Bacteria Flagella Utilize Evolutionary Foible
July 9, 2013

Bacteria Exploit Evolutionary Foible To Propel Themselves Through Water

redOrbit Staff & Wire Reports - Your Universe Online

Marine microbes change swimming directions with a sideways flick of their lone flagellum, a type of high-speed controlled failure first documented in 2011 as a unique swimming stroke but whose underlying mechanism had eluded researchers until now.

Bacteria swim by rotating the helical, hair-like flagella that extend from their unicellular bodies. Some bacteria, such as the Escherichia coli (E. coli) living in the human gut, have multiple flagella that rotate as a bundle to move the cell forward. These cells turn fairly acrobatically by unbundling their flagella, causing the cell to tumble, reorient and strike out in another direction.

However, many microbes, including 90 percent of mobile marine bacteria, have only a single rigid flagellum but are still able to swim both forward and backward by rotating this flagellum either counterclockwise or clockwise.

To investigate the mechanism behind these maneuvers, researchers from MIT used high-speed video to record individual swimming bacteria at up to 1,000 frames per second. They observed that the flick occurs when the so-called "hook," a tiny flexible rod connecting the flagellum to the cell's internal motor, buckles during forward swims.

The drag on the cell head caused by the water's resistance combines with the opposing thrust force from the rotating flagellum to compress the hook, causing it to buckle and flick the cell into a 90-degree reorientation, the researchers concluded in a paper published online July 7 in Nature Physics.

This ability to reorient by flicking is important, since it is what ultimately helps bacteria propel themselves toward food in the nutrient-sparse ocean. While this might seem like a cumbersome means of navigation, for marine bacteria whose flagellum spins at more than 1,000 revolutions per second creating 10-millisecond buckling, it makes perfect sense. This high-speed buckling allows the bacteria to swim at nearly 100 body lengths per second - the equivalent of a car traveling faster than the speed of sound.

The mechanism is of particular interest to engineers focused on preventing buckling to avoid structural failures.

"The bacteria have evolved to exploit this structural failure as a strategy," said lead author Roman Stocker, an associate professor in MIT's Department of Civil and Environmental Engineering, in an interview with MIT News.

"E. coli and other multiflagellated microbes have to synthesize and maintain all those flagella. But marine bacteria are able to achieve the same functionality with just one flagellum by turning physics on its head. It's controlled failure," said Stocker, whose research focuses on the ecology and biophysics of ocean microbes.

Understanding how marine microbes use controlled failure to change swimming direction is useful because these microorganisms are at the base of the ocean food chain, can cause red tides, destroy coral reefs or clean up oil spills. However, the current work may also have future applications in soft robotics or bioengineered systems for drug delivery.

"A single actuator, the flagellum, enables both propulsion and turning in these bacteria," said researcher Jeffrey Guasto, an MIT postdoc researcher.

"This is a well-known principle in robotics called 'underactuation,' but it is rarely considered at the micrometer scale."

Stocker attributes the insight that buckling is the mechanism behind the flick to the "engineering bias" of his team and their extensive knowledge of mechanics.

"When our high-speed imaging showed that flicks only occurred during forward motion, we intuited that this implied compression, and thus the potential for buckling," he said.

But the key to discovering the mechanism was in the high spatial and temporal resolution of the imaging technology, he added.

The researchers also studied the swimming patterns of the bacterium Vibrio alginolyticus by tracking individual cells. They observed that the microbe executes a sort of three-point turn consisting of a backward swim, a brief forward swim lasting only 10 milliseconds, and then the 90-degree flick to a new direction caused by the buckling of the hook. After the flick, when the bacteria swim at a steady speed, the hook then twists up and becomes stiffer, and flicking does not occur.

To test their hypothesis that compression was responsible for the flicking process, the researchers altered the concentration of sodium ions in the water. Because a sodium ion pump drives the cell's motor, decreasing the salt content slows the microbes, lowering the compressive forces on the hook and thus preventing the flick.

Altogether, they studied the trajectories of more than 17,000 bacteria, including a coral pathogen and a variety of microbes from the Atlantic Ocean. All displayed the same swimming pattern, leading the researchers to conclude the maneuver is a common means of reorientation for marine microbes.

"At first blush, one might think that a single polar flagellum is a more economical design than multiple flagella, especially since flagellar bundles are not very efficient," wrote Howard Berg, Professor of Physics and professor of molecular and cellular biology at Harvard University, in an analysis of the current work published in the same issue of Nature Physics.

"But most of the costs in this business are in the construction, not in the operation. Presumably, it's cheaper to place motors at random positions along the cell wall than it is to mount them on a specific platform at one pole. One benefit of the polar design might be enhanced swimming speeds; one cost, a more constrained search paradigm. Nature appears to have stumbled upon a solution to the latter problem: a flick triggered by a buckling instability."

"The buckling of the hook of these bacteria is one of the smallest examples in nature of structural failure turned into biological function, and it is a pervasive strategy in the ocean," wrote the study's first author Kwangmin Son, a graduate student at MIT.

"Above all, we have remained astonished throughout this project at the resourcefulness of these smallest of all organisms," Stocker adds.