Ancient microbial life used arsenic to thrive in a world without oxygen

Billions of years ago, life on Earth was mostly just sticky mats of great microbes living in shallow water. Sometimes these microbial communities made carbonate minerals that were encrusted together over many years to become layered limestone rocks called stromatolites. They are the oldest evidence of life on Earth. But the fossils do not tell researchers the details of how they formed.

Today, most of life is supplemented with oxygen. But these microbial mats were in place for a billion years before oxygen was present in the atmosphere. So what does life use instead?

Our team of geologists, physicists, and biologists found hints in fossil stromatolites that arsenic was the chemical of choice for ancient photosynthesis and respiration. But modern versions of these microbial communities still live on Earth today. Maybe one of those uses arsenic and could provide evidence for our theory?

So we joined an expedition of Chilean and Argentine scientists to search for live stromatolites in the harsh conditions of the high Andes mountains. In a small creek deep in the Atacama Desert, we found a big surprise. The bottom of the channel was bright purple and made of microbial mats of stromatolite thriving in the complete absence of oxygen. Just as the clues we found in ancient fossils suggest, these mats use two different forms of arsenic to perform photosynthesis and respiration. Our discovery provides the strongest evidence yet of how the oldest life on Earth survived in the pre-oxygen world.

Modern organisms make oxygen during photosynthesis and use it for respiration, but other elements, such as arsenic, shown here as As, can also work. Christophe Dobraz, Anthony Bouton, Peter Fisher, CC BY-ND

Converting sunlight into energy

Over the past 2.4 billion years, photosynthetic organisms such as plants and cyanobacteria have used sunlight, water and carbon dioxide to produce oxygen and organic matter. By doing this, they convert the energy from the sun into energy for life. Other organisms breathe oxygen as they digest organic carbon, and gain energy for their breathing in the process.

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Microbes in the ancient world also captured energy from sunlight, but their primitive mechanisms could neither produce oxygen from water nor use oxygen for respiration. They needed another chemical to do this.

From a biochemical perspective, there are only a few potential candidates: iron, sulfur, hydrogen, or arsenic. The lack of evidence in the fossil record and trace amounts of some of these chemicals in the primordial soup indicate that iron, sulfur, and hydrogen were not likely candidates for the first form of photosynthesis. This leaves the arsenic.

In 2014, our team found the first evidence that stromatolites were produced by photosynthesis and respiration with the help of arsenic. We collected 2.72 billion year-old pieces of stromatolite from a pre-oxygen world by digging into ancient coral reefs in outback Australia. Then we took these samples to France and cut them into thin slices. By measuring the x-rays that emerged from these samples when bombarded them with photons, we made a map of the chemical elements in the sample. If there are two types of arsenic in the map, this is a sign that life has been using arsenic for photosynthesis and respiration. In the remnants of ancient life we ​​find plenty of both forms of arsenic, but not iron or sulfur.

This was baffling, but we wanted more evidence: a modern isotope to help prove our arsenic theory. No researcher has ever found a microbial mat community living in a place completely devoid of oxygen, but if we do find one, it could help explain how the first stromatolites formed when our planet’s oceans and atmosphere lacked oxygen.

Peter Fisher uses field equipment to measure the chemical composition of purple microbial mats.

Samples from microbial mats contain high levels of arsenic and lithium, but no oxygen. Dangelo Duran, CC BY-ND

Modern microbes, their ancient analogues

The Atacama Desert in Chile is the driest place on Earth, surrounded by volcanoes and exposed to extremely high UV rays. It’s not much different from what Earth looked like 3 billion years ago and it doesn’t fully support life as we know it. Here – with the help of a team that spanned across four continents and seven countries – we found what we were looking for.

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Or the destination is Laguna La Brava, a very salty shallow lake deep in the harsh desert. A shallow stream fed by a volcanic groundwater spring led to the lake. The riverbed was a unique deep purple. The color came from a microbial mat, which thrives quite happily in waters that contain unusually high amounts of arsenic, sulfur, and lithium, but lack one important element – oxygen.

Could these sticky purple blobs provide answers to an old question?

A purple and brown microbial cluster that sits on a white background.

A piece of microbial mat that lives at the bottom of the oxygen-free stream. Peter Fisher, CC BY-ND

We cut out a piece of the mat and looked for clues to the metal. A drop of acid made the minerals fizz – carbonate! – This microbial community was the stromatolite. So our team went to work, camping on site for several days at a time.

We measured the water and mat chemistry with our field equipment during the day, night, summer and winter. We didn’t find the oxygen once, and back in the lab we confirmed that the sulfur and arsenic were ample. Looking through a microscope, we saw purple photosynthetic bacteria, but the oxygen-producing cyanobacteria were eerily absent. We also collected DNA samples from the mat and found genes for arsenic metabolism.

In the lab, we mixed the microbes from the mat, added arsenic, and exposed the mixture to sunlight. Photosynthesis was happening. Microbes used arsenic and sulfur, but preferred arsenic. When we added a small amount of organic matter, a different arsenic compound was used for respiration and preferred over sulfur.

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All that remains is to show that the two types of arsenic can be detected in modern stromatolites. We got back to France, and using X-ray emission technology, we made chemical maps from Chilean samples. Every experiment we conducted supported a robust arsenic cycle in the absence of oxygen in this unique modern stromatolite. This confirms, without a doubt, the idea that the fossil Australian samples we studied in 2014 bear evidence of an active arsenic cycle in deep time on our young planet.

The large Laguna La Brava lake with active volcanoes behind at sunset.

Laguna La Brava is closer to the Martian environment than most places on Earth. Peter Fisher, CC BY-ND

Answers are on Earth, leading to Mars

The extreme conditions of Atacama are so similar to the environments of early Mars and Earth that NASA scientists and astrobiologists are turning to the Atacama to answer questions about how life began on our planet, and how it might start elsewhere. The arsenic cycling mats we discovered at Laguna La Brava provide solid clues to some basic questions about life.

On board the Mars 2020 Perseverance rover currently propelling through space is a tool that can observe objects using the same process we used to create our object maps. Perhaps he will discover that arsenic is abundant in layered rocks on Mars, indicating that life on Mars also uses arsenic. For more than a billion years, it did so on Earth. Under the harshest circumstances life finds a way, and in this way we try to understand.

Peter Fisher, Professor of Marine Sciences, University of Connecticut; Brendan Paul Burns, Senior Lecturer, UNSWKimberley L. Gallagher, Assistant Professor of Chemistry, Quinnipiac University

This article is republished from The Conversation under a Creative Commons license. Read the original article.


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