Hot springs in Japan give insight into ancient microbial life on Earth
Iron-oxidising bacteria in the iron-rich hot springs suggest early microbes used iron and trace oxygen, not sunlight, as their primary energy source during the planet's shift from a low-oxygen to a high-oxygen atmosphere about 2.3 billion years ago.
image:
The picture shows Fatima Li-Hau preparing to sample water and sediment from a hot spring at low tide.
view moreCredit: Natsumi Noda, ELSI
Earth was not always the blue-green world we know today: the 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 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 the 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-oxidising 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 analyse 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 oxidisers, 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-oxidising 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 analogue 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.
Reference
Fatima Li-Hau1,2*, Mayuko Nakagawa2, Takeshi Kakegawa3, L.M. Ward4, Yuichiro Ueno1,2, and Shawn Erin McGlynn2,5,6*, Metabolic Potential and Microbial Diversity of Late Archean to Early Proterozoic Ocean Analog Hot Springs of Japan, Microbes and Environments, DOI: 10.1264/jsme2.ME24067
- Earth and Planetary Sciences Department, Institute of Science Tokyo, Tokyo, Japan
- Earth-Life Science Institute (ELSI), Institute of Science Tokyo, Tokyo, Japan
- Earth and Planetary Material Sciences, Tohoku University, Sendai, Japan
- Department of Geosciences, Smith College, Massachusetts, USA
- Blue Marble Space Institute of Science, Seattle, WA, USA
- Biofunctional Catalyst Research Team, RIKEN Center for Sustainable Resource Science, Wako, Japan
More information
Earth-Life Science Institute (ELSI) is one of Japan's ambitious World Premiere International research centers, whose aim is to achieve progress in broadly inter-disciplinary scientific areas by inspiring the world's greatest minds to come to Japan and collaborate on the most challenging scientific problems. ELSI's primary aim is to address the origin and co-evolution of the Earth and life.
Institute of Science Tokyo (Science Tokyo) was established on October 1, 2024, following the merger between Tokyo Medical and Dental University (TMDU) and Tokyo Institute of Technology (Tokyo Tech), with the mission of "Advancing science and human wellbeing to create value for and with society."
World Premier International Research Center Initiative (WPI) was launched in 2007 by Japan's Ministry of Education, Culture, Sports, Science and Technology (MEXT) to foster globally visible research centers boasting the highest standards and outstanding research environments. Numbering more than a dozen and operating at institutions throughout the country, these centers are given a high degree of autonomy, allowing them to engage in innovative modes of management and research. The program is administered by the Japan Society for the Promotion of Science (JSPS).
A panoramic picture of a hot spring from the source to the ocean
A close-up picture of the sediment and rocks of one of five hot springs during low tide, showing iron oxide mineral precipitates.
A panoramic picture of one of five hot springs during winter, showing the source water and CO2 bubbles.
A picture of the Sea of Japan as seen from one of five hot springs, where Shawn E. McGlynn is conducting sampling. Orange discharge of oxidated spring water can be seen flowing into the sea.
Credit
Fatima Li-Hau, ELSI
Journal
Microbes and Environments
Method of Research
Observational study
Subject of Research
Not applicable
Article Title
Metabolic Potential and Microbial Diversity of Late Archean to Early Proterozoic Ocean Analog Hot Springs of Japan
Minute witnesses from the primordial sea
Researchers at ETH Zurich have been able to measure - for the first time - how the amount of dissolved organic carbon in the sea has changed over geological time. The results reveal that our explanations of how the ice ages and complex life forms came about
ETH Zurich
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Cross-section of an egg-shaped iron oxide stone: It holds information about the amount of organic carbon in the sea millions of years ago, much like a time capsule.
view moreCredit: Nir Galili /ETH Zurich
Earth scientists often face huge challenges when researching the earth’s history: many significant events occurred such a long time ago that there is little direct evidence available. Consequently, researchers often have to rely on indirect clues or on computer models. The team led by ETH Professor Jordon Hemingway, however, has now discovered a unique natural witness to this period: tiny egg-shaped iron oxide stones that can be used to directly measure the carbon reserves in the primordial ocean.
Viewed on the outside, they resemble grains of sand, but in terms of their formation, these so-called ooids are more like rolling snowballs: they grow by layers as they are pushed across the sea floor by the waves. In the process, organic carbon molecules adhere to them and become part of the crystal structure.
Examining these impurities, Hemingway's team has succeeded in retracing the supply of organic carbon in the sea - by up to 1.65 billion years. In the journal Nature, the researchers show that, between 1,000 and 541 million years ago, this store was considerably lower than previously assumed. These findings refute the common explanations of significant geochemical and biological events of that time and cast a new light on the history of the Earth.
The ocean as a reservoir of life’s building blocks
How does carbon get into the oceans? On the one hand, carbon dioxide (CO2) dissolves from the air into seawater and is transported to the depths by mixing processes and ocean currents, where it is retained for a long time. On the other hand, organic carbon is produced by photosynthetic organisms such as phytoplankton or certain bacteria. Using the energy of sunlight and CO2, these microscopic organisms produce organic carbon compounds themselves. When the organisms die, they slowly sink towards the sea floor as marine snow. If it reaches the sea floor without being eaten by organisms along the way, the carbon is stored in the sea floor for millions of years.
But it is not only phytoplankton that provides a supply of carbon components. The building blocks of life are also reused: microorganisms decompose excrement and dead organisms, thereby releasing the building blocks again. These molecules form what is known as dissolved organic carbon, which drifts freely in the ocean: a huge reservoir of building blocks that contains 200 times more carbon than is actually ‘built into’ marine life.
The oxygen revolution changed everything
Based on anomalies in oceanic sedimentary rocks, researchers assumed that this building block reservoir must have been particularly voluminous between 1,000 and 541 million years ago. For a long time, this assumption served as the foundation for explaining how ice ages and complex life emerged at the same time. The photosynthetic production of the building blocks of life is closely linked to the development of the atmosphere and more complex life forms. It was only through photosynthesis that oxygen began to accumulate in the atmosphere.
In two waves - referred to as the oxygen catastrophes - the oxygen content rose to its current level of 21 per cent. Both events were accompanied by extreme ice ages that covered the entire planet in glaciers. Nevertheless, life continued to tinker and potter with new inventions: during the first oxygen catastrophe 2.4 to 2.1 billion years ago, organisms developed a metabolism converting food into energy with the help of oxygen. This exceedingly efficient way of generating energy enabled the development of more complex life forms.
Carbon content much lower than assumed
Hemingway's team is tracking such connections between geochemical and biological developments. The researchers have developed a new method that allows them to directly determine the size of the marine building block store at that particular time, based on the carbon particles in ooids.
"Our results contradict all previous assumptions," as Hemingway summarises. According to the measurements taken by the ETH researchers, between 1,000 to 541 million years ago, the ocean did not contain more, but actually 90 to 99 per cent less dissolved organic carbon than it does today. It was only after the second oxygen catastrophe that the values rose to the current level of 660 billion tonnes of carbon.
"We need new explanations for how ice ages, complex life and oxygen increase are related," says lead author Nir Galili. He explains the massive shrinkage of the carbon store with the emergence of larger organisms at that time: single-celled and early multicellular organisms sank faster after their death, thereby increasing marine snowfall.
However, the carbon particles were not recycled in the deeper layers of the ocean because there was very little oxygen there. They settled on the sea floor, causing the reservoir of dissolved organic carbon to decline sharply. It was only when oxygen accumulated in the deep sea that the carbon reservoir grew back to its current volume.
From the primordial ocean to the present day
Although the periods studied are long past, the research findings are significant for the future. They change our view of how life on earth and possibly also on exoplanets has developed. At the same time, they help us understand how the earth responds to disturbances, and humans are one such disturbance: the warming and pollution of the oceans caused by human activities are currently leading to a decline in marine oxygen levels. Consequently, it cannot be ruled out that the events described could repeat themselves in the distant future.
Reference
Galili N, Bernasconi SM, Nissan A et al.: The geologic history of marine dissolved organic carbon from iron oxides. Nature, 13 August 2025, doi: 10.1038/s41586-025-09383-3
Journal
Nature
Article Title
The geologic history of marine dissolved organic carbon from iron oxides
CaptionCarbon cycle in the ocean 1,000 to 541 million years ago.
Carbon cycle in the ocean today.
Credit
S. Hegelbach and J. Kuster / ETH Zurich
Important events in the history of the Earth
Credit
Jordon Hemingway / ETH Zurich
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