TY - JOUR
T1 - Bacteria push the limits of chemotactic precision to navigate dynamic chemical gradients
AU - Brumley, Douglas R.
AU - Carrara, Francesco
AU - Hein, Andrew M.
AU - Yawata, Yutaka
AU - Levin, Simon Asher
AU - Stocker, Roman
N1 - Funding Information:
ACKNOWLEDGMENTS. We thank V. Sourjik, N. Wingreen, T. Emonet, F. Menolascina, K. Son, V. Fernandez, and J. Keegstra for useful discussions. This work was supported by an Australian Research Council Discovery Early Career Researcher Award DE180100911 (to D.R.B.); The University of Melbourne Computational Biology Research Initiative and high-performance computing system (D.R.B.); a Swiss National Science Foundation Early Mobility Postdoctoral Fellowship (F.C.); a James S. McDonnell Foundation Fellowship (A.M.H.); Army Research Office Grants W911NG-11-1-0385 and W911NF-14-1-0431 (to S.A.L.); Simons Foundation Grant 395890 (to S.A.L.); Gordon and Betty Moore Marine Microbial Initiative Investigator Award GBMF3783 (to R.S.); and Simons Foundation Grant 542395 (to R.S.) as part of the Principles of Microbial Ecosystems Collaborative (PriME).
Funding Information:
25. Berg HC (2008) E. coli in Motion (Springer, Berlin). Materials and Methods A detailed discussion of the experimental protocols, mathematical theory, and numerical simulations is included in the SI Appendix. ACKNOWLEDGMENTS. We thank V. Sourjik, N. Wingreen, T. Emonet, F. Menolascina, K. Son, V. Fernandez, and J. Keegstra for useful discussions. This work was supported by an Australian Research Council Discovery Early Career Researcher Award DE180100911 (to D.R.B.); The University of Melbourne Computational Biology Research Initiative and high-performance computing system (D.R.B.); a Swiss National Science Foundation Early Mobility Postdoctoral Fellowship (F.C.); a James S. McDonnell Foundation Fellowship (A.M.H.); Army Research Office Grants W911NG-11-1-0385 and W911NF-14-1-0431 (to S.A.L.); Simons Foundation Grant 395890 (to S.A.L.); Gordon and Betty Moore Marine Microbial Initiative Investigator Award GBMF3783 (to R.S.); and Simons Foundation Grant 542395 (to R.S.) as part of the Principles of Microbial Ecosystems Collaborative (PriME). 26. Long J, Zucker SW, Emonet T (2017) Feedback between motion and sensation provides nonlinear boost in run-and-tumble navigation. PLoS Comput Biol 13: e1005429. 27. Xie L, Lu C, Wu XL (2015) Marine bacterial chemoresponse to a stepwise chemoattrac-tant stimulus. Biophys J 108:766–774. 28. Morton-Firth CJ, Shimizu TS, Bray D (1999) A free-energy-based stochastic simulation of the Tar receptor complex1. J Mol Biol 286:1059–1074. 29. Son K, Guasto JS, Stocker R (2013) Bacteria can exploit a flagellar buckling instability to change direction. Nat Phys 9:494–498. 30. Bray D, Levin MD, Lipkow K (2007) The chemotactic behavior of computer-based surrogate bacteria. Curr Biol 17:12–19. 31. Bialek W, Setayeshgar S (2005) Physical limits to biochemical signaling. Proc Natl Acad Sci USA 102:10040–10045. 32. Korobkova E, Emonet T, Vilar JMG, Shimizu TS, Cluzel P (2004) From molecular noise to behavioural variability in a single bacterium. Nature 428:574–578. 33. Keegstra JM, et al. (2017) Phenotypic diversity and temporal variability in a bacterial signaling network revealed by single-cell FRET. eLife 6:e27455. 34. Govern CC, ten Wolde PR (2014) Optimal resource allocation in cellular sensing sys-tems. Proc Natl Acad Sci USA 111:17486–17491. 35. Keller EF, Segel LA (1970) Initiation of slime mold aggregation viewed as an instability. J Theor Biol 26:399–415. 36. Seymour JR, Amin SA, Raina JB, Stocker R (2017) Zooming in on the phycosphere: The ecological interface for phytoplankton–bacteria relationships. Nat Microbiol 2:17065. 37. Azam F, Malfatti F (2007) Microbial structuring of marine ecosystems. Nat Rev Micro 5:782–791. 38. Barlow M (2009) What antimicrobial resistance has taught us about horizontal gene transfer. Horizontal Gene Transfer Genomes Flux 532:397–411. 39. Moor K, et al. (2017) High-avidity IgA protects the intestine by enchaining growing bacteria. Nature 544:498–502. 40. Stocker R, Seymour JR, Samadani A, Hunt DE, Polz MF (2008) Rapid chemotactic response enables marine bacteria to exploit ephemeral microscale nutrient patches. Proc Natl Acad Sci USA 105:4209–4214. 41. Barbara GM, Mitchell JG (2003) Marine bacterial organisation around point-like sources of amino acids. FEMS Microbiol Ecol 43:99–109. 42. Jackson GA (1987) Simulating chemosensory responses of marine microorganisms. Limnol Oceanogr 32:1253–1266. 43. Lan G, Sartori P, Neumann S, Sourjik V, Tu Y (2012) The energy-speed-accuracy trade-off in sensory adaptation. Nat Phys 8:422–428. 44. Lestas I, Vinnicombe G, Paulsson J (2010) Fundamental limits on the suppression of molecular fluctuations. Nature 467:174–178. 45. Magariyama Y, et al. (1995) Simultaneous measurement of bacterial flagellar rotation rate and swimming speed. Biophys J 69:2154–2162. 46. Flores M, Shimizu TS, ten Wolde PR, Tostevin F (2012) Signaling noise enhances chemotactic drift of E. coli. Phys Rev Lett 109:148101. 47. Sneddon M, Pontius W, Emonet T (2012) Stochastic coordination of multiple actuators reduces latency and improves chemotactic response in bacteria. Proc Natl Acad Sci USA 109:805–810. 48. He R, Zhang R, Yuan J (2016) Noise-induced increase of sensitivity in bacterial chemotaxis. Biophys J 111:430–437. 49. Hu B, Tu Y (2013) Coordinated switching of bacterial flagellar motors: Evidence for direct motor-motor coupling? Phys Rev Lett 110:158703. APPLIED PHYSICAL SCIENCES BIOPHYSICS AND COMPUTATIONAL BIOLOGY
Publisher Copyright:
© 2019 National Academy of Sciences. All rights reserved.
PY - 2019
Y1 - 2019
N2 - Ephemeral aggregations of bacteria are ubiquitous in the environment, where they serve as hotbeds of metabolic activity, nutrient cycling, and horizontal gene transfer. In many cases, these regions of high bacterial concentration are thought to form when motile cells use chemotaxis to navigate to chemical hotspots. However, what governs the dynamics of bacterial aggregations is unclear. Here, we use an experimental platform to create realistic submillimeter-scale nutrient pulses with controlled nutrient concentrations. By combining experiments, mathematical theory, and agent-based simulations, we show that individual Vibrio ordalii bacteria begin chemotaxis toward hotspots of dissolved organic matter (DOM) when the magnitude of the chemical gradient rises sufficiently far above the sensory noise that is generated by stochastic encounters with chemoattractant molecules. Each DOM hotspot is surrounded by a dynamic ring of chemotaxing cells, which congregate in regions of highDOMconcentration before dispersing as DOM diffuses and gradients become too noisy for cells to respond to. We demonstrate that V. ordalii operates close to the theoretical limits on chemotactic precision. Numerical simulations of chemotactic bacteria, in which molecule counting noise is explicitly taken into account, point at a tradeoff between nutrient acquisition and the cost of chemotactic precision. More generally, our results illustrate how limits on sensory precision can be used to understand the location, spatial extent, and lifespan of bacterial behavioral responses in ecologically relevant environments.
AB - Ephemeral aggregations of bacteria are ubiquitous in the environment, where they serve as hotbeds of metabolic activity, nutrient cycling, and horizontal gene transfer. In many cases, these regions of high bacterial concentration are thought to form when motile cells use chemotaxis to navigate to chemical hotspots. However, what governs the dynamics of bacterial aggregations is unclear. Here, we use an experimental platform to create realistic submillimeter-scale nutrient pulses with controlled nutrient concentrations. By combining experiments, mathematical theory, and agent-based simulations, we show that individual Vibrio ordalii bacteria begin chemotaxis toward hotspots of dissolved organic matter (DOM) when the magnitude of the chemical gradient rises sufficiently far above the sensory noise that is generated by stochastic encounters with chemoattractant molecules. Each DOM hotspot is surrounded by a dynamic ring of chemotaxing cells, which congregate in regions of highDOMconcentration before dispersing as DOM diffuses and gradients become too noisy for cells to respond to. We demonstrate that V. ordalii operates close to the theoretical limits on chemotactic precision. Numerical simulations of chemotactic bacteria, in which molecule counting noise is explicitly taken into account, point at a tradeoff between nutrient acquisition and the cost of chemotactic precision. More generally, our results illustrate how limits on sensory precision can be used to understand the location, spatial extent, and lifespan of bacterial behavioral responses in ecologically relevant environments.
KW - Chemotaxis
KW - Microbial ecology
KW - Motility
KW - Ocean
KW - Sensing noise
UR - http://www.scopus.com/inward/record.url?scp=85066426348&partnerID=8YFLogxK
UR - http://www.scopus.com/inward/citedby.url?scp=85066426348&partnerID=8YFLogxK
U2 - 10.1073/pnas.1816621116
DO - 10.1073/pnas.1816621116
M3 - Article
C2 - 31097577
AN - SCOPUS:85066426348
SN - 0027-8424
VL - 166
SP - 10792
EP - 10797
JO - Proceedings of the National Academy of Sciences of the United States of America
JF - Proceedings of the National Academy of Sciences of the United States of America
IS - 22
ER -