Journal of Micro-Bio Robotics

, Volume 9, Issue 3–4, pp 47–60 | Cite as

Swimming characterization of Serratia marcescens for bio-hybrid micro-robotics

  • Matthew R. Edwards
  • Rika Wright Carlsen
  • Jiang Zhuang
  • Metin Sitti
Research Paper

Abstract

The last decade has seen remarkable growth in the development of bio-hybrid micron-scale systems, which combine bacteria, tissue, and other biological material with synthetic components to produce uniquely capable devices. Serratia marcescens, a gram-negative bacteria, has many characteristics useful for bio-hybrid systems, including natural adhesiveness, high motility, and ease of cultivation. In light of the utility of the bacterium S. marcescens as a component of bio-hybrid microsystems, we characterize the motility of the species in a fashion useful for those developing such microdevices. The species also provides a complementary platform for studying attributes of flagellated bacteria motility which have thus far been primarily discussed in Escherichia coli. Using a three-dimensional multi-bacteria single-camera tracking system, we capture the trajectories of individual bacteria and calculate run speeds and tumble rates. The mean speed and tumble rate at room temperature are found to be 26 μm/s and 1.34 ± 0.16 tumbles/s, respectively. We characterize the relationship between motility and position on a growth plate and examine the effect of viscosity and temperature on bacterial motion. A linear relationship is found between speed and temperature proportional to that seen previously with E. coli. We also quantify the response of S. marcescens to the chemoattractant L-aspartate, with the strongest chemotactic response at a gradient of 10−4 M/mm. Finally, population scale measurements are compared to individual bacterial dynamics in a linear gradient and are used to validate a simple model of bacterial population dynamics under chemotaxis.

Keywords

3D tracking Chemotaxis Bio-hybrid Swimming speed 

Supplementary material

12213_2014_72_MOESM1_ESM.docx (75 kb)
(DOC 75.4 KB)

References

  1. 1.
    Ahmed T, Stocker R (2008) Experimental verification of the behavioral foundation of bacterial transport parameters using microfluidics. Biophys J 95:4481–4493CrossRefGoogle Scholar
  2. 2.
    Alberti L, Harshey RM (1990) Differentiation of Serratia marcescens 274 into swimmer and swarmer cells. J Bacteriol 172(8):4322–8Google Scholar
  3. 3.
    Arabagi V, Behkam B, Cheung E, Sitti M (2011) Modeling of stochastic motion of bacteria propelled spherical microbeads. J Appl Phys 109(11):114702CrossRefGoogle Scholar
  4. 4.
    Banks G, Schaefer DW, Alpert SS (1975) Light-scattering study of the temperature dependence of Escherichia coli motility. Biophys J 15:253–261CrossRefGoogle Scholar
  5. 5.
    Behkam B, Sitti M (2007) Bacterial flagella-based propulsion and on/off motion control of microscale objects. Appl Phys Lett 90(2):023902CrossRefGoogle Scholar
  6. 6.
    Behkam B, Sitti M (2008) Effect of quantity and configuration of attached bacteria on bacterial propulsion of microbeads. Appl Phys Lett 93(22):223901CrossRefGoogle Scholar
  7. 7.
    Berg HC (1971) How to track bacteria. Rev Sci Instrum 42(6):868CrossRefGoogle Scholar
  8. 8.
    Berg HC, Brown DA (1972) Chemotaxis in Escherichia coli analysed by three-dimensional tracking. Nature 239:500–504CrossRefGoogle Scholar
  9. 9.
    Block SM, Segall JE, Berg HC (1982) Impulse responses in bacterial chemotaxis. Cell 31:215–226CrossRefGoogle Scholar
  10. 10.
    Brown DA, Berg HC (1974) Temporal stimulation of chemotaxis in Escherichia coli. Proc Nat Acad Sci U S A 71:1388–1392CrossRefGoogle Scholar
  11. 11.
    Chen KC, Frod RM, Cummings PT (1998) Perturbation expansion of Alt’s cell balance equations reduces to Segel’s one-dimensional equations for shallow chemoattractant gradients. Nat Appl Math 59:35–57Google Scholar
  12. 12.
    Cheng SY, Heilman S, Wasserman M, Archer S, Shulerac ML, Wu M (2007) A hydrogel-based microfluidic device for the studies of directed cell migration. Lab Chip 7:763–769CrossRefGoogle Scholar
  13. 13.
    Darnton N, Turner L, Breuer K, Berg HC (2004) Moving fluid with bacterial carpets. Biophys J 86(3):1863–70CrossRefGoogle Scholar
  14. 14.
    Darnton NC, Turner L, Rojevsky S, Berg HC (2007) On torque and tumbling in swimming Escherichia coli. J Bacteriol 189(5):1756–64CrossRefGoogle Scholar
  15. 15.
    Demir M, Douarche C, Yoney A, Libchaber A, Salman H (2011) Effects of population density and chemical environment on the behavior of Escherichia coli in shallow temperature gradients. Phys Bio 8(6):063001CrossRefGoogle Scholar
  16. 16.
    Di Leonardo R, Angelani L, Dell’Arciprete D, Ruocco G, Iebba V, Schippa S, Conte MP, Mecarini F, De Angelis F, Di Fabrizio E (2010) Bacterial ratchet motors. Proc Natl Acad Sci U S A 107(21):9541–5CrossRefGoogle Scholar
  17. 17.
    Diao J, Young L, Kim S, Fogarty EA, Heilman SM, Zhou P, Shuler ML, Wu M, DeLisa MP (2006) A three-channel microfluidic device for generating static linear gradients and its application to the quantitative analysis of bacterial chemotaxis. Lab Chip 6:381–388CrossRefGoogle Scholar
  18. 18.
    Dickson JS, Koohmaraie M (1989) Cell surface charge characteristics and their relationship to bacterial attachment to meat surfaces. Appl Environ Microbiol 55(4):832–836Google Scholar
  19. 19.
    Diller E, Sitti M et al (2013) Micro-scale mobile robotics. Foundations and Trends®; in Databases 2(3):143–259Google Scholar
  20. 20.
    Edwards MR, Wright Carlsen R, Sitti M (2013) Near and far-wall effects on the three-dimensional motion of bacteria-driven microbeads. Appl Phys Lett 102(14):143701CrossRefGoogle Scholar
  21. 21.
    Fernandes R, Zuniga M, Sassine FR, Karakoy M, Gracias DH (2011) Enabling cargo-carrying bacteria via surface attachment and triggered release. Small 7(5):588–92CrossRefGoogle Scholar
  22. 22.
    Hejazi A, Falkiner FR (1997) Serratia marcescens. J Med Microbiol 46:903–912CrossRefGoogle Scholar
  23. 23.
    Hesse WR, Kim MJ (2008) Visualization of flagellar interactions on bacterial carpets. J Microsc 233:302–308CrossRefMathSciNetGoogle Scholar
  24. 24.
    Hiratsuka Y, Miyata M, Tada T, Uyeda TQP (2006) A microrotary motor powered by bacteria. Proc Natl Acad Sci U S A 103(37):13618–23CrossRefGoogle Scholar
  25. 25.
    Hoshino T, Imagawa K, Akiyama Y, Morishima K (2012) Cardiomyocyte-driven gel network for bio mechano-informatic wet robotics. Biomed Microdevices 14(6):969–77CrossRefGoogle Scholar
  26. 26.
    Jeon H, Lee Y, Jin S, Koo S, Lee CS, Yoo JY (2009) Quantitative analysis of single bacterial chemotaxis using a linear concentration gradient microchannel. Biomed Microdevices 11:1135–1143CrossRefGoogle Scholar
  27. 27.
    Keller EF, Segel LA (1971) Model for chemotaxis. J Theor Biol 30:225–234CrossRefMATHGoogle Scholar
  28. 28.
    Kim D, Liu A, Diller E, Sitti M (2012) Chemotactic steering of bacteria propelled microbeads. Biomed Microdevices 14(6):1009–1017CrossRefGoogle Scholar
  29. 29.
    Kim MJ, Breuer KS (2008) Microfluidic pump powered by self-organizing bacteria. Small 4(1):111–8CrossRefGoogle Scholar
  30. 30.
    Lauga E, Diluzio WR, Whitesides GM, Stone HA (2006) Swimming in circles : motion of bacteria near solid boundaries. Biophys J 90(2):400–412CrossRefGoogle Scholar
  31. 31.
    Lowe G, Meister M, Berg HC (1987) Rapid rotation of flagellar bundles in swimming bacteria. Nature 325:637–640CrossRefGoogle Scholar
  32. 32.
    Ma Q, Chen C, Wei S, Chen C, Wu LF, Song T (2012) Construction and operation of a microrobot based on magnetotactic bacteria in a microfluidic chip. Biomicrofluidics 6(2):24,107–2410,712CrossRefGoogle Scholar
  33. 33.
    Maeda K, Imae Y, Shioi JI (1976) Effect of temperature on motility and chemotaxis of Escherichia coli. J Bacteriol:127Google Scholar
  34. 34.
    Magariyama Y, Kudo S (2002) A mathematical explanation of an increase in bacterial swimming speed with viscosity in linear-polymer solutions. Biophys J 83(2):733–9CrossRefGoogle Scholar
  35. 35.
    Martel S, Tremblay CC, Ngakeng S, Langlois G (2006) Controlled manipulation and actuation of micro-objects with magnetotactic bacteria. Appl Phys Lett 89(23):233904CrossRefGoogle Scholar
  36. 36.
    Martel S, Mohammadi M, Felfoul O, Lu Z, Pouponneau P (2009) Flagellated magnetotactic bacteria as controlled MRI-trackable propulsion and steering systems for medical nanorobots operating in the human microvasculature. Int J Rob Res 28(4):571–582CrossRefGoogle Scholar
  37. 37.
    Oleksiuk O, Jakovljevic V, Vladimirov N, Carvalho R, Paster E, Ryu WS, Meir Y, Wingreen NS, Kollmann M, Sourjik V (2011) Thermal robustness of signaling in bacterial chemotaxis. Cell 145(2):312–21CrossRefGoogle Scholar
  38. 38.
    Park SJ, Bae H, Kim J, Lim B, Park J, Park S (2010) Motility enhancement of bacteria actuated microstructures using selective bacteria adhesion. Lab Chip 10(13):1706–11CrossRefGoogle Scholar
  39. 39.
    Paster E, Ryu WS (2008) The thermal impulse response of Escherichia coli. Proc Natl Acad Sci U S A 105(14):5373–7CrossRefGoogle Scholar
  40. 40.
    Phillips BR, Quinn JA, Goldfine H (1994) Random motility of swimming bacteria: single cells compared to cell populations. AIChE J 40(2):334–348CrossRefGoogle Scholar
  41. 41.
    Phuyal K, Kim MJ (2013) Mechanics of swimming of multi-body bacterial swarmers using non-labeled cell tracking algorithm. Phys Fluids 25(1):011901CrossRefGoogle Scholar
  42. 42.
    Ricotti L, Menciassi A (2012) Bio-hybrid muscle cell-based actuators. Biomed Microdevices 14(6):987–98CrossRefGoogle Scholar
  43. 43.
    Rivero MA, Tranquillo RT, Buettner HM, Lauffenburger DA (1989) Transport model for chemotactic cell-populations based on individual cell behavior. Chem Eng Sci 44:2281–2897CrossRefGoogle Scholar
  44. 44.
    Sakar MS, Steager EB, Kim DH, Julius AA, Kim M, Kumar V, Pappas GJ (2011) Modeling, control and experimental characterization of microbiorobots. Int J Rob Res 30(6):647–658CrossRefGoogle Scholar
  45. 45.
    Schneider WR, Doetsch RN (1974) Effect of viscosity on bacterial motility. J Bacteriol 117(2):696–701Google Scholar
  46. 46.
    Sitti M (2007) Microscale and Nanoscale Robotics Systems. IEEE Robot Autom Mag 14(1):53–60CrossRefGoogle Scholar
  47. 47.
    Sitti M (2009) Voyage of the microrobots. Nature 458(7242):1121–1122CrossRefGoogle Scholar
  48. 48.
    Sokolov A, Apodaca MM, Grzybowski BA, Aranson IS (2010) Swimming bacteria power microscopic gears. Proc Natl Acad Sci U S A 107(3):969–74CrossRefGoogle Scholar
  49. 49.
    Steager EB, Patel JA, Kim CB, Yi DK, Lee W, Kim MJ (2007) A novel method of microfabrication and manipulation of bacterial teamsters in low Reynolds number fluidic environments. Microfluid Nanofluid 5(3):337–346CrossRefGoogle Scholar
  50. 50.
    Steager EB, Kim CB, Kim MJ (2008) Dynamics of pattern formation in bacterial swarms. Phys Fluids 20(7):073601CrossRefGoogle Scholar
  51. 51.
    Steager EB, Sakar MS, Kim DH, Kumar V, Pappas GJ, Kim MJ (2011) Electrokinetic and optical control of bacterial microrobots. J Micromech Microeng 21(3):035001CrossRefGoogle Scholar
  52. 52.
    Tran TH, Hyung Kim D, Kim J, Jun Kim M, Byun D (2011) Use of an AC electric field in galvanotactic on/off switching of the motion of a microstructure blotted by Serratia marcescens. Appl Phys Lett99(6):063702CrossRefGoogle Scholar
  53. 53.
    Traoré M, Sahari A, Behkam B (2011) Computational and experimental study of chemotaxis of an ensemble of bacteria attached to a microbead. Phys Rev E Stat Nonlin Soft Matter Phys 84(6):1–6Google Scholar
  54. 54.
    Weibel DB, Garstecki P, Ryan D, DiLuzio WR, Mayer M, Seto JE, Whitesides GM (2005) Microoxen: microorganisms to move microscale loads. Proc Natl Acad Sci U S A 102(34):11963–7CrossRefGoogle Scholar
  55. 55.
    Willert CE, Gharib M (1992) Three-dimensional particle imaging with a single camera. Exp Fluids 358:353–358Google Scholar
  56. 56.
    Wu M, Roberts JW, Buckley M (2005) Three-dimensional fluorescent particle tracking at micron-scale using a single camera. Exp Fluids 38(4):461–465CrossRefGoogle Scholar
  57. 57.
    Xi J, Schmidt JJ, Montemagno CD (2005) Self-assembled microdevices driven by muscle. Nat Mater 4(2):180–4CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2014

Authors and Affiliations

  • Matthew R. Edwards
    • 1
  • Rika Wright Carlsen
    • 1
  • Jiang Zhuang
    • 1
  • Metin Sitti
    • 1
  1. 1.Department of Mechanical EngineeringCarnegie Mellon UniversityPittsburghUSA

Personalised recommendations