Published online 30 June 2010 | Nature | doi:10.1038/news.2010.323

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Two-billion-year-old fossils could indicate steps towards multicellularity.

The colonial macrofossils found in Gabon. El Albani

Thumb-sized fossils discovered in Gabon, West Africa, were veritable behemoths 2.1 billion years ago. Palaeontologists reporting the finding in Nature say that the fossils represent ancient signs of multicellular life1.

Fossils of putative multicellular organisms, found in India, were nearly half a billion years younger2. And not until the Cambrian period, which began some 542 million years ago, were large, complex organisms commonplace.

"We have these macrofossils turning up in a world that was purely microbial," says Stefan Bengtson, a palaeozoologist at the Swedish Museum of Natural History in Stockholm and a co-author on the report. "That's a big deal because when you finally get big organisms, it changes the way the biosphere works, as they interact with microbes and each other."

Just as organisms change the biological and chemical make-up of their immediate environment, so the chemistry of the environment affects life too. Palaeontologists say that a rise in global atmospheric oxygen about 750 million years ago made the 'explosion' of multicellular animals in the Cambrian period possible. Similarly, the so-called Great Oxidation Event 2.4 billion years ago might have allowed the Gabon organisms to survive, Bengtson says.

"It's just remarkable how large the fossils they've found are," says Philip Donoghue of the University of Bristol, UK. "Normally, to find fossils from this time period you need to dissolve rocks and look under a microscope."

The 21-person team examined the fossils' structure and chemical content using micro-computed tomography and mass spectrometry, and concluded that the specimens were not rock formations but the remains of living organisms. They had flexible, fringed flaps surrounding their 7–120-millimetre-long bodies, and from this the authors infer that the organisms consisted of multiple cells.

Complex and communicative

According to the team, the organisms might have been colonial bacteria that signalled to one another and so were able to form complicated structures. Mats of bacteria bound with sediment existed for millions of years before the Gabon fossils. Yet the Gabon specimens look different.

Microtomography reconstruction of the outer (left) and inner (right) morphology of one of the macrofossils. El Albani - Masurier

"These aren't aggregations of bacteria binding sediment," says Donoghue. "They're three-dimensional, which suggests coordinated multicellularity at a time just after the Great Oxidation Event."

Evolutionary geneticist Iñaki Ruiz-Trillo at the University of Barcelona in Spain says that key genes for cell adhesion and cell-cell communication existed before multicellularity arose. A case in point, he says, is his team's finding that a species of Amastigomonas, single-celled flagellates belonging to an ancient lineage, possess cell-signalling genes3.

More than a dozen lineages appear to have independently made the unicellular-to-multicellular transition — animals, plants and fungi being the most widely known. The Gabon organisms might have been an earlier 'experiment' in multicellularity, says Bengtson.

Eukaryotic affinity

Classifying the Gabon fossils is a difficult matter because they don't resemble any fossil or living organism. "The only modern analog might be microbial colonies, but these tend to be quite small and flimsy, while these are large and thick and resilient," says Bengtson.

"It's quite possible they represent eukaryotes, which tend to make more resilient and larger structures." Eukaryotes, such as animals and algae, have cells with membrane-bound nuclei. But seeing those cells is impossible here.

The fossils carry traces of sterol compounds typically found in the cell walls of eukaryotes. Coupled with their size and complexity, this evidence supports a eukaryotic affinity, says the paper's lead author Abderrazak El Albani of the University of Poitiers in France.

However, sterols and other organic soluble molecules can migrate into older sediment from organisms buried at a later date. And if these were eukaryotes, they would be very much older than any known members, says Donoghue.

"Why go out on a limb and argue that [sterol] is indicative of eukaryotes?" he comments. "We should take the most pessimistic view."

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Bengtson anticipates debate about the report. "Early macrofossils are always a contentious subject," he says.

Calling the Gabon specimens "pseudo-fossils", palaeontologist Adolf Seilacher at Yale University in New Haven, Connecticut, instead interprets them as aggregations of the mineral pyrite that grew in different shapes depending on the changing state of the surrounding sediment. In 1998, Seilacher reported finding a fossil eukaryote 1.1 billion years old4. Referring to that find, he says: "I now firmly believe that my own so-called first animals were pseudo-fossils too."

As long as the fossil bed in Gabon isn't transformed into a quarry, El Albani says, he will be returning soon to dig up more dirt on these exquisitely preserved curiosities.