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Ancestral clock proteins in cyanobacteria reveal link between Earth's rotation and photosynthetic rhythms

To better understand the circadian clock in modern-day cyanobacteria, a Japanese research team has studied ancient timekeeping systems. They examined the oscillation of the clock proteins KaiA, KaiB, and KaiC (Kai-proteins) in modern cyanobacteria, comparing it to the function of ancestral Kai proteins.

Their research is in the Nature Communications.

"Extant cyanobacteria utilize a circadian clock to predict the light-dark environmental cycle by the Earth's rotation in order to achieve efficient photosynthetic reactions. We wanted to know the evolutionary history of when ancient bacteria acquired the circadian clock and how this property was inherited by the present cyanobacteria," said Atsushi Mukaiyama, Associate Professor, Fukui Prefectural University.

Cyanobacteria, sometimes called blue-green algae, are photosynthetic bacteria that influence Earth's oceans and atmosphere in important ways. Scientists know that the most recent common ancestor of cyanobacteria emerged about 3 billion years ago. It evolved into the current ecosystem through the Great Oxidation event, which occurred when the level of oxygen in Earth's atmosphere rose about 2.3 billion years ago.

This evolution continued through at least two Snowball Earth events, about 2.4 and 0.7 billion years ago, when the planet was covered in ice, and through the Neoproterozoic Oxygenation event, when Earth's oxygen levels rose a second time. The Neoproterozoic Oxygenation event occurred between 800 and 540 million years ago.

Through studies of fossils and molecular evolution models, scientists suggest that the most recent common ancestor of cyanobacteria already possessed primitive oxygen photosynthetic systems. The efficiency of photosynthesis is strongly influenced by light-dark environmental cycles.

The research team set out to examine whether primitive cyanobacteria had a timekeeping system when photosynthesis became active during the Great Oxidation event. This can help scientists understand the physiological origin of circadian clock systems.

Scientists have identified circadian clocks, those internal timekeepers that guide an organism to run on a 24-hour clock, in various organisms, such as bacteria, fungi, plants, and mammals.

The research team studied the cyanobacteria's circadian clock using the cyanobacteria strain Synechococcus elongatus. They reconstructed the clock oscillator in a test tube using the clock protein KaiC. They also examined the function and structure of ancestral Kai proteins to determine how self-sustained Kai-protein oscillators have evolved over time.

Knowing that light–dark cycles affect how efficient photosynthesis is in cyanobacteria, the team wanted to determine whether ancient cyanobacteria possessed a self-sustained circadian clock when the ancient oxidation events occurred and the photosynthetic systems were first established.

They discovered that faster rhythmic phenomenon was encoded in ancestral clock proteins. "The ancient cyanobacterial clock was synchronized to the cycle of 18 to 20 hours. This means that the history of Earth's rotation period has been restored by tracing the evolution of clock protein molecules," said Yoshihiko Furuike, Assistant Professor, Institute for Molecular Science.

The team's results show that the oldest KaiC in ancestral bacteria lacked the function and structure that is essential for rhythmic qualities. Through molecular evolution, the ancestral Kai proteins acquired the necessary function and structure around the Global Oxidation and Snowball Earth events.

Eventually, the most recent common ancestor of cyanobacteria capable of photosynthesis inherited this self-sustained circadian oscillator.

These results are extremely helpful in scientists' understanding of chronobiology.

"Our ultimate goal is to design modified cyanobacteria that can adapt to the rotation period of planets and satellites other than Earth by shortening or lengthening the period of the Kai-protein oscillator. Cyanobacteria have taken a long time to tune their clock to 24 hours, but we may be able to achieve even faster evolution using modern knowledge and technology," said Shuji Akiyama, Professor, Institute for Molecular Science.