Viscoelasticity improves the collective movement of bacteria Summary Bacteria form the human and animal microbiota . They are the main causes of many infections and constitute an important class of active matter. Concentrated bacterial suspensions exhibit large-scale turbulent-type locomotion and swarming. While the collective behavior of bacteria in Newtonian fluids is relatively well understood, many fundamental questions remain open for complex fluids. Here, we report on collective bacterial movement in a representative non-Newtonian biological viscoelastic environment exemplified by mucus . The experiments are performed with synthetic porcine gastric mucus, natural cow cervical mucus, and a Newton-like polymer solution. We have found that an increase in mucin concentration and, correspondingly, an increase in suspension elasticity monotonically increases the length scale of collective bacterial locomotion. In contrast, this length remains virtually unchanged in a Newtonian polymer solution over a wide range of concentrations. Experimental observations are supported by computational models. Our results provide insight into how viscoelasticity affects the spatiotemporal organization of bacterial active matter. They also expand our understanding of bacterial colonization of mucosal surfaces and the emergence of antibiotic resistance due to swarming. |
Statement of importance
Mucus , a viscoelastic gel-like substance, is essential for many biological functions . Mucus coats the surfaces of cells and tissues. It is permeable to oxygen and nutrients and protects against pathogens such as bacteria, fungi and viruses. Understanding bacterial motility in mucus-like fluids provides insights into infections born from bacteria, including gastric and sexually transmitted diseases. This work demonstrates that mucus viscoelasticity improves bacterial organization, leading to the appearance of coherently moving bacterial groups. The results shed light on how viscoelasticity controls the spatiotemporal organization of bacterial communities and provide insights into how to control and prevent bacterial invasion of mucosal surfaces.
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New study shows thicker mucus boosts bacteria’s ability to self-organize into swarms to spread infections
Sniffles, sneezes and runny noses are hallmarks of cold and flu season, and that increased mucus is exactly what bacteria use to mount a coordinated attack on the immune system, according to a new study from Penn State researchers. The team found that the thicker the mucus, the better bacteria can proliferate. The findings could have implications for treatments that reduce the bacteria’s ability to spread.
The study, published in the journal PNAS Nexus , demonstrates how bacteria use mucus to improve their ability to self-organize and possibly cause infections. The experiments, performed with synthetic mucus from pig stomach, natural cow cervical mucus, and a water-soluble polymeric compound called polyvidone , revealed that bacteria coordinate movement better in thick mucus than in aqueous substances.
The findings provide information about how bacteria colonize mucus and mucosal surfaces, the researchers said. The findings also show how mucus enhances bacterial collective movement, or swarming, which can increase the antibiotic resistance of bacterial colonies.
"To our knowledge, our study is the first demonstration of bacteria collectively swimming in mucus," said Igor Aronson, Huck Chair Professor of Biomedical Engineering, Chemistry and Mathematics at Penn State and corresponding author of the paper. "We have shown that mucus, unlike liquids of similar consistency, improves collective behavior."
Mucus is essential for many biological functions, Aronson explained. It covers the surfaces of cells and tissues and protects against pathogens such as bacteria, fungi and viruses. But it is also the host material for bacterial infections, including gastric and sexually transmitted diseases. According to Aronson, a better understanding of how bacteria swarm in mucus could pave the way for new strategies to combat infections and the growing problem of antibiotic resistance.
"Our findings demonstrate how mucus consistency affects the random movement of individual bacteria and influences their transition to the coordinated collective movement of large bacterial groups," Aronson said. "There are studies that show that the collective movement or swarming of bacteria improves the ability of bacterial colonies to defend themselves from the effect of antibiotics. The appearance of the collective behavior studied in our work is directly related to swarming."
Mucus is a notoriously difficult substance to study because it exhibits both liquid and solid properties, Aronson explained. Liquids are generally described by their viscosity level, how thick or thin the liquid is, and solids are described by their elasticity, how much force may be required before breaking. Mucus, a viscoelastic fluid, behaves as both a liquid and a solid.
To better understand how mucus becomes infected, the team used microscopic imaging techniques to observe the collective movement of the concentrated bacteria Bacillus subtilis in synthetic mucus from the pig’s stomach and in the cow’s natural cervical mucus. They compared those results with observations of Bacillus subtilis moving in a water-soluble polyvidone polymer over a wide range of concentrations, from high to low polyvidone levels. The researchers also compared their experimental results with a computational model for bacterial collective movement in viscoelastic fluids such as mucus.
The team found that the consistency of mucus profoundly affects the collective behavior of bacteria. The results indicated that the thicker the mucus, the more likely the bacteria were to exhibit collective movement, forming a coordinated swarm.
"We were able to demonstrate how the viscoelasticity of mucus enhances bacterial organization, which in turn leads to bacterial groups that move coherently and cause infection," Aronson said. "Our results reveal that mucus elasticity and viscosity levels are an important factor in how bacterial communities are organized, which may provide information on how we can control and prevent bacterial invasion into mucus."
Aronson explained that the team expects human mucus to show similar physical properties, meaning their findings are also relevant to human health.
"The onset of the collective movement of bacteria and their interaction with mucus should be the same as in cow, pig or human mucus, since these substances have similar mechanical properties," Aronson said. "Our results have implications for human and animal health. We are demonstrating that the viscoelasticity of mucus can enhance the collective movement of bacteria on a large scale, which can accelerate how quickly bacteria penetrate the protective mucus barrier and infect the internal tissues".
