A physiological perspective on the origin and evolution of photosynthesis

Area of Science:

• Biochemistry
• Astrobiology
• Evolutionary Biology

Background:

• Early Earth ecosystems were chemotrophic, relying on geological H2 at hydrothermal vents for energy and CO2 fixation.
• The evolution of chlorophyll-based phototrophy (chlorophototrophy) provided an alternative energy source, reducing reliance on H2.
• High-intensity surface radiation posed a risk to early photosynthetic cells, suggesting an origin in protected environments.

Purpose of the Study:

• To review the origin and early evolution of photosynthesis from an ecophysiological viewpoint.
• To explore the transition from chemotrophic to phototrophic metabolisms.
• To propose a model for the emergence of photosynthesis in early Earth environments.

Main Methods:

• Literature review and synthesis of ecophysiological and evolutionary data.
• Analysis of the biochemical requirements for early photosynthesis, including pigments and electron transport chains.
• Hypothesizing the environmental conditions and evolutionary steps leading to photosynthesis.

Main Results:

• Photosynthesis likely began at hydrothermal vents using low-intensity geothermal light and possibly Zn-tetrapyrrole pigments.
• The evolution involved red-absorbing chlorophyll-like pigments, type-1 reaction centers using H2S, and a progression from anoxygenic to oxygenic photosynthesis.
• Photothioautotrophy served as a crucial intermediate step, sustaining primary production in Archean oceans.

Conclusions:

• Photosynthesis originated in an anoxygenic cyanobacterial progenitor, with chlorophyll a as the ancestral pigment.
• Anoxygenic chlorophototrophic lineages acquired key components through horizontal gene transfer from cyanobacteria.
• The evolution of photosynthesis was a gradual process, bridging chemolithoautotrophy and water-splitting, ultimately shaping early Earth's biosphere.