- Open Access
Rheologically tuned diffusion modulates quorum sensing in Vibrio fischeri
APS Open Sci. 1, 000188 – Published 27 October, 2026
DOI: https://doi.org/10.1103/z4r6-49vn
Abstract
Understanding how the physical properties of a fluid influence bacterial behavior is essential for explaining how microorganisms interact with their environment and with animal hosts. Here, we examine how changes in fluid viscosity and rheological properties affect the locomotion of the marine bacterium Vibrio fischeri and its ability to produce luminescence through cell-cell communication. We track the three-dimensional motion of single cells in well-defined fluids with different physical properties and measure the luminescence emitted by cell populations. We find that fluids with higher viscosity cause V. fischeri to spend more time in a slower, turning-focused swimming mode, which reduces how effectively cells spread out and encounter the chemical signals required to activate luminescence. As a result, luminescence first increases and then decreases in Newtonian fluids, but decreases monotonically in fluids that exhibit non-Newtonian rheological behavior. Computer simulations based on our measurements confirm that the ability of cells to explore their surroundings plays a central role in determining when and how strongly they communicate. These findings reveal a direct link between the physical environment, bacterial movement, and collective behavior, and offer insight into how microorganisms adapt to complex fluid habitats, including those found inside animal hosts.
Physics Subject Headings (PhySH)
Article Text
Supplemental Material
References (52)
- K. V. S. Chaithanya and S. P. Thampi, Viscoelastic effects on the hydrodynamics of an active compound particle, Eur. J. Mech. - B/Fluids 114, 204324 (2025).
- G. J. Elfring and E. Lauga, Theory of locomotion through complex fluids, Complex Fluids in Biological Systems: Experiment, Theory, and Computation, edited by S. Spagnolie, Biological and Medical Physics, Biomedical Engineering (Springer, New York, NY, 2015), pp. 283–317.
- E. Lauga, Bacterial hydrodynamics, Annu. Rev. Fluid Mech. 48, 105 (2016).
- Y. Quan, Y. Quan, M. Zhang, Z. Yu, J. Lin, Y. Xia, and Z. Lin, The locomotion of microorganisms in viscoelastic fluids at finite Reynolds numbers, J. Fluid Mech. 1020, A57 (2025).
- V. Wong et al., Fluid flow structures gut microbiota biofilm communities by advective transport of molecules, Proc. Natl. Acad. Sci. USA 120, e2217577120, (2023).
- J. J. Winkle, S. Saha, J. Essman, M. R. Bennett, W. Ott, K. Josić, and A. Mugler, Signaling in microbial communities with open boundaries, Biophys. J. 122, 2808 (2023).
- D. Scheidweiler, A. D. Bordoloi, W. Jiao, V. Sentchilo, M. Bollani, A. Chhun, P. Engel, and P. de Anna, Spatial structure, chemotaxis and quorum sensing shape bacterial biomass accumulation in complex porous media, Nat. Commun. 15, 191 (2024).
- D. M. Cornforth, R. Popat, L. McNally, J. Gurney, T. C. Scott-Phillips, A. Ivens, S. P. Diggle, and S. P. Brown, Combinatorial quorum sensing allows bacteria to resolve their social and physical environment, Proc. Natl. Acad. Sci. USA 111, 4280 (2014).
- M. Boyer and F. Wisniewski-Dyè, Cell–cell signalling in bacteria: Not simply a matter of quorum, FEMS Microbiol. Ecol. 70, 1 (2009).
- L. Gram, H.-P. Grossart, A. Schlingloff, and T. Kiørboe, Possible quorum sensing in marine snow bacteria: production of acylated homoserine lactones by roseobacter strains isolated from marine snow, Appl. Environ. Microbiol. 68, 4111 (2002).
- H. Dang and C. R. Lovell, Microbial surface colonization and biofilm development in marine environments, Microbiol. Mol. Biol. Rev. 80, 91 (2016).
- S. K. Lai, Y.-Y. Wang, D. Wirtz, and J. Hanes, Micro- and macrorheology of mucus, Adv. Drug Delivery Rev. 61, 86 (2009).
- M. M. Mrokowska, A. Krztoń-Maziopa, and M. Dȩbowski, Effect of exopolymer gels on the viscoelasticity of mucus-rich saltwater and settling dynamics of particles, Mar. Chem. 246, 104163 (2022).
- U. Passow, R. F Shipe, A. Murray, D. K Pak, M. A Brzezinski, and A. L Alldredge, The origin of transparent exopolymer particles (TEP) and their role in the sedimentation of particulate matter, Cont. Shelf Res. 21, 327 (2001).
- R. Bansil and B. S. Turner, The biology of mucus: Composition, synthesis and organization, Adv. Drug Deliv. Rev. 124, 3 (2018).
- S. V. Nyholm, E. V. Stabb, E. G. Ruby, and M. J. McFall-Ngai, Establishment of an animal–bacterial association: Recruiting symbiotic vibrios from the environment, Proc. Natl. Acad. Sci. USA 97, 10231 (2000).
- J. C. Nawroth, H. Guo, E. Koch, E. A. C. Heath-Heckman, J. C. Hermanson, E. G. Ruby, J. O. Dabiri, E. Kanso, and M. J. McFall-Ngai, Motile cilia create fluid-mechanical microhabitats for the active recruitment of the host microbiome, Proc. Natl. Acad. Sci. USA 114, 9510 (2017).
- S. V. Nyholm and M. J. McFall-Ngai, Dominance of Vibrio fischeri in secreted mucus outside the light organ of Euprymna scolopes: The first site of symbiont specificity, Appl. Environ. Microbiol. 69, 3932 (2003).
- S. V. Nyholm and M. J. McFall-Ngai, A lasting symbiosis: How the Hawaiian bobtail squid finds and keeps its bioluminescent bacterial partner, Nat. Rev. Microbiol. 19, 666 (2021).
- K. A. Gundlach, J. Nawroth, E. Kanso, F. Nasrin, E. G. Ruby, and M. McFall-Ngai, Ciliated epithelia are key elements in the recruitment of bacterial partners in the squid-vibrio symbiosis, Front. Cell Dev. Biol. 10, 974213 (2022).
- A. Chavez-Dozal, D. A. Hogan, C. Gorman, A. Quintanal-Villalonga, and M. K. Nishiguchi, Multiple Vibrio fischeri genes are involved in biofilm formation and host colonization, FEMS Microbiol. Ecol. 81, 562 (2012).
- See Supplemental Material at http://link.aps.org/supplemental/10.1103/z4r6-49vn for detailed experimental results and the resistive force theory, which includes Refs. [28, 34, 44, 48, 49, 50, 51, 52].
- J. Engebrecht and M. Silverman, Identification of genes and gene products necessary for bacterial bioluminescence, Proc. Natl. Acad. Sci. USA 81, 4154 (1984).
- C. Fuqua, S. C. Winans, and E. P. Greenberg, Census and consensus in bacterial ecosystems: The LuxR-LuxI family of quorum-sensing transcriptional regulators, Annu. Rev. Microbiol. 50, 727 (1996).
- B. Qin, A. Gopinath, J. Yang, J. P. Gollub, and P. E. Arratia, Flagellar kinematics and swimming of algal cells in viscoelastic fluids, Sci. Rep. 5, 9190 (2015).
- J. B. Keller, Effect of viscosity on swimming velocity of bacteria, Proc. Natl. Acad. Sci. USA 71, 3253 (1974).
- E. Lauga and T. R. Powers, The hydrodynamics of swimming microorganisms, Rep. Prog. Phys. 72, 096601 (2009).
- Z. Qu, F. Z. Temel, R. Henderikx, and K. S. Breuer, Changes in the flagellar bundling time account for variations in swimming behavior of flagellated bacteria in viscous media, Proc. Natl. Acad. Sci. USA 115, 1707 (2018).
- Z. Qu and K. S. Breuer, Effects of shear-thinning viscosity and viscoelastic stresses on flagellated bacteria motility, Phys. Rev. Fluids 5, 073103 (2020).
- A. E. Patteson, A. Gopinath, M. Goulian, and P. E. Arratia, Running and tumbling with E. coli in polymeric solutions, Sci. Rep. 5, 15761 (2015).
- A. Zöttl and J. M. Yeomans, Enhanced bacterial swimming speeds in macromolecular polymer solutions, Nat. Phys. 15, 554 (2019).
- X. Y. Zhuang, C. K. Tseng, and C. J. Lo, Viscosity-dependent swimming patterns assist for symbiont partner finding, Phys. Rev. Res. 6, 033214 (2024).
- J. B. Lynch, N. James, M. McFall-Ngai, E. G. Ruby, S. Shin, and D. Takagi, Transitioning to confined spaces impacts bacterial swimming and escape response, Biophys. J. 121, 2653 (2022).
- Y. Kinosita, Y. Kikuchi, N. Mikami, D. Nakane, and T. Nishizaka, Unforeseen swimming and gliding mode of an insect gut symbiont, Burkholderia sp. RPE64, with wrapping of the flagella around its cell body, ISME J. 12, 838 (2018).
- R. Stocker, J. R. Seymour, A. Samadani, D. E. Hunt, and M. F. Polz, Rapid chemotactic response enables marine bacteria to exploit ephemeral microscale nutrient patches, Proc. Natl. Acad. Sci. USA 105, 4209 (2008).
- M. Tian, Z. Wu, R. Zhang, and J. Yuan, A new mode of swimming in singly flagellated Pseudomonas aeruginosa, Proc. Natl. Acad. Sci. USA 119, e2120508119 (2022).
- A. Villa-Torrealba, C. Chávez-Raby, P. de Castro, and R. Soto, Run-and-tumble bacteria slowly approaching the diffusive regime, Phys. Rev. E 101, 062607 (2020).
- G. Guccione, D. Pimponi, P. Gualtieri, and M. Chinappi, Diffusivity of E. coli-like microswimmers in confined geometries: The role of the tumbling rate, Phys. Rev. E 96, 042603 (2017).
- J. C. Makemson, Luciferase-dependent oxygen consumption by bioluminescent vibrios, J. Bacteriol. 165, 461 (1986).
- J.-J. Bourgois, F. E. Sluse, F. Baguet, and Jérôme Mallefet, Kinetics of light emission and oxygen consumption by bioluminescent bacteria, J. Bioenerg. Biomembr. 33, 353 (2001).
- A. L. Schaefer, B. L. Hanzelka, A. Eberhard, and E. P. Greenberg, Quorum sensing in Vibrio fischeri: Probing autoinducer-LuxR interactions with autoinducer analogs, J. Bacteriol. 178, 2897 (1996).
- C. Lupp and E. G. Ruby, Vibrio fischeri uses two quorum-sensing systems for the regulation of early and late colonization factors, J. Bacteriol. 187, 3620 (2005).
- A. Jepson, V. A. Martinez, J. Schwarz-Linek, A. Morozov, and W. C. K. Poon, Enhanced diffusion of nonswimmers in a three-dimensional bath of motile bacteria, Phys. Rev. E 88, 041002(R) (2013).
- J. Taktikos, H. Stark, and V. Zaburdaev, How the motility pattern of bacteria affects their dispersal and chemotaxis, PLoS One 8, e81936 (2013).
- D. S. Millikan and E. G. Ruby, Alterations in Vibrio fischeri motility correlate with a delay in symbiosis initiation and are associated with additional symbiotic colonization defects, Appl. Environ. Microbiol. 68, 2519 (2002).
- J. Graf, P. V. Dunlap, and E. G. Ruby, Effect of transposon-induced motility mutations on colonization of the host light organ by Vibrio fischeri, J. Bacteriol. 176, 6986 (1994).
- H. P. Erickson, Size and shape of protein molecules at the nanometer level determined by sedimentation, gel filtration, and electron microscopy, Biol. Proc. Online 11, 32 (2009).
- Z. Qu, X. Yi, and K. S. Breuer, Measuring the viscoelastic behavior of dilute polymer solutions using high-speed statistical particle microrheology, Flow Meas. Instrum. 89, 102270 (2023).
- V. A. Martinez, J. Schwarz-Linek, M. Reufer, L. G. Wilson, A. N. Morozov, and W. C. K. Poon, Flagellated bacterial motility in polymer solutions, Proc. Natl. Acad. Sci. USA 111, 17771 (2014).
- R. Kubo, Statistical-mechanical theory of irreversible processes. I. General theory and simple applications to magnetic and conduction problems, J. Phys. Soc. Jpn. 12, 570 (1957).
- E. A. Codling, M. J. Plank, and S. Benhamou, Random walk models in biology, J. R. Soc. Interface 5, 813 (2008).
- P. S. Lovely and F. W. Dahlquist, Statistical measures of bacterial motility and chemotaxis, J. Theor. Biol. 50, 477 (1975).