Endosymbiotic evolution of Photosynthesis challenges Neo-Darwinism

Article "Taming the perils of photosynthesis by eukaryotes: constraints on endosymbiotic evolution in aquatic ecosystems" by Shin-ya Miyagishima:

Ancestral eukaryotes acquired photosynthesis through the genetic integration of a cyanobacterial endosymbiont, giving rise to chloroplasts. This endosymbiotic event marked a pivotal moment in eukaryotic evolution, enabling autotrophy and paving the way for the diversification of photosynthetic organisms. However, photosynthesis comes at a cost. The process of converting light energy into chemical energy inevitably generates reactive oxygen species (ROS), which can cause oxidative stress and damage cellular components.

Photosynthetic eukaryotes have evolved a suite of mechanisms to mitigate oxidative stress, including:

1. Regulating chloroplast light absorption: Excess light exposure can exacerbate ROS production. Photosynthetic organisms employ photoprotective mechanisms, such as non-photochemical quenching (NPQ), to dissipate excess energy as heat, preventing the accumulation of harmful ROS.

2. Repairing or removing damaged chloroplasts: Chloroplasts are the primary sites of ROS production during photosynthesis. To maintain cellular health, photosynthetic organisms have developed mechanisms to repair or remove damaged chloroplasts. These mechanisms involve identifying and dismantling damaged chloroplasts, preventing them from further contributing to oxidative stress.

The evolution of these stress-mitigating mechanisms has been shaped by constraints imposed by the endosymbiotic origin of chloroplasts. The ancestral eukaryote that acquired photosynthesis had to adapt its existing cellular machinery to cope with the ROS generated by its newly acquired endosymbiont. This process likely involved extending preexisting mechanisms for dealing with oxidative stress from mitochondrial respiration to the chloroplast.

The limitations of these mechanisms become apparent in acquired phototrophic organisms, which are organisms that obtain photosynthetic capabilities through means other than endosymbiosis. These organisms, such as ciliates that sequester chloroplasts from algal prey (kleptoplasts), often exhibit reduced capacity to cope with oxidative stress compared to organisms with innate chloroplasts. This suggests that the evolutionary pathways leading to acquired phototrophy may have been constrained by the need to adapt existing stress-mitigating mechanisms to a foreign photosynthetic apparatus.

The article "Taming the perils of photosynthesis by eukaryotes: constraints on endosymbiotic evolution in aquatic ecosystems" sheds light on the intricate relationship between photosynthesis and oxidative stress in eukaryotes. It highlights the challenges faced by photosynthetic organisms in balancing the benefits of autotrophy with the inherent risks of ROS production. Understanding these constraints is crucial for comprehending the evolutionary trajectory of photosynthetic eukaryotes and their adaptation to diverse aquatic environments.

The concepts of the article  challenges neo-Darwinism in several ways.

1. The evolution of photosynthetic eukaryotes is not solely driven by natural selection.

Neo-Darwinism suggests that evolution is primarily driven by natural selection, which favors traits that enhance an organism's reproductive success. However, the evolution of photosynthetic eukaryotes involved the acquisition of a cyanobacterial endosymbiont, which is a significant genetic and metabolic change that could not have occurred solely through natural selection. This suggests that other evolutionary mechanisms, such as symbiosis and horizontal gene transfer, may also play important roles in evolution.

2. The evolution of photosynthetic eukaryotes is constrained by the need to mitigate oxidative stress.

Photosynthesis generates reactive oxygen species (ROS), which can damage cells. To mitigate this oxidative stress, photosynthetic eukaryotes have developed various antioxidant and repair mechanisms. The article suggests that these mechanisms may have limited the evolutionary potential of photosynthetic eukaryotes, as they may have prevented the development of more efficient or novel photosynthetic pathways.

3. The evolution of photosynthetic eukaryotes is not a smooth, linear process.

Neo-Darwinism often portrays evolution as a gradual process of adaptation. However, the evolution of photosynthetic eukaryotes involved several abrupt transitions, such as the acquisition of the cyanobacterial endosymbiont and secondary endosymbiotic events. These transitions suggest that evolution may be more punctuated than previously thought.

4. The evolution of photosynthetic eukaryotes is not always driven towards increased fitness.

Neo-Darwinism suggests that evolution favors traits that enhance an organism's fitness. However, the acquisition of the cyanobacterial endosymbiont initially reduced the fitness of the host cell, as it would have required the host to provide resources to the endosymbiont. This suggests that evolution may not always be driven towards increased fitness, and that trade-offs between different traits may be important.

Overall, the article challenges the notion that neo-Darwinism is a complete and unchallenged theory of evolution. It highlights the role of symbiosis, horizontal gene transfer, and constraints in shaping evolutionary trajectories. These insights suggest that a more nuanced understanding of evolution is needed to fully explain the diversity of life on Earth.