Life emerged on Earth some 3.8 billion years ago. The "primordial soup theory" proposes that chemicals floating in pools of water, in the presence of sunlight and electrical discharge, spontaneously formed organic molecules. These building blocks of life underwent chemical reactions, likely driven by RNA, eventually leading to the formation of single cells.
But what sparked single cells to assemble into more complex, multicellular life forms?
Nature Physics published a new insight about a possible driver of this key step in evolution — the fluid dynamics of cooperative feeding.
"So much work on the origins of multicellular life focuses on chemistry," says Shashank Shekhar, lead author of the study and assistant professor of physics at Emory University. "We wanted to investigate the role of physical forces in the process."
Shekhar got the idea while watching the filter feeding of stentors — trumpet-shaped, single-celled giants that float near the surface of ponds.
Through microscope video, he captured the fluid dynamics of a stentor in a liquid-filled lab dish as the organism sucked in particles suspended in the liquid. He also recorded the fluid dynamics of pairs and groups of stentors clumped together and feeding.
"The project started with beautiful images of the fluid flows," Shekhar says. "Only later did we realize the evolutionary significance of this behavior."
Shekhar and his colleagues discovered that grouping together benefits a stentor colony as a whole by generating more powerful flows to sweep in more food from a greater distance away.
The stentor's multicellular-like behavior could be used as a model system to help understand how life evolved from single-cell organisms to complex organisms like humans — made up of trillions of cells with specialized tasks.
Co-corresponding authors of the paper are John Costello, a marine biologist at Providence College in Rhode Island and Eva Kenso, a mathematician in the Department of Aeorospace and Mechanical Engineering at the University of South California, Los Angeles.
The project began in 2014 when Shekhar participated in the physiology program at the Marine Biological Laboratory (MBL) in Woods Hole, Massachusetts, an international center for research and education in biological sciences. Shekhar has since held a visiting position at MBL
"Renowned scientists come there every summer from around the world for organic collaborations," Shekhar says of the MBL. "You have the time and resources to explore extreme questions that capture your interest."
Shekhar drew particular inspiration from three scientists who became his co-authors on the Nature Physics paper. Costello and Sean Colin (a marine biologist from Roger Williams University) study the biomechanics of marine creatures like jellyfish and zooplankton. Wallace Marshall (a cell biologist from the University of California, San Francisco) uses the stentor as a model organism to explore phenomenon like regeneration — for example, the ability of an octopus to regrow a leg.
"You can chop up a stentor and each tiny piece will become a complete organism within 12 hours," Shekhar says. "They are fascinating in many ways."
These single-celled eukaryotes, common in freshwater ponds and streams, are named after the mythological Greek herald Stentor, due to their horn shape.
At the narrow end of the stentor is a gripping mechanism known as a "holdfast" which allows the organism to anchor to a twig, leaf or other organic matter floating in water. The wide end of the stentor is essentially a giant mouth rimmed with hair-like cilia. The cilia beat in the water, generating currents that drive food particles, such as bacteria or algae, into its mouth.
Stentors can secrete a kind of goo from their holdfast end. This goo enables them to stick to organic surfaces and temporarily form into colonies that take on a half-hemisphere shape.
Perhaps the most remarkable thing about stentors is their size. Most human cells are at least 10 times smaller than the width of a human hair. A single-celled stentor, however, is visible to the human eye at about 1-to-2 millimeters long — the widths of the tip of a sharpened pencil or crayon.
The size of stentors makes it easy to record detailed imagery of their behaviors under a microscope.
Shekhar decided to investigate the fluid dynamics involved in the filter feeding of stentors. He first focused on a single stentor, from the species Stentor coeruleus, attached to the surface of a fluid-filled lab dish.
"I added micron-sized plastic spheres to the liquid to see what would happen," he says.
The tiny, plastic particles served as tracers, making the flows generated by the stentor's cilia visible. Shekhar captured striking time-lapsed video of twin vortices forming around the mouth of the stentor.
Shekhar wondered if the behavior of stentors to occasionally form pairs or colonies was related to their quest for food.
To test the idea, he videoed the fluid dynamics of pairs of stentors. Their heads swayed towards and away from one another. "I call that movement 'I love you, I love you not,'" Shekhar says.
As their heads drew together, the flows generated by the two stentors combined into a single vortex that created a stronger current, able to draw in more particles from a greater distance.
Shekhar wondered why the stentors would move their heads apart since having them together seemed to provide a clear benefit.
A similar behavior was observed in colonies of stentors joined into half-hemisphere-shapes. In this configuration, their heads swayed between an array of adjacent partners and generated flows more powerful than the those of pairs.
Forming colonies seemed to further enhance their ability to suck in particles. So why did individual stentors occasionally break away from a group to swim off on their own?
The researchers theorized that weaker stentors benefitted more from joining forces than the stronger ones.
"The colonies are dynamic as the stentors keep changing partners," he explains. "The stronger ones are being taken advantage of, in a sense. They change partners often so that everyone benefits similarly."
The researchers developed mathematical models to test this theory in experimental setups through the expertise of Kanso and co-author Haniliang Guo, a mathematician at Ohio Wesleyan University, Delaware.
The results showed that one stentor always gained more advantage than the other in a paired system. And that forming a large colony, including the dynamic relocation of individuals, enhances the feeding flow rate for individual stentors on average.
The findings provide new insight into the selective forces that may have favored the early evolution of multiceullar organization.
"It's amazing that a single-celled organism, with no brain or neurons, developed behaviors for opportunism and cooperation," Shekhar says. "Perhaps these kinds of behaviors were hard-wired into organisms much earlier in evolution than we previously realized."
The stentor project is a new research direction for Shekhar. His lab is known for uncovering insights into actin — a protein that assembles into filaments in living cells and is essential to their mobility.
"The stentor work was a passion project," Shekhar says. "It's wonderful to work at your own pace, over many years, on a question that fascinates you and wind up with such beautiful and significant results."
