Snowball Earth's iron deposits may have formed through microbes living without sunlight

Iron is one of the most abundant metals on Earth's surface, yet how such massive iron ore deposits formed throughout geological history has long remained a mystery. The prevailing theory has been that ancient photosynthetic bacteria oxidized iron, causing it to precipitate and accumulate in the oceans.

Now, a team of Korean researchers has discovered iron-oxidizing microorganisms and key genes in marine sediments beneath the Antarctic Larsen C Ice Shelf, an environment isolated from light and oxygen. Their experiments confirmed that a key protein encoded by these microbes can oxidize iron, offering new clues to how massive iron formations developed on ancient Earth.

The team included Professor Jihyun F. Kim, Dr. Jaekyung Yoon, Dr. Boyoung Lee, and Dr. Min-Jung Kwak from Yonsei University; Professor Hwan Su Yoon from Sungkyunkwan University; Dr. Kyu-Cheul Yoo from the Korea Polar Research Institute; Professor Chung Yeon Hwang from Seoul National University; and Professor Soon-Kyeong Kwon from Gyeongsang National University. They analyzed environmental DNA preserved in marine sediments beneath the ice shelf.

Through metagenomic analysis, they identified a new clade of chemolithotrophic bacteria capable of oxidizing iron(II) in environments where light and oxygen are restricted. They also experimentally demonstrated that the bacterium's Cyc2 protein—a porin-cytochrome fusion protein located in the bacterial outer membrane—acts as a biocatalyst, converting iron(II) to iron(III).

Snowball Earth challenges the photosynthesis model

This discovery is particularly significant because iron and oxygen are critical elements for understanding Earth's history and the evolution of life. In particular, massive banded iron formations (BIFs), composed of alternating layers of iron and silica, have long been thought to have formed through the activity of photosynthetic bacteria.

However, BIFs from the Cryogenian "Snowball Earth" period of the Neoproterozoic Era, when the planet is believed to have been covered by ice hundreds of meters thick, posed a major challenge to this hypothesis. The research team found crucial clues beneath Antarctic ice shelves.

Sediment DNA reveals an iron-oxidizing bacterium

In 2013, the icebreaking research vessel Araon collected a 2.4-meter-long (7.9-foot-long) Holocene sediment core (GC16B) from the seafloor at a depth of 324 meters (1,063 feet) near the Larsen C Ice Shelf, on the front line of climate change. The research team analyzed the genetic information of the microbiota contained in the environmental DNA from this core. This sedimentary layer preserves records of the marine environment that shifted as the ice shelf changed over a span of about 12,000 years, from the last glacial period of the Quaternary Period in the Cenozoic Era to the present.

The team identified bacteria acting as network hubs within the anaerobic microbial ecosystem of sediment layers resembling BIFs formed beneath the ice shelf. They observed alternating dominance between two distinct microbial groups closely associated with these bacteria. This cyclical pattern could offer a biological explanation for the repetitive banding seen in BIFs.

The researchers reconstructed and analyzed the genome of this keystone species, revealing it to be a new lineage of chemolithotrophic bacteria. Experimental validation confirmed its presence in the sediment samples. The bacterium was provisionally named "Candidatus Mariimomonas ferrooxydans." Within its genome, the team discovered a gene encoding the Cyc2 protein, believed to be involved in iron oxidation.

The research team then cloned the cyc2 gene into E. coli and expressed it, observing that iron(II) was rapidly oxidized to insoluble iron(III), leading to precipitation. This provides direct experimental evidence of the iron-oxidizing activity of the Cyc2 enzyme. Since iron(III) is far less soluble in water than iron(II), its accumulation on the seafloor over time could lead to the formation of iron minerals.

A pathway potentially predating photosynthesis

This study offers insights into how microorganisms survived and cycled iron in ice-covered oceans during the Snowball Earth period. In particular, it points to a new microbiological mechanism for the formation of banded iron formations that could not be fully explained by the traditional photosynthesis-centered model.

Furthermore, the findings suggest that iron oxidation by chemolithotrophic bacteria may have operated not only in light-deprived environments but also on ancient Earth from the Archean to the early Proterozoic eons, when even anoxygenic photosynthesis had not yet emerged. This points to the possibility that it is a universal biogeochemical mechanism throughout geological history.

By uncovering a new iron oxidation pathway that challenges the conventional photosynthesis-based model of iron deposit formation, the discovery could reshape our understanding of iron formation in Earth science, geology, life science, microbiology, geobiology, biogeochemistry and other fields.

Connecting reconstructed genomes with experimental evidence

Yoon, a research professor at Yonsei University's Laboratory of Microbial Genomics and Systems/Synthetic Biology, who led the analysis as the paper's first author, explained, "By analyzing DNA from Antarctic sediments containing records spanning over 10,000 years, we reconstructed the environmental conditions and microbial ecosystems of that time.

"Connecting genome reconstruction of key microorganisms with functional validation is a major achievement of this study. It presents an empirical research methodology that goes beyond sequence data analysis in environmental genomics, enabling us to solve unresolved puzzles in Earth's history."

Kim, director of the Microbiome Research Institute and lead investigator of the study, stated, "This marks the first instance of finding a sediment layer beneath an Antarctic ice shelf analogous to BIFs from the Snowball Earth period and using advanced microbiome analysis techniques to confirm that chemolithotrophic iron-oxidizing bacteria could contribute to iron deposit formation.

"This expands the traditional photosynthesis-centered perspective on iron formation and proposes a new viewpoint for understanding how Earth's surface environments and microbial metabolisms have interacted, transformed and evolved together."