Photosynthesis is one of the most important metabolisms for the sustaining of life on Earth. It is performed by plants, algae, and even bacteria, its purpose is to exploit solar energy for the production of sugars. By using an external source of energy, these organisms are able to convert (reduce) inorganic carbon (CO2 in the air) to organic carbon, which can be used as a source of energy.
This “jump”
from the inorganic to the organic world is done also by other organisms, by
exploiting different autotrophic metabolisms such as chemosynthesis.
Photoautotrophic organisms are involved in the maintaining of the C cycle in our planet, in particular by sequestrating CO2 from the atmosphere, and trapping it in difficult-to-hydrolyze polymers (lignin and cellulose), and by producing molecular oxygen as a side product.
Why
engineering
The next
years will be a challenge in terms of food production: with an expected population
of more than 9 billion in 2050, the majority of pressure will weigh on the
primary sector, in particular crop production, which is responsible for almost
2/3 of total consumed calories worldwide. Food security is a challenge that humans
always needed to face, and one of the main problem in this regard, are food
wastes (almost 1/3 of the produced food is discarded each year).
With a so
big problem of food managing and preservation, someone can think that the real problem
is on wasting, more than increasing productivity. And that would be
true, or better, the solution lies in the middle: reducing wastes is possible and
is mainly due to education problems than actual technology limits (most wastes comes
from houses), but with an increasing need for high-quality animal foods, and reducing
land availability, more food needs to be produced per unit of land.
The yield of crops has increased drastically in the last years, in the case of rice and wheat, for example, it almost doubled since 1960. With “yield” I’m referring to the Yield potential (Yp), defined as the mass of harvested material (fruits of grains) collected by a particular genotype in the complete absence of stresses. The Yp is influenced mainly by:
- The efficiency
of the plant of intercepting incoming light
- The partition
of energy and carbon in the harvested part
- The
conversion of the intercepted light into chemical energy
This increase
in productivity, commonly known as Green Revolution, has been possible thanks to
improved agronomy and improved crops genotypes, achieved, so far, with traditional
breeding and varieties selection. But almost no effort was put into increasing the
metabolism responsible for the conversion of the solar energy into usable chemicals by the plant (3rd factor): Photosynthesis.
It seems
that in some crops, the improvement of light detection, influenced by physiological
and climatic factors, and carbon partitioning in the plant tissue, have reached
their biological maximum. Engineering of
the pathway could be possible by “taking inspiration” from the different types
of photosynthesis evolved in plants, or in other distantly related species,
like bacteria and cyanobacteria.
What is photosynthesis
Photosynthesis
is a well-known metabolism, I will reassume just a few aspects that are
particularly important for its engineering, and I will leave additional
material for the ones interested.
In general, Photosynthesis is split into two different reactions:
During the (i)light reaction, the sunlight energy is captured as reducing potential; a molecule of chlorophyll is excited by light, resulting in an excited high-energetic state. The specific wavelength of light that is absorbed depends on the chlorophyll and other accessory pigments, chlorophyll is found in chloroplasts, specifically in the reaction center of big proteins complexes called photosystems. In this state, energy is transferred in the form of pairs of electrons to a series of other molecules until the final acceptor: NADP+, is then reduced to NADH.
As electrons are passed between each intermediate of the reaction chain, H+ ions are accumulated in the thylakoid lumen, this chemical potential is used to synthesize ATP molecules similarly to what happens during respiration. To regenerate (give back electrons and H atoms) the starting chlorophyll, water molecules are split and deprived of H atoms in a process called photolysis.
During the (ii)dark reaction, the Calvin cycle is used to fix CO2 from the atmosphere and
synthesize triose sugars. The first enzyme of the metabolism is RuBisCO and it catalyzes
the carboxylation of Ribulose 1-5P (5C sugar), the so synthesized 6C
intermediate is split, releasing two 3C sugars. One of these molecules of 3P glycerate
is used as the precursor of sugars, amino acids, or other complex biomolecules,
the other one, will continue the cycle and will regenerate the starting ribulose
molecule. During the regeneration process, ATP and NADPH produced in the
previous reaction are consumed.
Scheme of Calvin Cycle (on the right), compared to Photorespiration (see the last chapter). Source:https://fr.wikipedia.org/wiki/Fichier:Simplified_photorespiration_diagram.jpg |
Engineering of Photosynthesis
Our
capacity of engineering photosynthesis mainly depends on our knowledge of
the reactions and enzymes involved, the availability of computational models for
making predictions and performing in silico screenings, and our capability of performing
reliable gene editing (CRISPR, Zn fingers, vectors…). Photosynthesis itself
is a complex pathway, and we can act at many different levels.
The wavelength
absorbed by chlorophyll is in the range of 400-700 nm, slight differences can
be found in the 2 major types of chlorophyll: A and B (the latter acts as
accessory pigment). With this narrow range of wavelengths, none of the energy of
the near-UV or far-infrared spectrum is absorbed, reducing by half the energy
that the plant can absorb. Expansion of the spectrum further in the red is limited
by the energy of photons at low frequencies, that are not powerful enough to
drive the water photolysis. This pushes the limit of wavelengths for oxygenic photosynthetic
organisms to 750 nm, like in the case of Acaryochloris marina, a cyanobacterium that uses variants
of chlorophyll A to carry out photosynthesis underwater.
Another factor
that limits the efficiency of the photosynthetic pathway is the inefficient use
of ATP and NADPH, mostly when the incoming radiation saturates all the available
pigment, in those conditions, energy is lost by dissipation and fluorescence. Also,
the continuous changes of exposure of leaves in the canopy due to the tissue
structure, or variable climatic conditions, are another source of inefficiency.
Saturation conditions may also cause chlorophyll molecules in their excited state to transfer their energy to oxygen, leading to the formation of harmful oxygen radicals, that may cause damage, and that require energy to be managed by the cell.
Another
important bottleneck of the system is the dark reaction, in particular the
activity of the RuBisCO enzyme.
The most
abundant protein on earth: RuBisCO
This enzyme
is so abundant due to the broad extension of photosynthetic organisms on earth,
but also due to its inefficient kinetics. RuBisCo, in fact, is not specific for CO2 but can interact also with O2, leading to a series
of wasteful reactions that consume energy and previously fixed carbon (Photorespiration).
Due to this aspecific activity, large amounts of it are necessary to support an
adequate photosynthetic rate.
So, how we
can deal with this bottleneck? Well, nature can show us an example of
adaptation. The photosynthesis previously described is common only in some
species: C3 plants. In these organisms CO2 is absorbed directly from the atmosphere,
however, C4 plants (like maize and sugarcane) have evolved a mechanism to
concentrate and translocate CO2 in the vicinity of RuBisCO. This process, which
evolved 60 independent times in history as an adaptive measure, has two main
steps:
- The initial fixation of CO2 happens in the mesophyll (exterior) cells, where phosphoenolpyruvate carboxylase forms the C4 acid oxaloacetate
- The C4 acid is then transferred to the cells of the bundle sheath, where it is decarboxylated to release CO2 in the vicinity of Rubisco.
So, a
strategy could be the insertions of C4 genes in C3 crops like rice, wheat, and
oat, to increase their efficiency. A few results have been achieved in this
regard, but the lack of the correct anatomy in C3 plant leaves to sustain this
type of CO2 translocation, could be the major problem.
Another
solution could be taking inspiration from the mechanisms found in bacteria and
cyanobacteria, that use carbonic anhydrases to concentrate CO2 near the RuBisCO
site. These enzymes are pretty common and convert CO2 molecules in bicarbonate
ions (causing a decrease in pH), that are solubilized and more easily transferred.
This seems
simpler than inserting the entire C4 anatomy in C3 crops but requires the
insertion of bicarbonate and CO2 pumps in the chloroplast membrane, and correct
localization of the anhydrase activity in the plant cell to work. The latter option
seems more promising, since, it has been shown that even the addition of only
bicarbonate pumps in the chloroplast, successfully increased the efficiency of
photosynthesis.
The field
of research is open and very productive, interfering and modifying the way in which
the light is absorbed by the plant seems to be challenging and maybe more
results could be achieved by modifying the dark reactions, and other secondary
metabolisms. Modifications of vital metabolisms are not often straightforward
and can result in unexpected side, detrimental effects.
References:
- General introduction to photosynthesis:
- https://www.nationalgeographic.org/encyclopedia/photosynthesis/
- https://en.wikipedia.org/wiki/Photosynthesis#Light-dependent_reactions
- Photosynthesis in details: http://photobiology.info/Schurmann.html
- C4-C3 engineering: Matsuoka, M., Furbank, R. T., Fukayama, H., & Miyao, M. (2001). Molecular engineering of C4 photosynthesis. Annual review of plant biology, 52(1), 297-314.
- Photosynthesis review: Orr, D. J., Pereira, A. M., da Fonseca Pereira, P.,
Pereira-Lima, Í. A., Zsögön, A., & Araújo, W. L. (2017). Engineering
photosynthesis: Progress and perspectives. F1000Research, 6.
- Engineering of photosynthesis as the answer to food security: Long, S. P., Marshall-Colon, A.,
& Zhu, X. G. (2015). Meeting the global food demand of the future by
engineering crop photosynthesis and yield potential. Cell, 161(1),
56-66.
- The spectrum of absorbtion of photosynthestic organisms: Blankenship,
R. E., & Chen, M. (2013). Spectral expansion and antenna reduction can
enhance photosynthesis for energy production. Current opinion in chemical biology, 17(3), 457-461.
- RuBisCO activity and engineering: Parry, M.
A., Andralojc, P. J., Scales, J. C., Salvucci, M. E., Carmo-Silva, A. E.,
Alonso, H., & Whitney, S. M. (2013). Rubisco activity and regulation as targets for crop improvement. Journal
of experimental botany, 64(3), 717-730.
- The Calvin cycle in details: https://www.wikidoc.org/index.php/Calvin_cycle
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