The detection of a mass of intertwined polysaccharides surrounding bacterial cells, termed a "glycocalyx," remains a seminal discovery in bacterial physiology, giving rise to the biofilm concept for surface-attached microbial community growth within a polysaccharide matrix (Costerton et al., 1978). Within a biofilm, bacteria can physically interact, be protected from external stressors (e.g., antibiotics, reactive oxygen species, dehydration, etc.), replicate, communicate via secreted signals, and differentiate their functions (O'Toole et al., 2000;Zhang et al., 2012). While the importance of secreted polysaccharides for biofilm formation is widely appreciated, the mechanisms by which these polymers promote 3D matrix structuration and the cellular organization within are areas of intense study (Limoli et al., 2015). One such bacterium that displays robust biofilm existence is Myxococcus xanthus, a predatory Gram-negative δ-proteobacterium with a social multicellular lifecycle (Monds & O'Toole, 2009;O'Toole et al., 2000;Van Gestel et al., 2015). Groups of M. xanthus cells are encased within a secreted polysaccharide matrix, promoting intimate contacts. On surfaces, swarms of these cells
This model could be used in the course of a Legionnaires' disease outbreak to provide early estimates of the total number of cases, thus helping to inform public-health planning. Toward the end of the outbreak, estimates of the release end date could help corroborate standard epidemiologic, environmental, and microbiologic investigations that seek to identify the source.
In nature, bacteria often live in surface-associated communities known as biofilms. Biofilm-forming bacteria typically deposit a layer of polysaccharide on the surfaces they inhabit; hence, polysaccharide is their immediate environment on many surfaces. In this study, we examined how the physical characteristics of polysaccharide substrates influence the behavior of the biofilm-forming bacterium Myxococcus xanthus. M. xanthus responds to the compression-induced deformation of polysaccharide substrates by preferentially spreading across the surface perpendicular to the axis of compression. Our results suggest that M. xanthus is not responding to the water that accumulates on the surface of the polysaccharide substrate after compression or to compression-induced changes in surface topography such as the formation of troughs. These directed surface movements do, however, consistently match the orientation of the long axes of aligned and tightly packed polysaccharide fibers in compressed substrates, as indicated by behavioral, birefringence and small angle X-ray scattering analyses. Therefore, we suggest that the directed movements are a response to the physical arrangement of the polymers in the substrate and refer to the directed movements as polymertropism. This behavior might be a common property of bacteria, as many biofilm-forming bacteria that are rod-shaped and motile on soft surfaces exhibit polymertropism.
Biofilm-forming bacteria typically deposit layers of polysaccharides on the surfaces they inhabit; hence, polysaccharides are their immediate environment on such surfaces. Previously, we showed that many biofilm-forming bacteria preferentially spread in the direction of aligned and densely packed polysaccharide fibers in compressed substrates, a behavior we referred to as polymertropism. This arrangement of polysaccharide fibers is likely to be similar to that found in the "slime" trails deposited by many biofilm-forming bacteria and would explain previous observations that bacteria tend to follow these trails of polysaccharides. Here, we show that groups of cells or flares spread more rapidly on substrates containing aligned and densely packed polysaccharide fibers. Flares also persist longer, tend to hold their trajectories parallel to the long axes of polysaccharide fibers longer, and ultimately show an increase in displacement away from their origin. On the basis of these findings and others, we propose a model for polymertropism. Namely, we suggest that the packing of the aligned polymers increases the efficiency of surface spreading in the direction of the polymer's long axes; therefore, bacteria tend to spread more rapidly in this direction. Additional work suggests that bacteria can leverage polymertropism, and presumably more efficient surface spreading, for a survival advantage. In particular, when two bacterial species were placed in close proximity and in competition with each other, the ability of one species to move rapidly and directly away from the other by utilizing the aligned polymers of compressed agar substrates led to a clear survival benefit. The directed movement of bacteria on compressed substrates was first described in the 1940s and referred to as elasticotaxis (R. Y. Stanier, J Bacteriol 44:405-412, 1942). More recently, this behavior was referred to as polymertropism, as it seems to be a response to the nematic alignment and tight packing of polymers in the substrate (D. J. Lemon, X. Yang, P. Srivastava, Y. Y. Luk, A. G. Garza, Sci Rep 7:7643, 2017, https://doi.org/10.1038/s41598-017-07486-0). The data presented here suggest that bacteria are more efficient at surface spreading when the polymers in the substrate are arranged in this manner. These data also suggest that bacteria can leverage polymertropism, and presumably more efficient surface spreading, for a survival advantage. Namely, one bacterial species was able to use its strong polymertropism response to escape from and survive competition with another species that normally outcompetes it.
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