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Earth was not always the blue-green world we know today: early Earth's oxygen levels were about a million times lower than we now experience. There were no forests and no animals. For ancient organisms, oxygen was toxic. What did life look like at that time then?

A recent study led by Fatima Li-Hau (graduate student at ELSI at the time of the research) along with the supervisor Associate Professor Shawn McGlynn (at the time of research) of the Earth-Life Science Institute (ELSI) at Institute of Science Tokyo, Japan, explores this question by examining iron-rich hot springs that mimic the chemistry of Earth's ancient oceans around the time of one of Earth's most dramatic changes: the oxygenation of the atmosphere.

Their findings, in the journal Microbes and Environments, suggest that early microbial communities used iron, along with oxygen released by photosynthetic microbes, for energy, revealing a transitional ecosystem where life turned a waste product of one organism into a new energy source before photosynthesis became dominant.

The Great Oxygenation Event (GOE) occurred around 2.3 billion years ago and marked the rise of atmospheric oxygen, likely triggered by green cyanobacteria that used sunlight to split water, subsequently converting carbon dioxide into oxygen through photosynthesis.

The result is that the current atmosphere is around 78% nitrogen and 21% oxygen, with only traces of other gases such as methane and carbon dioxide, which might have played a greater role before the rise of oxygen.

The GOE fundamentally changed the course of life on Earth. This high amount of oxygen allows us animals to breathe, but it also complicates life for ancient life forms, which were almost unaware of the O₂ molecule. Understanding how these ancient microbes adapted to the presence of oxygen remains a major question.

To answer this, the team studied five hot springs in Japan, which are rich in varied water chemistries. Those five springs (one in Tokyo, two each in Akita and Aomori prefectures) are naturally rich in ferrous iron (Fe²⁺). They are rare in today's oxygen-rich world because ferrous iron quickly reacts with oxygen and turns into an insoluble ferric iron form (Fe³⁺).

But in these springs, the water still contains high levels of ferrous iron, low levels of oxygen, and a near-neutral pH, conditions thought to resemble parts of early Earth's oceans.

"These iron-rich hot springs provide a unique natural laboratory to study microbial metabolism under early Earth-like conditions during the late Archean to early Proterozoic transition, marked by the Great Oxidation Event. They help us understand how primitive microbial ecosystems may have been structured before the rise of plants, animals, or significant atmospheric oxygen," says Shawn McGlynn, who supervised Li-Hau during her dissertation work.

In four of the five hot springs, the team found microaerophilic iron-oxidizing bacteria to be the dominant microbes. These organisms thrive in low-oxygen conditions and use ferrous iron as an energy source, converting it into ferric iron.

Cyanobacteria, known for producing oxygen through photosynthesis, were also present but in relatively small numbers. The only exception was one of the Akita hot springs, where non-iron-based metabolisms were surprisingly dominant.

Using metagenomic analysis, the team assembled over 200 high-quality microbial genomes and used them to analyze in detail the functions of microbes in the community.

The same microbes that coupled iron and oxygen metabolism converted a toxic compound into an energy source and helped maintain conditions that allowed oxygen-sensitive anaerobes to persist.

These communities carried out essential biological processes such as carbon and nitrogen cycling, and the researchers also found evidence of a partial sulfur cycle, identifying genes involved in sulfide oxidation and sulfate assimilation. Given that hot springs contained very little sulfur compounds, this was a surprising discovery.

The researchers propose that this may indicate a "cryptic" sulfur cycle, where microbes recycle sulfur in complex ways that are not yet fully understood.

"Despite differences in geochemistry and microbial composition across sites, our results show that in the presence of ferrous iron and limited oxygen, communities of microaerophilic iron oxidizers, oxygenic phototrophs, and anaerobes consistently coexist and sustain remarkably similar and complete biogeochemical cycles," says Li-Hau.

The research suggests a shift in our understanding of early ecosystems, showing that microbes may have harnessed energy from iron oxidation and oxygen produced by early phototrophs.

The study proposes that, similar to these hot springs, early Earth-hosted ecosystems were composed of diverse microbes, including iron-oxidizing bacteria, anaerobes, and cyanobacteria living alongside one another and modulating oxygen concentrations.

"This paper expands our understanding of microbial ecosystem function during a crucial period in Earth's history, the transition from an anoxic, iron-rich ocean to an oxygenated biosphere at the onset of the GOE. By understanding modern analog environments, we provide a detailed view of metabolic potentials and community composition relevant to early Earth's conditions," says Li-Hau.

Together, these insights deepen our understanding of life's early evolution on Earth and have implications for the search for life on other planets with geochemical conditions similar to those of early Earth.