin of chloroplasts
[
edit
]
Several groups of animals have formed
symbiotic
relationships with photosynthetic algae. These are most common in
corals
,
sponges
and
sea anemones
. It is presumed that this is due to the particularly simple
body plans
and large surface areas of these animals compared to their volumes.
[17]
In addition, a few marine
mollusks
Elysia viridis
and
Elysia chlorotica
also maintain a symbiotic relationship with chloroplasts they capture from the algae in their diet and then store in their bodies. This allows the mollusks to survive solely by photosynthesis for several months at a time.
[18]
[19]
Some of the genes from the plant
cell nucleus
have even been transferred to the slugs, so that the chloroplasts can be supplied with proteins that they need to survive.
[20]
An even closer form of symbiosis may explain the origin of chloroplasts. Chloroplasts have many similarities with
photosynthetic bacteria
, including a circular
chromosome
, prokaryotic-type
ribosomes
, and similar proteins in the photosynthetic reaction center.
[21]
[22]
The
endosymbiotic theory
suggests that photosynthetic bacteria were acquired (by
endocytosis
) by early
eukaryotic
cells to form the first
plant
cells. Therefore, chloroplasts may be photosynthetic bacteria that adapted to life inside plant cells. Like
mitochondria
, chloroplasts still possess their own DNA, separate from the
nuclear DNA
of their plant host cells and the genes in this chloroplast DNA resemble those in
cyanobacteria
.
[23]
DNA in chloroplasts codes for
redox
proteins such as photosynthetic reaction centers. The
CoRR Hypothesis
proposes that this
Co
-location is required for
R
edox
R
egulation.
Evolution of photosynthetic pathways
[
edit
]
In its simplest form, photosynthesis is adding water to CO
2
to produce sugars and oxygen, but a complex chemical pathway is involved, facilitated along the way by a range of
enzymes
and co-enzymes. The
enzyme
RuBisCO
is responsible for "fixing" CO
2
? that is, it attaches it to a carbon-based molecule to form a sugar, which can be used by the plant, releasing an oxygen molecule along the way. However, the enzyme is notoriously inefficient, and just as effectively will also fix oxygen instead of CO
2
in a process called
photorespiration
. This is energetically costly as the plant has to use energy to turn the products of photorespiration back into a form that can react with CO
2
.
[
citation needed
]
[24]
Concentrating carbon
[
edit
]
The
C
4
metabolic pathway
is a valuable recent evolutionary innovation in plants, involving a complex set of adaptive changes to
physiology
and
gene expression
patterns.
[25]
About 7600 species of plants use C
4
carbon fixation, which represents about 3% of all terrestrial species of plants. All these 7600 species are
angiosperms
.
C
4
plants evolved carbon concentrating mechanisms. These work by increasing the concentration of CO
2
around RuBisCO, thereby facilitating photosynthesis and decreasing photorespiration. The process of concentrating CO
2
around RuBisCO requires more energy than allowing gases to
diffuse
, but under certain conditions ? i.e. warm temperatures (>25 °C), low CO
2
concentrations, or high oxygen concentrations ? pays off in terms of the decreased loss of sugars through photorespiration.
[
citation needed
]
One type of C
4
metabolism employs a so-called
Kranz anatomy
. This transports CO
2
through an outer mesophyll layer, via a range of organic molecules, to the central bundle sheath cells, where the CO
2
is released. In this way, CO
2
is concentrated near the site of RuBisCO operation. Because RuBisCO is operating in an environment with much more CO
2
than it otherwise would be, it performs more efficiently.
[
citation needed
]
[26]
In C
4
photosynthesis, carbon is fixed by an enzyme called PEP carboxylase, which, like all enzymes involved in C
4
photosynthesis, originated from non-photosynthetic ancestral enzymes.
[27]
[28]
A second mechanism,
CAM photosynthesis
, is a
carbon fixation
pathway that evolved in some
plants
as an adaptation to
arid
conditions.
[29]
[30]
The most important benefit of CAM to the plant is the ability to leave most leaf
stomata
closed during the day.
[31]
This reduces water loss due to
evapotranspiration
. The stomata open at night to collect CO
2
, which is stored as the four-carbon acid
malate
, and then used during
photosynthesis
during the day. The pre-collected CO
2
is concentrated around the enzyme
RuBisCO
, increasing
photosynthetic efficiency
. More CO
2
is then harvested from the atmosphere when stomata open, during the cool, moist nights, reducing water loss.
[
citation needed
]
CAM has
evolved convergently
many times.
[32]
It occurs in 16,000 species (about 7% of plants), belonging to over 300
genera
and around 40
families
, but this is thought to be a considerable underestimate.
[33]
It is found in
quillworts
(relatives of
club mosses
), in
ferns
, and in
gymnosperms
, but the great majority of plants using CAM are
angiosperms
(flowering plants).
[
citation needed
]
Evolutionary record
[
edit
]
These two pathways, with the same effect on RuBisCO, evolved a number of times independently ? indeed, C
4
alone arose 62 times in 18 different plant
families
. A number of 'pre-adaptations' seem to have paved the way for C
4
, leading to its clustering in certain clades: it has most frequently developed in plants that already had features such as extensive vascular bundle sheath tissue.
[34]
Whole-genome and individual gene duplication are also associated with C
4
evolution.
[35]
Many potential evolutionary pathways resulting in the C
4
phenotype
are possible and have been characterised using
Bayesian inference
,
[25]
confirming that non-photosynthetic adaptations often provide evolutionary stepping stones for the further evolution of C
4
.
The C
4
construction is most famously used by a subset of grasses, while CAM is employed by many succulents and
cacti
. The trait appears to have emerged during the
Oligocene
, around
25 to 32
million years ago
;
[36]
however, they did not become ecologically significant until the
Miocene
,
6 to 7
million years ago
.
[37]
Remarkably, some charcoalified fossils preserve tissue organised into the Kranz anatomy, with intact bundle sheath cells,
[38]
allowing the presence C
4
metabolism to be identified without doubt at this time. Isotopic markers are used to deduce their distribution and significance.
C
3
plants preferentially use the lighter of two
isotopes
of carbon in the atmosphere,
12
C, which is more readily involved in the chemical pathways involved in its fixation. Because C
4
metabolism involves a further chemical step, this effect is accentuated. Plant material can be
analysed
to deduce the ratio of the heavier
13
C to
12
C. This ratio is denoted
δ
13
C
. C
3
plants are on average around 14‰ (parts per thousand) lighter than the atmospheric ratio, while C
4
plants are about 28‰ lighter. The
δ
13
C
of CAM plants depends on the percentage of carbon fixed at night relative to what is fixed in the day, being closer to C
3
plants if they fix most carbon in the day and closer to C
4
plants if they fix all their carbon at night.
[39]
It is troublesome procuring original fossil material in sufficient quantity to analyse the grass itself, but fortunately there is a good proxy: horses. Horses were globally widespread in the period of interest, and browsed almost exclusively on grasses. There's an old phrase in
isotope palæontology
, "you are what you eat (plus a little bit)" ? this refers to the fact that organisms reflect the isotopic composition of whatever they eat, plus a small adjustment factor. There is a good record of horse teeth throughout the globe, and their
δ
13
C
has been measured. The record shows a sharp negative inflection around
6 to 7
million years ago
, during the Messinian, and this is interpreted as the rise of C
4
plants on a global scale.
[37]
When is C
4
an advantage?
[
edit
]
While C
4
enhances the efficiency of RuBisCO, the concentration of carbon is highly energy intensive. This means that C
4
plants only have an advantage over C
3
organisms in certain conditions: namely, high temperatures and low rainfall. C
4
plants also need high levels of sunlight to thrive.
[40]
Models suggest that, without wildfires removing shade-casting trees and shrubs, there would be no space for C
4
plants.
[41]
But, wildfires have occurred for 400 million years ? why did C
4
take so long to arise, and then appear independently so many times? The Carboniferous period (~
300
million years ago
) had notoriously high oxygen levels ? almost enough to allow
spontaneous combustion
[42]
? and very low CO
2
, but there is no C
4
isotopic signature to be found. And there doesn't seem to be a sudden trigger for the Miocene rise.
[
citation needed
]
During the Miocene, the atmosphere and climate were relatively stable. If anything, CO
2
increased gradually from
14 to 9
million years ago
before settling down to concentrations similar to the Holocene.
[43]
This suggests that it did not have a key role in invoking C
4
evolution.
[36]
Grasses themselves (the group which would give rise to the most occurrences of C
4
) had probably been around for 60 million years or more, so had had plenty of time to evolve C
4
,
[44]
[45]
which, in any case, is present in a diverse range of groups and thus evolved independently. There is a strong signal of climate change in South Asia;
[36]
increasing aridity ? hence increasing fire frequency and intensity ? may have led to an increase in the importance of grasslands.
[46]
However, this is difficult to reconcile with the North American record.
[36]
It is possible that the signal is entirely biological, forced by the fire- and grazer-
[47]
driven acceleration of grass evolution ? which, both by increasing weathering and incorporating more carbon into sediments, reduced atmospheric CO
2
levels.
[47]
Finally, there is evidence that the onset of C
4
from
9 to 7
million years ago
is a biased signal, which only holds true for North America, from where most samples originate; emerging evidence suggests that grasslands evolved to a dominant state at least 15Ma earlier in South America.
[
citation needed
]
See also
[
edit
]
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[
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