Fast, high-throughput measurement of collective behaviour in a bacterial population

Journal of the Royal Society Interface

Volumn 11, Issue 98, 2014, Pages

  Colin, R ^a,c   Zhang, R ^b   Wilson, L G ^a,d  

^a HARVARD UNIVERSITY   (United States)

^b UNIVERSITY OF SCIENCE AND TECHNOLOGY OF CHINA   (China)

^c MAX PLANCK INSTITUTE FOR TERRESTRIAL MICROBIOLOGY   (Germany)

^d UNIVERSITY OF YORK   (United Kingdom)

Author keywords

Bacterial chemotaxis; Collective motion; Fourier image analysis

Indexed keywords

ALKYLATION; BACTERIA; BACTERIOLOGY; IMAGE ANALYSIS;

BACTERIAL CHEMOTAXIS; BACTERIAL POPULATION; COLLECTIVE BEHAVIOUR; COLLECTIVE MOTIONS; ESCHERICHIA COLI BACTERIA; HIGH-THROUGHPUT MEASUREMENTS; HIGH-TIME RESOLUTION; IMAGE ANALYSIS METHOD;

BIOCHEMISTRY;

ARTICLE; BACTERIAL PHENOMENA AND FUNCTIONS; BACTERIAL SURVIVAL; BACTERIAL VIRULENCE; CELL MIGRATION; CHEMOTAXIS; ESCHERICHIA COLI; FLUID FLOW; HIGH THROUGHPUT MEASUREMENT; MEASUREMENT; METHYLATION; NONHUMAN; SIMULATION; THEORY; VALIDATION PROCESS; ALGORITHM; BIOLOGICAL MODEL; COMPUTER PROGRAM; COMPUTER SIMULATION; IMAGE PROCESSING; LIGHT; PHYSIOLOGY; RADIATION SCATTERING; SIGNAL TRANSDUCTION; VIDEORECORDING;

LIGAND;

ALGORITHMS; BACTERIAL PHYSIOLOGICAL PHENOMENA; CHEMOTAXIS; COMPUTER SIMULATION; ESCHERICHIA COLI; IMAGE PROCESSING, COMPUTER-ASSISTED; LIGANDS; LIGHT; METHYLATION; MODELS, BIOLOGICAL; SCATTERING, RADIATION; SIGNAL TRANSDUCTION; SOFTWARE; VIDEO RECORDING;

EID: 84904992232     PISSN: 17425689     EISSN: 17425662     Source Type: Journal    
DOI: 10.1098/rsif.2014.0486     Document Type: Article

References (48)

1. Crocker JC, Grier DG. 1996 Methods of digital video microscopy for colloidal studies. J. Colloid Interface Sci. 179, 298-310. (doi:10.1006/jcis. 1996.0217)
2. Berg HC, Brown DA. 1972 Chemotaxis in Escherichia coli analyzed by three-dimensional tracking. Nature 239, 500-504. (doi:10.1038/239500a0)
3. Schneider WR, Doetsch RN. 1974 Effect of viscosity on bacterial motility. J. Bacteriol. 117, 696-701.
4. Wu M, Roberts JW, Kim S, Koch DL, DeLisa MP. 2006 Collective bacterial dynamics revealed using a three-dimensional population-scale defocused particle tracking technique. Appl. Environ. Microbiol. 72, 4987-4994. (doi:10.1128/AEM.00158-06)
5. Polin M, Tuval I, Drescher K, Gollub JP, Goldstein RE. 2009 Chlamydomonas swims with two 'gears' in a eukaryotic version of run-and-tumble locomotion. Science 325, 487-490. (doi:10.1126/science.1172667)
6. Wilson LG, Carter LM, Reece SE. 2013 High-speed holographic microscopy of malaria parasites reveals ambidextrous flagellar waveforms. Proc. Natl Acad. Sci. USA 110, 18 769-18 774. (doi:10.1073/pnas.1309934110)
7. Berne BJ, Pecora R. 2000 Dynamic light scattering: with applications to chemistry, biology, and physics. New York, NY: Courier Dover Publications.
8. Cerbino R, Trappe V. 2008 Differential dynamic microscopy: probing wave vector dependent dynamics with a microscope. Phys. Rev. Lett. 100, 188102. (doi:10.1103/PhysRevLett.100.188102)
9. Giavazzi F, Brogioli D, Trappe V, Bellini T, Cerbino R. 2009 Scattering information obtained by optical microscopy: differential dynamic microscopy and beyond. Phys. Rev. E 80, 031403. (doi:10.1103/PhysRevE.80.031403)
10. Wilson LG, Martinez VA, Schwarz-Linek J, Tailleur J, Bryant G, Pusey PN, Poon WCK. 2011 Differential dynamic microscopy of bacterial motility. Phys. Rev. Lett. 106, 018101. (doi:10.1103/PhysRevLett.106.018101)
11. Martinez VA, Besseling R, Croze OA, Tailleur J, Reufer M, Schwarz-Linek J, Wilson LG, Bees MA, Poon WCK. 2012 Differential dynamic microscopy: a high-throughput method for characterizing the motility of microorganisms. Biophys. J. 103, 1637-1647. (doi:10.1016/j.bpj.2012.08.045)
12. Morandi C, Piazza F, Capancioni R. 1986 Robust 1-D equivalent of phase-correlation image registration algorithm. Electron. Lett. 22, 386-388. (doi:10. 1049/el:19860263)
13. Vernon D. 1999 Computation of instantaneous optical flow using the phase of Fourier components. Image Vis. Comput. 17, 189-199. (doi:10.1016/S0262- 8856(98)00094-8)
14. Keymer JE, Galajda P, Lambert G, Liao D, Austin RH. 2008 Computation of mutual fitness by competing bacteria. Proc. Natl Acad. Sci. USA 105, 20 269-20 273. (doi:10.1073/pnas.0810792105)
15. Cates ME. 2012 Diffusive transport without detailed balance in motile bacteria: does microbiology need statistical physics? Rep. Prog. Phys. 75, 042601. (doi:10.1088/0034-4885/75/4/042601)
16. Wolgemuth CW. 2011 Does cell biology need physicists? Physics 4, 4. (doi:10.1103/Physics.4.4)
17. Sourjik V, Wingreen NS. 2012 Responding to chemical gradients: bacterial chemotaxis. Curr. Opin. Cell. Biol. 24, 262-268. (doi:10.1016/j.ceb.2011.11.008)
18. Tindall MJ, Gaffney EA, Maini PK, Armitage JP. 2012 Theoretical insights into bacterial chemotaxis. Wiley Interdiscip. Rev. Syst. Biol. Med. 4, 247259. (doi:10.1002/wsbm.1168)
19. Saragosti J, Calvez V, Bournaveas N, Perthame B, Buguin A, Silberzan P. 2011 Directional persistence of chemotactic bacteria in a traveling concentration wave. Proc. Natl Acad. Sci. USA 108, 16 235-16 240. (doi:10.1073/pnas.1101996108)
20. Mello BA, Tu Y. 2005 An allosteric model for heterogeneous receptor complexes: understanding bacterial chemotaxis responses to multiple stimuli. Proc. Natl Acad. Sci. USA 102, 17 354-17 359. (doi:10.1073/pnas.0506961102)
21. Keymer JE, Endres RG, Skoge M, Meir Y, Wingreen NS. 2006 Chemosensing in Escherichia coli: two regimes of two-state receptors. Proc. Natl Acad. Sci. USA 103, 1786-1791. (doi:10.1073/pnas.0507438103)
22. Mello BA, Tu Y. 2007 Effects of adaptation in maintaining high sensitivity over a wide range of backgrounds for Escherichia coli chemotaxis. Biophys. J. 92, 2329-2337. (doi:10.1529/biophysj.106.097808)
23. Sourjik V. 2004 Receptor clustering and signal processing in E. coli chemotaxis. Trends Microbiol. 12, 569-576. (doi:10.1016/j.tim.2004.10.003)
24. Bai F, Branch RW, Nicolau DV, Pilizota T, Steel BC, Maini PK, Berry RM. 2010 Conformational spread as a mechanism for cooperativity in the bacterial flagellar switch. Science 327, 685-689. (doi:10.1126/science.1182105)
25. Lele PP, Branch RW, Nathan VSJ, Berg HC. 2012 Mechanism for adaptive remodeling of the bacterial flagellar switch. Proc. Natl Acad. Sci. USA 109, 20 018-20 022. (doi:10.1073/pnas.1212327109)
26. Mesibov R, Ordal GW, Adler J. 1973 The range of attractant concentrations for bacterial chemotaxis and the threshold and size of response over this range Weber law and related phenomena. J. Gen. Physiol. 62, 203-223. (doi:10.1085/jgp.62.2.203)
27. Kalinin YV, Jiang L, Tu Y, Wu M. 2009 Logarithmic sensing in Escherichia coli bacterial chemotaxis. Biophys. J. 96, 2439-2448. (doi:10.1016/j.bpj.2008. 10.027)
28. Lazova MD, Ahmed T, Bellomo D, Stocker R, Shimizu TS. 2011 Response rescaling in bacterial chemotaxis. Proc. Natl Acad. Sci. USA 108, 13 870-13 875. (doi:10.1073/pnas.1108608108)
29. Tindall M, Maini P, Porter S, Armitage J. 2008 Overview of mathematical approaches used to model bacterial chemotaxis II: bacterial populations. Bull. Math. Biol. 70, 1570-1607. (doi:10.1007/s11538-008-9322-5)
30. Lovely PS, Dahlquist F. 1975 Statistical measures of bacterial motility and chemotaxis. J. Theor. Biol. 50, 477-496. (doi:10.1016/0022-5193(75)90094-6)
31. Gennes P-Gd. 2004 Chemotaxis: the role of internal delays. Eur. Biophys. J. 33, 691-693. (doi:10.1007/ s00249-004-0426-z)
32. Emonet T, Macal CM, North MJ, Wickersham CE, Cluzel P. 2005 AgentCell: a digital single-cell assay for bacterial chemotaxis. Bioinformatics 21, 2714-2721. (doi:10.1093/bioinformatics/bti391)
33. Bray D, Levin MD, Lipkow K. 2007 The chemotactic behavior of computer-based surrogate bacteria. Curr. Biol. 17, 12-19. (doi:10.1016/j.cub. 2006.11.027)
34. Keller EF, Segel LA. 1971 Model for chemotaxis. J. Theor. Biol. 30, 225-234. (doi:10.1016/0022-5193(71)90050-6)
35. Berg HC. 1993 Random walks in biology. Princeton, NJ: Princeton University Press.
36. Masson J-B, Voisinne G, Wong-Ng J, Celani A, Vergassola M. 2012 Noninvasive inference of the molecular chemotactic response using bacterial trajectories. Proc. Natl Acad. Sci. USA 109, 1802-1807. (doi:10.1073/pnas. 1116772109)
37. Tu Y, Shimizu TS, Berg HC. 2008 Modeling the chemotactic response of Escherichia coli to time-varying stimuli. Proc. Natl Acad. Sci. USA 105, 14 855-14 860. (doi:10.1073/pnas.0807569105)
38. Monod J, Wyman J, Changeux JP. 1965 On the nature of allosteric transitions: a plausible model. J. Mol. Biol. 12, 88-118. (doi:10.1016/S0022- 2836(65)80285-6)
39. Cluzel P, Surette M, Leibler S. 2000 An ultra-sensitive bacterial motor revealed by monitoring signaling proteins in single cells. Science 287, 1652-1655. (doi:10.1126/science.287.5458.1652)
40. Si G, Wu T, Ouyang Q, Tu Y. 2012 Pathway-based mean-field model for Escherichia coli chemotaxis. Phys. Rev. Lett. 109, 048101. (doi:10.1103/ PhysRevLett.109.048101)
41. Salman H, Libchaber A. 2007 A concentration-dependent switch in the bacterial response to temperature. Nat. Cell Biol. 9, 1098-1100. (doi:10.1038/ncb1632)
42. Westerweel J, Elsinga GE, Adrian RJ. 2013 Particle image velocimetry for complex and turbulent flows. Annu. Rev. Fluid Mech. 45, 409-436. (doi:10.1146/annurev-fluid-120710-101204)
43. Locsei JT. 2007 Persistence of direction increases the drift velocity of run and tumble chemotaxis. J. Math. Biol. 55, 41-60. (doi:10.1007/s00285-007- 0080-z)
44. Nicolau Jr DV, Armitage JP, Maini PK. 2009 Directional persistence and the optimality of run-and-tumble chemotaxis. Comput. Biol. Chem. 33, 269-274. (doi:10.1016/j.compbiolchem.2009.06.003)
45. Yuan J, Branch RW, Hosu BG, Berg HC. 2012 Adaptation at the output of the chemotaxis signalling pathway. Nature 484, 233-236. (doi:10.1038/nature10964)
46. Ahmed T, Shimizu TS, Stocker R. 2010 Bacterial chemotaxis in linear and nonlinear steady microfluidic gradients. Nano Lett. 10, 3379-3385. (doi:10.1021/nl101204e)
47. Segall JE, Block SM, Berg HC. 1986 Temporal comparisons in bacterial chemotaxis. Proc. Natl Acad. Sci. USA 83, 8987-8991. (doi:10.1073/pnas.83.23. 8987)
48. Celani A, Vergassola M. 2010 Bacterial strategies for chemotaxis response. Proc. Natl Acad. Sci. USA 107, 1391-1396. (doi:10.1073/pnas. 0909673107)