Even the oldest eukaryotic fossils display dazzling diversity and complexity

The sun has just set on a quiet mudflat in Australia’s Northern Territory; he will return in 7 hours. A young moon dominates the desolate landscape. No animals scurry into the fading light. No leaves rustle in the breeze. No lichen encrusted the exposed rock. The only sign of life is a little foam in some puddles and ponds. And among them lives a diverse microbial community of our ancient ancestors.

In a new account of superbly preserved microfossils, researchers from UC Santa Barbara and McGill University reveal that eukaryotic organisms had already evolved into a wide range of forms as early as 1.64 billion years ago. The article, published in the journal Paleontology articles, recounts an assemblage of eukaryotic fossils from an early era in the group’s evolutionary history. The authors describe four new taxa, as well as evidence for several advanced features already present in these early eukaryotes.

“These are among the oldest eukaryotes ever discovered,” explained lead author Leigh Anne Riedman, an assistant research scientist in UCSB’s Department of Earth Sciences. “Yet even in these early records we see a lot of diversity.”

Eukarya constitutes one of the major domains of life, encompassing clades of plants, animals, and fungi, as well as all other groups whose cells have a membrane-bound nucleus, such as protists and algae. Many scientists believed that the first eukaryotes were all quite similar in the late Paleoproterozoic and that diversification took place around 800 million years ago. But Riedman and his co-authors found fossils of a delightfully diverse and complex group of characters in a rock almost twice as old.

Scientists knew from previous studies that eukaryotes evolved around this time, but their diversity at this time was poorly understood. So Riedman went into the hinterland in late 2019. In one week, she had collected about 430 samples from eight cores drilled by a prospecting company; they now reside in the Northern Territory Geological Survey library. The two cores used for this study covered approximately 500 meters of stratigraphy, or 133 million years, with approximately 15 million years of significant deposits.

Riedman returned to the United States with shale and mudstone, remnants of an ancient coastal ecosystem that alternated between shallow subtidal mudflats and coastal lagoons. A bath of hydrofluoric acid dissolved the matrix rock, concentrating the precious microfossils which she then analyzed under a microscope.

“We were hoping to find species with interesting and different features of their cell walls,” Riedman said. She hoped these features could shed light on what was happening in cells during this time. However, reaching conclusions about the interior of cells would require a lot of research, because fossils only preserve the exterior of cells.

Researchers were surprised by the diversity and complexity preserved in these fossils. They recorded 26 taxa, including 10 previously undescribed species. The team found indirect evidence of cytoskeletons, as well as plaque-like structures suggesting the presence of internal vesicles in which the plaques formed, perhaps ancestral to Golgi bodies, present in modern eukaryotic cells. Other microbes had cell walls made of linked fibers, which also suggests the presence of a complex cytoskeleton.

The authors also discovered cells with a tiny trapdoor, evidence of a certain level of sophistication. Some microbes can form a cyst while waiting for adverse environmental conditions to pass. To emerge, they must be able to carve an opening in their protective shell. Making this door is a specialized process.

“If you want to produce an enzyme that dissolves your cell wall, you have to be very careful about how you use that enzyme,” Riedman said. “So in one of the earliest records of eukaryotes, we see some pretty impressive levels of complexity.”

Many people in the field thought this ability arose later, and the evidence for this assembly further highlights how diverse and advanced eukaryotes were, even at this early stage. “The assumption has always been that this was around the time eukaryotes appeared. And now we think people just didn’t explore older rocks,” said the co- author Susannah Porter, professor of earth sciences at UC Santa Barbara.

This article is part of a larger project investigating the early evolution of eukaryotes. Riedman and Porter want to know what environments early eukaryotes diversified into, why they were there, when they migrated to other places, and what adaptations they needed to occupy these new niches.

Much of this effort involves understanding when different features of eukaryotes first appeared. For example, the authors want to know whether these organisms were adapted to oxygenated or anoxic environments. The former would suggest that they had aerobic metabolism, and possibly mitochondria. Every modern eukaryote discovered is descended from ancestors with mitochondria. This suggests that eukaryotes acquired the organelle very early and that this gave them a significant advantage.

Riedman and Porter are currently working on a new description of the diversity of eukaryotes through time. They also collected even older samples in Western Australia and Minnesota. Meanwhile, their geochemistry collaborators at McGill are conducting a study on the oxygen levels and preferred habitats of eukaryotes, aspects that could shed light on their evolution.

“These results inspire us to look for older material, older eukaryotes, because this is clearly not the beginning of eukaryotes on Earth,” Riedman said.