On January 15, 1919, just as Martin Clougherty was waking from a nap, a towering wall of syrup slammed into his bedroom and swept him into the middle of the street. Battered but conscious, he managed to stand in the chest-deep mire flowing past him and wipe great globs of gunk from his eyes. Here and there the splintered remains of his house drifted on a sea of thick, amber fluid. Heaving himself onto a raft of passing debris—his bed frame—he spied a hand just above the muck. He grabbed it and pulled, eventually lifting a gasping woman onto the raft: his sister, Teresa.
Less than 30 yards from the Cloughertys’ home, a rickety, five-story-high storage tank of molasses filled to near capacity had split open, releasing more than two million gallons of syrup onto the streets of Boston’s North End. A wave 25 feet high and 160 feet wide at its peak demolished buildings, crushed freight cars and tore the Engine 31 firehouse from its foundation. The second floor of the firehouse collapsed onto the first, trapping several firefighters and a stonecutter in a narrow crawl space. The burly men tried to tread molasses as they would water, but every kick required enormous effort. One firefighter drowned from exhaustion. Ultimately the disaster killed 21 people and injured 150 others, many of whom were engulfed by the ooze and could not escape without assistance, as Stephen Puleo describes in detail in his book Dark Tide (Beacon Press, 2003).
From a human perspective, a tidal wave of molasses is a freak scenario—something so bizarre that it is difficult to believe at first. For some of the most abundant life-forms on the planet, however, a quagmire of syrup is a moment-to-moment reality. Because they are so tiny, many bacteria, paramecia and other microorganisms spend their lives struggling through water as people would struggle in molasses. In fact, bacteria battle viscous forces millions of times greater than those unleashed on Boston in 1919.
To overcome this predicament, microorganisms have evolved sophisticated and wacky ways of moving all their own. Bacteria and other kinds of Lilliputian life do not simply swim—they push and pull, twitch and skitter, spin and corkscrew their way through fluids and across slimy surfaces. Most microbes depend on obvious appendages to get around, but certain minuscule critters have baffled scientists for decades by refusing to reveal their tricks. In recent years, with the help of increasingly powerful cameras and microscopes, biologists have solved some of these long-standing mysteries and uncovered an array of previously unknown adaptations. It turns out that even some closely studied microbial species travel in ways scientists never noticed before. New research has unveiled intricate protein motors concealed within bacterial cells, slime-thinning enzymes that modify a microorganism’s environment as it swims to make the journey easier and a bacterium that uses miniature grappling hooks to slingshot itself through fluid.
“If the world were suddenly covered in molasses today, people would have real problems,” says Jacinta Conrad, who studies bacteria and complex fluids at the University of Houston. “But bacteria reproduce quite quickly, and they are quite adaptable, which are some things that have given them the ability to conquer the world. If they don’t have the right appendages or tools to move through fluids, there’s a good chance some of their progeny will have them in the near future.”
A Sticky Situation
Bacteria immersed in water and people submerged in molasses are in more or less the same sticky situation. One can predict how easily a bacterium, person or any other living thing will move through a given fluid by calculating the relevant Reynolds number, which, in this case, takes into account the viscosity and density of the fluid and the velocity and size of the organism. The higher the Reynolds number, the more likely everything will go along swimmingly.
In most situations, human swimmers enjoy very high Reynolds numbers. The Reynolds number for an adult man in water, for example, is around one million. In contrast, many microscopic swimmers permanently inhabit a low-Reynolds-number world, as American physicist Edward Mills Purcell explained in his famous 1974 lecture “Life at Low Reynolds Number.” Some bacteria must combat Reynolds numbers of around 10−5. To illustrate this fact, Purcell compared a microbial swimmer to a person submerged in a swimming pool full of molasses. In such circumstances, the Reynolds number for an adult man plummets to around 130.
To make matters worse, a man immersed in molasses would not get anywhere with the kinds of symmetric swimming strokes that would propel him in water. Each repetitive stroke would only undo what was done before. Pulling his arm toward himself would move molasses away from his head, but reaching up to repeat the stroke would push the molasses back where it was before. He would stay in place, like a gnat trapped in tree sap. Likewise, bacteria and other microbes cannot use reciprocal movements to travel through any fluid, be it water in the ocean or a pond or the nutritious broth sloshing through the human gut. So they have evolved entirely different ways of swimming.
Microorganisms’ two most common solutions to the problems posed by low Reynolds numbers are cilia and flagella. Short, hairlike projections called cilia coat the surfaces of paramecia and other single-celled protozoans, which are distinct from bacteria. To move, paramecia constantly row their cilia like miniature oars, albeit in an unusual way. During the power stroke, the cilia are fully extended, creating a lot of drag; during the recovery stroke, however, the cilia flex and curl into little question marks, creating much less drag. Because of this difference in drag, the power stroke pushes the microorganisms forward more than the recovery stroke pulls them back—so they swim.
Many species of bacteria, such as the extensively studied Escherichia coli, propel themselves with helical, whiplike filaments of protein called flagella. Flagella look like long cilia but behave quite differently. Instead of rowing, a bacterial flagellum rotates, pushing the cell to which it is attached through a fluid somewhat like a corkscrew boring into a cork. When the flagellum turns counterclockwise, the bacterium moves forward in a straight line; quickly switching to clockwise rotation allows a microbe to tumble and change directions.
In a low-Reynolds-number world, inertia is practically meaningless. Whereas a human swimmer could take a few backstrokes, stop and still glide along for a while, some microorganisms must move ceaselessly through fluids if they are to get anywhere at all. If a bacterium stopped spinning its flagella, it would reach a complete standstill in a distance less than one tenth of the diameter of a hydrogen atom, according to calculations by Howard Berg of Harvard University, a pioneer of research on bacterial movement.
Microbial Mysteries
Since the 1970s biologists have learned much about microbes that rely on cilia and flagella. Other microbes, however, were not so easy to figure out: they moved without using cilia, flagella or any other obvious means of propulsion. In the past 10 years scientists have finally started to solve some of these mysteries of microbial locomotion, often with the help of keen imaging tools not previously available. “The past few decades have yielded one surprising finding after another of different ways bacteria have for getting around,” says Mark McBride, who studies bacteria at the University of Wisconsin–Milwaukee. “Some of the most surprising discoveries are very abundant bacteria that swim but don’t have any flagella.”
Fusilli-shaped bacteria in the genus Spiroplasma, for example, swim through the juices of the plants and insects they infect, although they have no swimming appendages of any kind. Joshua W. Shaevitz, now at Princeton University, and his colleagues think that Spiroplasma bacteria have evolved a rather kinky way of moving. Helical ribbons of protein inside the bacteria provide structural support. In 2005 Shaevitz and his colleagues took a close look at these ribbons with a sophisticated microscopy technique that splits and refocuses polarized light to enhance the contrast and detail of the image. Their observations revealed that tiny protein motors twist one segment of the ribbons in one direction and another segment in the opposite direction, creating a 111-degree kink where the two segments meet—similar to the way a phone cord tangles. These kinks rapidly and continuously travel from one end of the cell to another in waves, forming crooks in the cell body itself that push against surrounding fluids to move the bacterium forward.
Synechococcus, a group of pill-shaped photosynthetic ocean bacteria, continues to flummox scientists. Like Spiroplasma, the Synechococcus bacterium manages to swim even though it lacks an evident means of moving. In a 2012 paper George Oster of the University of California, Berkeley, and Kurt Ehlers of the Desert Research Institute–Reno in Nevada proposed the most plausible explanation to date. The pair found insight in recent research on an unrelated soil bacterium called Myxococcus xanthus. Scientists knew that M. xanthus sometimes glides along surfaces without using any external appendages, but they were not sure how.
In 2011 Oster’s Berkeley colleagues David Zusman and Beiyan Nan tagged proteins known to help M. xanthus move with fluorescent molecules that glow cherry red in ultraviolet light. With a powerful microscope, they observed blushing proteins of different sizes running along a loop of twisted protein fibers, creating lumps in the cell surface that essentially act like tank treads. Ehlers and Oster think Synechococcus relies on a similar system—but one that operates in a much higher gear. According to their mathematical model, if an analogous protein motor exists inside Synechococcus, “nothing in physics prevents” it from spinning fast enough to move the bacterium through water, Oster says.
Some bacteria have evolved ways to travel through fluids and gels thousands of times more viscous than water—a mind-boggling feat, considering that their size makes moving through water alone a huge challenge. Pseudomonas aeruginosa lives in soil, in water and on many man-made materials; it also thrives in the human body, infecting the blood, lungs and urinary tract in particular. In 2011 Conrad and her colleagues filmed P. aeruginosa moving through a viscous medium on a piece of glass, using cameras with much higher frame rates than those in earlier studies. The bacterium repeatedly extended and reabsorbed sticky, hairlike appendages called pili, using them like grappling hooks to pull itself forward—a well-known microbial move. The new film footage revealed a surprise, however: P. aeruginosa sometimes detached a single pilus while keeping others taut, slingshotting itself across the glass 20 times faster than usual.
Conrad and her colleagues think that the bacterium’s superspeedy skittering reduces the viscosity of the surrounding fluid through a process known as shear thinning. Non-Newtonian fluids, such as molasses, ketchup and the kind of slime P. aeruginosa often moves through, become less viscous when under pressure. Just as giving a Mrs. Butterworth’s bottle a squeeze gets the stagnant syrup it holds flowing, P. aeruginosa uses the recoil of its own body to thin out the sticky fluid around it.
The spiral-shaped Helicobacter pylori has evolved an even more impressive way to reduce viscosity. A bacterium that makes its home in the human stomach, the ulcer-inducing H. pylori faces two major challenges: first, it must survive the stomach’s caustic soup; second, it must cross a thick layer of mucus to reach the stomach’s epithelial cells, its preferred niche. To solve the first problem, H. pylori secretes the enzyme urease, which catalyzes a chemical reaction that turns urea in the stomach into ammonia and carbon dioxide, neutralizing hydrochloric acid. Biologists have always assumed that H. pylori relies on the power of its spinning flagella to bore its way through mucus. Yet when Jonathan Celli, now at the University of Massachusetts Boston, and his colleagues deprived H. pylori of urea in the laboratory in 2009, it could not move through imitation mucus. The same chemical reaction that neutralizes acid in the stomach, Celli’s research suggests, also changes the conformation of proteins in mucus, transforming it from a virtually solid gel into a more navigable fluid.
All around us—and inside us—infinitesimal creatures such as H. pylori reckon with daunting physical forces to which we are oblivious. A casual look at bacteria under the microscope, twirling like runaway carousels or zigzagging with apparent ease, does not reveal their struggle. To understand what it would be like to live and move as a microbe, we must immerse ourselves in a bizarre alternative reality—in a world where water is as thick as molasses. What Martin Clougherty experienced in 1919 is what many microorganisms endure every second of their brief, brutal lives. For a microbe, flapping a cilium or jitterbugging to move a fraction of a millimeter is not a trivial act—it is a monumental feat and a testament to eons of evolutionary grit.
Less than 30 yards from the Cloughertys’ home, a rickety, five-story-high storage tank of molasses filled to near capacity had split open, releasing more than two million gallons of syrup onto the streets of Boston’s North End. A wave 25 feet high and 160 feet wide at its peak demolished buildings, crushed freight cars and tore the Engine 31 firehouse from its foundation. The second floor of the firehouse collapsed onto the first, trapping several firefighters and a stonecutter in a narrow crawl space. The burly men tried to tread molasses as they would water, but every kick required enormous effort. One firefighter drowned from exhaustion. Ultimately the disaster killed 21 people and injured 150 others, many of whom were engulfed by the ooze and could not escape without assistance, as Stephen Puleo describes in detail in his book Dark Tide (Beacon Press, 2003).
From a human perspective, a tidal wave of molasses is a freak scenario—something so bizarre that it is difficult to believe at first. For some of the most abundant life-forms on the planet, however, a quagmire of syrup is a moment-to-moment reality. Because they are so tiny, many bacteria, paramecia and other microorganisms spend their lives struggling through water as people would struggle in molasses. In fact, bacteria battle viscous forces millions of times greater than those unleashed on Boston in 1919.
To overcome this predicament, microorganisms have evolved sophisticated and wacky ways of moving all their own. Bacteria and other kinds of Lilliputian life do not simply swim—they push and pull, twitch and skitter, spin and corkscrew their way through fluids and across slimy surfaces. Most microbes depend on obvious appendages to get around, but certain minuscule critters have baffled scientists for decades by refusing to reveal their tricks. In recent years, with the help of increasingly powerful cameras and microscopes, biologists have solved some of these long-standing mysteries and uncovered an array of previously unknown adaptations. It turns out that even some closely studied microbial species travel in ways scientists never noticed before. New research has unveiled intricate protein motors concealed within bacterial cells, slime-thinning enzymes that modify a microorganism’s environment as it swims to make the journey easier and a bacterium that uses miniature grappling hooks to slingshot itself through fluid.
“If the world were suddenly covered in molasses today, people would have real problems,” says Jacinta Conrad, who studies bacteria and complex fluids at the University of Houston. “But bacteria reproduce quite quickly, and they are quite adaptable, which are some things that have given them the ability to conquer the world. If they don’t have the right appendages or tools to move through fluids, there’s a good chance some of their progeny will have them in the near future.”
A Sticky Situation
Bacteria immersed in water and people submerged in molasses are in more or less the same sticky situation. One can predict how easily a bacterium, person or any other living thing will move through a given fluid by calculating the relevant Reynolds number, which, in this case, takes into account the viscosity and density of the fluid and the velocity and size of the organism. The higher the Reynolds number, the more likely everything will go along swimmingly.
In most situations, human swimmers enjoy very high Reynolds numbers. The Reynolds number for an adult man in water, for example, is around one million. In contrast, many microscopic swimmers permanently inhabit a low-Reynolds-number world, as American physicist Edward Mills Purcell explained in his famous 1974 lecture “Life at Low Reynolds Number.” Some bacteria must combat Reynolds numbers of around 10−5. To illustrate this fact, Purcell compared a microbial swimmer to a person submerged in a swimming pool full of molasses. In such circumstances, the Reynolds number for an adult man plummets to around 130.
To make matters worse, a man immersed in molasses would not get anywhere with the kinds of symmetric swimming strokes that would propel him in water. Each repetitive stroke would only undo what was done before. Pulling his arm toward himself would move molasses away from his head, but reaching up to repeat the stroke would push the molasses back where it was before. He would stay in place, like a gnat trapped in tree sap. Likewise, bacteria and other microbes cannot use reciprocal movements to travel through any fluid, be it water in the ocean or a pond or the nutritious broth sloshing through the human gut. So they have evolved entirely different ways of swimming.
Microorganisms’ two most common solutions to the problems posed by low Reynolds numbers are cilia and flagella. Short, hairlike projections called cilia coat the surfaces of paramecia and other single-celled protozoans, which are distinct from bacteria. To move, paramecia constantly row their cilia like miniature oars, albeit in an unusual way. During the power stroke, the cilia are fully extended, creating a lot of drag; during the recovery stroke, however, the cilia flex and curl into little question marks, creating much less drag. Because of this difference in drag, the power stroke pushes the microorganisms forward more than the recovery stroke pulls them back—so they swim.
Many species of bacteria, such as the extensively studied Escherichia coli, propel themselves with helical, whiplike filaments of protein called flagella. Flagella look like long cilia but behave quite differently. Instead of rowing, a bacterial flagellum rotates, pushing the cell to which it is attached through a fluid somewhat like a corkscrew boring into a cork. When the flagellum turns counterclockwise, the bacterium moves forward in a straight line; quickly switching to clockwise rotation allows a microbe to tumble and change directions.
In a low-Reynolds-number world, inertia is practically meaningless. Whereas a human swimmer could take a few backstrokes, stop and still glide along for a while, some microorganisms must move ceaselessly through fluids if they are to get anywhere at all. If a bacterium stopped spinning its flagella, it would reach a complete standstill in a distance less than one tenth of the diameter of a hydrogen atom, according to calculations by Howard Berg of Harvard University, a pioneer of research on bacterial movement.
Microbial Mysteries
Since the 1970s biologists have learned much about microbes that rely on cilia and flagella. Other microbes, however, were not so easy to figure out: they moved without using cilia, flagella or any other obvious means of propulsion. In the past 10 years scientists have finally started to solve some of these mysteries of microbial locomotion, often with the help of keen imaging tools not previously available. “The past few decades have yielded one surprising finding after another of different ways bacteria have for getting around,” says Mark McBride, who studies bacteria at the University of Wisconsin–Milwaukee. “Some of the most surprising discoveries are very abundant bacteria that swim but don’t have any flagella.”
Fusilli-shaped bacteria in the genus Spiroplasma, for example, swim through the juices of the plants and insects they infect, although they have no swimming appendages of any kind. Joshua W. Shaevitz, now at Princeton University, and his colleagues think that Spiroplasma bacteria have evolved a rather kinky way of moving. Helical ribbons of protein inside the bacteria provide structural support. In 2005 Shaevitz and his colleagues took a close look at these ribbons with a sophisticated microscopy technique that splits and refocuses polarized light to enhance the contrast and detail of the image. Their observations revealed that tiny protein motors twist one segment of the ribbons in one direction and another segment in the opposite direction, creating a 111-degree kink where the two segments meet—similar to the way a phone cord tangles. These kinks rapidly and continuously travel from one end of the cell to another in waves, forming crooks in the cell body itself that push against surrounding fluids to move the bacterium forward.
Synechococcus, a group of pill-shaped photosynthetic ocean bacteria, continues to flummox scientists. Like Spiroplasma, the Synechococcus bacterium manages to swim even though it lacks an evident means of moving. In a 2012 paper George Oster of the University of California, Berkeley, and Kurt Ehlers of the Desert Research Institute–Reno in Nevada proposed the most plausible explanation to date. The pair found insight in recent research on an unrelated soil bacterium called Myxococcus xanthus. Scientists knew that M. xanthus sometimes glides along surfaces without using any external appendages, but they were not sure how.
In 2011 Oster’s Berkeley colleagues David Zusman and Beiyan Nan tagged proteins known to help M. xanthus move with fluorescent molecules that glow cherry red in ultraviolet light. With a powerful microscope, they observed blushing proteins of different sizes running along a loop of twisted protein fibers, creating lumps in the cell surface that essentially act like tank treads. Ehlers and Oster think Synechococcus relies on a similar system—but one that operates in a much higher gear. According to their mathematical model, if an analogous protein motor exists inside Synechococcus, “nothing in physics prevents” it from spinning fast enough to move the bacterium through water, Oster says.
Some bacteria have evolved ways to travel through fluids and gels thousands of times more viscous than water—a mind-boggling feat, considering that their size makes moving through water alone a huge challenge. Pseudomonas aeruginosa lives in soil, in water and on many man-made materials; it also thrives in the human body, infecting the blood, lungs and urinary tract in particular. In 2011 Conrad and her colleagues filmed P. aeruginosa moving through a viscous medium on a piece of glass, using cameras with much higher frame rates than those in earlier studies. The bacterium repeatedly extended and reabsorbed sticky, hairlike appendages called pili, using them like grappling hooks to pull itself forward—a well-known microbial move. The new film footage revealed a surprise, however: P. aeruginosa sometimes detached a single pilus while keeping others taut, slingshotting itself across the glass 20 times faster than usual.
Conrad and her colleagues think that the bacterium’s superspeedy skittering reduces the viscosity of the surrounding fluid through a process known as shear thinning. Non-Newtonian fluids, such as molasses, ketchup and the kind of slime P. aeruginosa often moves through, become less viscous when under pressure. Just as giving a Mrs. Butterworth’s bottle a squeeze gets the stagnant syrup it holds flowing, P. aeruginosa uses the recoil of its own body to thin out the sticky fluid around it.
The spiral-shaped Helicobacter pylori has evolved an even more impressive way to reduce viscosity. A bacterium that makes its home in the human stomach, the ulcer-inducing H. pylori faces two major challenges: first, it must survive the stomach’s caustic soup; second, it must cross a thick layer of mucus to reach the stomach’s epithelial cells, its preferred niche. To solve the first problem, H. pylori secretes the enzyme urease, which catalyzes a chemical reaction that turns urea in the stomach into ammonia and carbon dioxide, neutralizing hydrochloric acid. Biologists have always assumed that H. pylori relies on the power of its spinning flagella to bore its way through mucus. Yet when Jonathan Celli, now at the University of Massachusetts Boston, and his colleagues deprived H. pylori of urea in the laboratory in 2009, it could not move through imitation mucus. The same chemical reaction that neutralizes acid in the stomach, Celli’s research suggests, also changes the conformation of proteins in mucus, transforming it from a virtually solid gel into a more navigable fluid.
All around us—and inside us—infinitesimal creatures such as H. pylori reckon with daunting physical forces to which we are oblivious. A casual look at bacteria under the microscope, twirling like runaway carousels or zigzagging with apparent ease, does not reveal their struggle. To understand what it would be like to live and move as a microbe, we must immerse ourselves in a bizarre alternative reality—in a world where water is as thick as molasses. What Martin Clougherty experienced in 1919 is what many microorganisms endure every second of their brief, brutal lives. For a microbe, flapping a cilium or jitterbugging to move a fraction of a millimeter is not a trivial act—it is a monumental feat and a testament to eons of evolutionary grit.
