ES-06-0003

Green sea hypothesis: coevolution of photosynthetic organism and habitat and suggestion of a possible biosignature

Taro Matsuo

Cyanobacteria induced the great oxidation event (GOE) around 2.4 billion years ago, leading to the promotion of biodiversity. However, the birth and prosperity of cyanobacteria on the Earth are still shrouded in mystery. To tackle this question, we need to understand why cyanobacteria developed their own light-harvesting antennas for photosynthesis containing phycobilin pigments, which are largely different from those of the other photosynthetic organisms such as the light-harvesting complex containing chlorophyll. Notably, the two pigments have complementary absorption spectra: the phycobilin pigment for absorbing green light and chlorophyll-a for the blue and red light. Here, we propose a scenario for developing the own light-harvesting system in cyanobacteria, named the "green sea hypothesis." Focusing on the fact that the available light spectrum for photosynthetic organisms is characterized by the degree of oxidation on the surface, the Earth's history is mainly divided into three eras from the perspective of the coevolution of photosynthetic organisms and its habitat:
1. Birth of photosynthetic microorganisms in fully reduced water
2. Evolution of cyanobacteria from its common ancestor in a partially oxidized photic zone
3. Formation of the modern light-harvesting system on the fully oxidized surface
After the photosystems consisting of the chlorophyll pigment have been completed, the green sea formed by oxidization of the photic zone cultivated the phycobilin pigments in the second era. The modern photosynthetic organisms do not apply the pigments related to the green light to the light-harvesting system after GOE. This big picture of the photosynthesis evolution is matched to the characteristics of the common ancestor based on the evolutionary tree analysis of cyanobacteria and the cultivation experiments of ancestor cyanobacteria under a simulated green sea. This green sea indicates an oxygenic photosynthesis in the reduced water, which is a possible new biosignature for the search for life activity on nearby habitable exoplanets with future space telescopes.