Toxic gas use among microbes: Battle for iron in the oceans of the early Earth

On the early Earth, the atmosphere did not yet contain oxygen; nevertheless, the iron dissolved in the oceans was oxidized in gigantic quantities and deposited as rock, for example as banded iron ore in South Africa. Various bacteria excrete insoluble iron via their own metabolic reactions: Some, the phototrophic iron oxidizers, gain energy by oxidizing the iron with the help of sunlight, and others by converting the iron with nitrate as an oxidizing agent. An international research team including Casey Bryce from the University of Bristol and Dr. Verena Nikeleit and Andreas Kappler from the Department of Geomicrobiology at the University of Tübingen investigated who had the upper hand in the competition for the iron. The bacterial competitors also used toxic nitric oxide. The study was published in the journal Nature Geoscience.

Two to three billion years ago, the Earth’s atmosphere had a completely different composition than it does today. "Today, the iron present in the oceans at that time in its reduced form would have been quickly oxidized by the oxygen in the atmosphere to form rusty iron minerals," explains Andreas Kappler. Although there was no oxygen on early Earth, huge rock deposits of iron showed that microbes were already oxidizing it effectively at that time.

Experiments in the laboratory

"Before there was oxygen on Earth, phototrophic iron oxidizers formed the huge iron oxide deposits known today as banded iron ores," says Casey Bryce, head of the project, formerly at the University of Tübingen, now at the University of Bristol. "We wanted to know whether these bacteria were in competition with other iron oxidizers that used nitrate." This led to the questions of whether these competing microbes could actually coexist, and if so, which of them were primarily responsible for iron oxidation.

To better understand the situation on early Earth, we conducted laboratory experiments," says Verena Nikeleit from the University of Tübingen, who has since moved to the Norwegian research center NORCE. The research team used one bacterial strain of each of the different iron oxidizers and allowed them to grow under the conditions that prevailed two to three billion years ago, in the light and with the same concentrations of iron, nitrate and carbon dioxide. To our surprise, the nitrate was quickly used up and the iron was oxidized. But we could not detect any iron oxidation by the phototrophic iron oxidizers," says Nikeleit. The analyses showed that the nitrate-consuming iron oxidizers formed nitrogen monoxide as a toxic by-product. "This brought the activity of the phototrophic iron oxidizers to a complete standstill. In other words, these microbes killed the phototrophic iron oxidizers by producing a toxic gas."

Complex network of interactions

"One hypothesis is that the phototrophic iron oxidizers probably contributed very little to the formation of banded iron ores in later phases of the Earth’s history," says Andreas Kappler. This is because the activity of other microbes caused the Earth’s atmosphere to contain more and more oxygen - in a first major environmental pollution, so to speak. "This may also have reached some areas of the oceans, where nitrate was subsequently formed. Our results provide the first experimental evidence for the hypothesis that phototrophic iron oxidizers in areas of high productivity may have been exposed to toxic nitric oxide during this time. They must have moved further away from the nutrient-rich areas and were therefore able to deposit less iron."

Casey Bryce reports that, according to the research team’s calculations, iron oxidation by nitrate-reducing bacteria could have initially compensated for the reduced contribution of phototrophic iron oxidizers. "The initial competition between the different bacteria would therefore not immediately stop the formation of the banded iron formations," she says. Further measurements and investigations are needed to get a more precise picture of the processes. "Our study provides an insight into how the oxygen enrichment of the Earth’s atmosphere could have affected other nutrient cycles in the oceans. This illustrates the complex web of biogeochemical interactions that controlled life in the Earth’s early oceans."

Publication:

Verena Nikeleit, Adrian Mellage, Giorgio Bianchini, Lea Sauter, Steffen Buessecker, Stefanie Gotterbarm, Manuel Schad, Kurt Konhauser, Aubrey L. Zerkle, Patricia Sanchez-Baracaldo, Andreas Kappler, Casey Bryce: Inhibition of phototrophic iron oxidation by nitric oxide in ferruginous environments. Nature Geoscience, https://doi.org/10.1038/s41561’024 -01560-9

Andreas Kappler
University of Tübingen
Faculty of Mathematics and Natural Sciences
Geomicrobiology
7071 29-74992
andreas.kappler @uni-tuebingen.de

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