The filamentous remnants of microbes in ancient microbial mats are evidence that photosynthesis was happening 3.3 billion years ago. Credit: Frances Westall

The most direct evidence yet for ancient photosynthesis has been uncovered in a fossil of a matted carpet of microbes that lived on a beach 3.3 billion years ago.

Frances Westall at the Centre for Molecular Biophysics, a laboratory of the French National Centre for Scientific Research (CNRS), in Orleans and her colleagues looked at the well-preserved Josefsdal Chert microbial mat — a thin sheet formed by layer upon layer of tiny organisms — from the Barberton Greenstone Belt in South Africa.

These layers of ancient microorganisms grew at a time when Earth's atmosphere did not contain oxygen. The mat would have lain on a beach in a place that sunlight could reach, but there would have been few carbon-rich nutrients around at that time. So early life would have relied on photosynthesis for nourishment, and working out when this process evolved is fundamental to understanding how life began.

Photosynthetic filaments

Westall and her team used electron microscopes and a synchrotron light source to look at the structure and composition of the preserved microbial mat. In the mat's surface layer they saw tiny filaments, about 0.3 micrometres long: remnants of photosynthetic microbes, Westall says. Beneath the surface they found small particles of aragonite, a calcium carbonate mineral. This could only have come to be there if the surface was photosynthesizing: taking energy from the Sun and turning it into useful nutrients for other microbes to feed on. "We've never before seen in situ calcification," Westall says. "There is no other way [besides photosynthesis] of producing this structure in this environment."

Westall says that as the mat grew, layers of dead photosynthetic microbes underneath the active top layer were consumed by non-photosynthetic organisms called heterotrophs lower down in the mat. As the heterotrophs degraded the carbon-rich layers produced by photosynthesis, she says, they excreted metabolites that caused the pH in the mat to rise. The higher pH released calcium ions taken up from the water by carbonaceous polymers that form part of the mat. The calcium mixed with carbonates from the seawater and precipitated as calcium carbonate.

Modern photosynthetic mats contain sulphur-reducing bacteria that also precipitate calcium carbonates. Westall spotted a sulphur-containing molecule, thiophene, in her sample, and was able to quantify the total amount of sulphur present — up to 1%. This, she says, suggests that the heterotrophs in the ancient mat included sulphur-reducing bacteria similar to those in modern mats.

"One of many mysteries about the early fossil record is the lack of calcified examples of microbial filaments, which are usually found in shallow marine contexts consistent with photosynthesis," says Martin Brasier, an expert on ancient biological processes at the University of Oxford, UK. Brasier is cautious about the results, saying he would like to see independent confirmation of the work.

Another view

Other ancient mats have been studied, but Westall says evidence that they photosynthesized has been indirect — either being assumed from their carbon-isotope composition, which Westall argues can also come from non-photosynthetic microbes, or by looking closely at the mat's structure and seeing microbe-like structures.

One such study, by Michael Tice, now at Texas A&M University in College Station, suggested that a 3.4-billion-year-old mat was photosynthetic1. In an e-mail to Nature, Tice says that his arguments in that work were more compelling than Westall suggests. "A key component to our arguments for photosynthesis was the observation that these mats were formed in shallow sunlit environments but not in deep-water environments recorded in the same geologic unit," he says. When combined with what they concluded about the fluids the mats grew in and their bulk isotopic compositions, Tice and his colleagues decided that "they could only have been produced by anoxygenic photosynthetic micro organisms".

Tice says that the calcification is important new evidence, but he doesn't think it is definitive. "They add to a body of indirect evidence suggesting that photosynthesis had evolved by the end of the Palaeoarchean, but we are still not in possession of a smoking gun," Tice says.

Westall presented her group's findings at the Origins2011 conference in Montpellier, France.