ABOVE: Stentor roeseli

Reproducing the results of a 100-year-old discredited study, a paper in Current Biology today (December 5) confirms that the pond-dwelling protozoa Stentor roeseli can make complex and predictable behavior modifications to escape harm.

“What [the paper] shows is that a single cell can have several different possible responses and then choose among them in a defined order,” says cell geometrist Wallace Marshall of the University of California, San Francisco, who was not involved in the study. “Jennings had reported this more than a century ago but nobody really believed it, so showing this result again using modern methods is really exciting in my opinion,” he continues. “I love the fact that they really took the old results very seriously.”

It’s fascinating . . . that a single cell that is not a neuron has everything you need to make a decision.

—Sindy Tang,...

S. roeseli, which lives in ponds and other still or slow-moving bodies of fresh water, is a trumpet-shape, unicellular organism large enough to be visible to the naked eye. It spends its time attached to submerged vegetation, feeding on bacteria and other small organisms and occasionally swimming.

In 1902, zoologist Herbert Jennings published a paper in which he described the changing behavior of S. roeseli in response to an unpleasant stimulus—the pipetting of carmine (a red dye made from powdered insect shells) into the creature’s general vicinity. According to the paper, S. roeseli’s first avoidance strategy is to bend away from the irritant. If that doesn’t work, the creature alters the direction in which its cilia beat to drive away the particles. Failing that, S. roeseli contracts its body to escape the assault. And, as a last resort, the creature detaches from the object to which it was adhered and swims away.

A 1967 paper, which failed to replicate Jennings’ findings, led to these earlier observations being largely forgotten.

Harvard University systems biologist Jeremy Gunawardena, became fascinated with Jennings’s discovery after learning about it in a lecture about a decade ago because it “suggests that individual cells can have more complex behavior than we typically think.” Then, he says, he became aggravated by the1967 paper that claimed the results were wrong. “It was one of the shoddiest studies I’d ever seen,” he says. The paper reported that in response to the carmine powder, the cells swim away, but “they used the wrong organism,” says Gunawardena—Stentor coeruleus. “So that really got my goat.” The sense of injustice motivated him and his colleagues to see if they could recapitulate Jennings’s old experiments.

The investigations immediately hit a roadblock when the team failed to elicit any response whatsoever from S. roeseli using carmine powder. “We almost gave up at that point,” says Gunawardena. Desperate to find anything that might produce a response, they tested a bunch of substances readily available in the lab and found that microscopic polystyrene beads “elicited reproducible avoidance behaviors”—indeed, all of the four behaviors that Jennings himself had noted. It’s not clear why the carmine didn’t work, but it’s possible the composition of the product may have changed since the early 1900s, the authors suggest.

While Jennings reported his observations as generalized descriptions of the organism, Gunawardena’s team took a statistical approach. They gathered data from almost 60 separate experiments in which one, two, or three organisms were subjected to between one and seven pulses of beads in solution. In the case of multiple pulses, each was given after the organism had resumed its resting state.

Computational analysis of the assembled data revealed that, as Jennings had seen, the behaviors tended to occur in a hierarchical order. However, this hierarchy was only observed at the population level. In any individual organism, the reversal of cilia direction, bending, or contraction could occur in any order. In the cases where an organism detached, however, a contraction was always the immediately preceding behavior.

Although its not yet clear how S. roeseli switches between behaviors, “now we’re pretty sure that [Jennings’s result] really is true. . . . It puts it into the realm where people could start to investigate it at a more mechanistic level,” says Marshall.

“It’s fantastic that they were able to repeat [the findings],” says mechanical and biological engineer Sindy Tang of Stanford University who was not involved in the study. “It’s fascinating . . . that a single cell that is not a neuron has everything you need to make a decision.”

“This paper nicely settles a debate between those [researchers] willing to accept that non-neuronal organisms are also capable of processing information and acting on that information, and those that stick to the idea that only neuronal organisms are capable of complex decision making,” Madeleine Beekman, an evolutionary ecologist at the University of Sydney who was not involved in the study, writes in an email to The Scientist. “Clearly there is a fundamental difference between brained and brainless organisms,” she continues, “[b]ut the point is that a brain did not come out of nothing. The brain is the result of selection pressure placed on organisms with the most basic form of information processing. Gunawardena and colleagues show that this basic ground work is already present in unicellular organisms.”

J.P. Dexter et al., “A complex hierarchy of avoidance behaviors in a single-cell eukaryote,” Curr Biol, doi:10.1016/j.cub.2019.10.059, 2019.

Ruth Williams is a freelance journalist based in Connecticut. Email her at ruth@wordsbyruth.com or find her on Twitter @rooph.

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