Advertisement

Microscale confinement features can affect biofilm formation

Abstract

The majority of bacteria in nature live in biofilms, where they are encased by extracellular polymeric substances (EPS) and adhere to various surfaces and interfaces. Investigating the process of biofilm formation is critical for advancing our understanding of microbes in their most common mode of living. Despite progress in characterizing the effect of various environmental factors on biofilm formation, work remains to be done in the realm of exploring the inter-relationship between hydrodynamics, microbial adhesion and biofilm growth. We investigate the impact of secondary flow structures, which are created due to semi-confined features in a microfluidic device, on biofilm formation of Shewanella oneidensis MR-1. Secondary flows are important in many natural and artificial systems, but few studies have investigated their role in biofilm formation. To direct secondary flows in the creeping flow regime, where the Reynolds number is low, we flow microbe-laden culture through microscale confinement features. We demonstrate that these confinement features can result in pronounced changes in biofilm dynamics as a function of the fluid flow rate.

This is a preview of subscription content, log in to check access.

Access options

Buy single article

Instant unlimited access to the full article PDF.

US$ 39.95

Price includes VAT for USA

Subscribe to journal

Immediate online access to all issues from 2019. Subscription will auto renew annually.

US$ 99

This is the net price. Taxes to be calculated in checkout.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

References

  1. Ardekani AM, Gore E (2012) Emergence of a limit cycle for swimming microorganisms in a vortical flow of a viscoelastic fluid. Phys Rev E 85(5):056309. doi:10.1103/PhysRevE.85.056309

  2. Boedicker JQ, Vincent ME, Ismagilov RF (2009) Microfluidic confinement of single cells of bacteria in small volumes initiates high-density behavior of quorum sensing and growth and reveals its variability. Angewandte Chemie 48(32):5908–5911. doi:10.1002/anie.200901550

  3. Callow JA, Callow ME (2011) Trends in the development of environmentally friendly fouling-resistant marine coatings. Nat Commun 2:244. doi:10.1038/ncomms1251

  4. Chai L, Vlamakis H, Kolter R (2011) Extracellular signal regulation of cell differentiation in biofilms. MRS Bull 36(5):374–379. doi:10.1557/mrs.2011.68

  5. Chen CH, Lu Y, Sin MLY, Mach KE, Zhang DD, Gau V, Liao JC, Wong PK (2010) Antimicrobial susceptibility testing using high surface-to-volume ratio microchannels. Anal Chem 82(3):1012–1019. doi:10.1021/ac9022764

  6. Cho HJ, Jonsson H, Campbell K, Melke P, Williams JW, Jedynak B, Stevens AM, Groisman A, Levchenko A (2007) Self-organization in high-density bacterial colonies: efficient crowd control. PLoS Biol 5(11):2614–2623. doi:e30210.1371/journal.pbio.0050302

  7. Chung KK, Schumacher JF, Sampson EM, Burne RA, Antonelli PJ, Brennan AB (2007) Impact of engineered surface microtopography on biofilm formation of Staphylococcus aureus. Biointerphases 2(2):89–94. doi:10.1116/1.2751405

  8. Connell JL, Wessel AK, Parsek MR, Ellington AD, Whiteley M, Shear JB (2010) Probing prokaryotic social behaviors with bacterial “Lobster Traps”. Mbio 1(4):e00202–e00210. doi:1128/mBio.00202-10

  9. Costerton JW, Lewandowski Z, Caldwell DE, Korber DR, Lappinscott HM (1995) Microbial biofilms. Annu Rev Microbiol 49:711–745

  10. De la Fuente L, Montanes E, Meng YZ, Li YX, Burr TJ, Hoch HC, Wu MM (2007) Assessing adhesion forces of type I and type IV pili of Xylella fastidiosa bacteria by use of a microfluidic flow chamber. Appl Environ Microbiol 73(8):2690–2696. doi:101128/Aem.02649-06

  11. Guglielmini L, Rusconi R, Lecuyer S, Stone HA (2011) Three-dimensional features in low-Reynolds-number confined corner flows. J Fluid Mech 668:33–57. doi:10.1017/s0022112010004519

  12. Haussler S, Parsek MR (2010) Biofilms 2009: new perspectives at the heart of surface-associated microbial communities. J Bacteriol 192(12):2941–2949. doi:10.1128/jb.00332-10

  13. Hochbaum AI, Aizenberg J (2010) Bacteria pattern spontaneously on periodic nanostructure arrays. Nano Lett 10(9):3717–3721. doi:10.1021/nl102290k

  14. Hohne DN, Younger JG, Solomon MJ (2009) Flexible microfluidic device for mechanical property characterization of soft viscoelastic solids such as bacterial biofilms. Langmuir 25(13):7743–7751. doi:10.1021/la803413x

  15. Ingham CJ, Vlieg J (2008) MEMS and the microbe. Lab Chip 8(10):1604–1616. doi:10.1039/b804790a

  16. Janakiraman V, Englert D, Jayaraman A, Baskaran H (2009) Modeling growth and quorum sensing in biofilms grown in microfluidic chambers. Ann Biomed Eng 37(6):1206–1216. doi:10.1007/s10439-009-9671-8

  17. Khoo X, Grinstaff MW (2011) Novel infection-resistant surface coatings: a bioengineering approach. MRS Bull 36(5):357–366. doi:10.1557/mrs.2011.66

  18. Kim KP, Kim YG, Choi CH, Kim HE, Lee SH, Chang WS, Lee CS (2010) In situ monitoring of antibiotic susceptibility of bacterial biofilms in a microfluidic device. Lab Chip 10(23):3296–3299. doi:10.1039/c0lc00154f

  19. Lee JH, Kaplan JB, Lee WY (2008) Microfluidic devices for studying growth and detachment of Staphylococcus epidermidis biofilms. Biomed Microdevices 10(4):489–498. doi:10.1007/s10544-007-9157-0

  20. Liu Y, Tay JH (2002) The essential role of hydrodynamic shear force in the formation of biofilm and granular sludge. Water Res 36(7):1653–1665. doi:10.1016/s0043-1354(01)00379-7

  21. Lovley DR (2008) The microbe electric: conversion of organic matter to electricity. Curr Opin Biotechnol 19(6):564–571. doi:10.1016/j.copbio.2008.10.005

  22. Mabrouk N, Deffuant G, Tolker-Nielsen T, Lobry C (2010) Bacteria can form interconnected microcolonies when a self-excreted product reduces their surface motility: evidence from individual-based model simulations. Theory Biosci 129(1):1–13. doi:10.1007/s12064-009-0078-8

  23. Moffatt HK (1964) Viscous and resistive eddies near a sharp corner. J Fluid Mech 18(1):1–18. doi:10.1017/s0022112064000015

  24. Nakagaki T, Yamada H, Toth A (2000) Maze-solving by an amoeboid organism. Nature 407(6803):470. doi:10.1038/35035159

  25. Nealson KH, Finkel SE (2011) Electron flow and biofilms. MRS Bull 36(5):380–384. doi:10.1557/mrs.2011.69

  26. Neethirajan S, Karig D, Kumar A, Mukherjee PP, Retterer S, Doktycz M (2012) Biofilms in microfluidic devices. In: Bhushan B (ed) Encylopedia of nanotechnology. Springer, New York

  27. Paramonova E, Kalmykowa OJ, van der Mei HC, Busscher HJ, Sharma PK (2009) Impact of hydrodynamics on oral biofilm strength. J Dent Res 88(10):922–926. doi:10.1177/0022034509344569

  28. Park A, Jeong H–H, Lee J, Kim KP, Lee C-S (2011) Effect of shear stress on the formation of bacterial biofilm in a microfluidic channel. Biochip J 5(3):236–241. doi:10.1007/s13206-011-5307-9

  29. Purevdorj B, Costerton JW, Stoodley P (2002) Influence of hydrodynamics and cell signaling on the structure and behavior of Pseudomonas aeruginosa biofilms. Appl Environ Microbiol 68(9):4457–4464. doi:10.1128/aem.68.9.4457-4464.2002

  30. Qian F, Baum M, Gu Q, DE Morse (2009) A 1.5 µL microbial fuel cell for on-chip bioelectricity generation. Lab Chip 9(21):3076–3081. doi:10.1039/b910586g

  31. Remis JP, Costerton JW, Auer M (2010) Biofilms: structures that may facilitate cell–cell interactions. ISME J 4(9):1085–1087. doi:10.1038/ismej.2010.105

  32. Richter L, Stepper C, Mak A, Reinthaler A, Heer R, Kast M, Bruckl H, Ertl P (2007) Development of a microfluidic biochip for online monitoring of fungal biofilm dynamics. Lab Chip 7(12):1723–1731. doi:10.1039/b708236c

  33. Rusconi R, Lecuyer S, Guglielmini L, Stone HA (2010) Laminar flow around corners triggers the formation of biofilm streamers. J R Soc Interface 7(50):1293–1299. doi:10.1098/rsif.2010.0096

  34. Rusconi R, Lecuyer S, Autrusson N, Guglielmini L, Stone HA (2011) Secondary flow as a mechanism for the formation of biofilm streamers. Biophys J 100(6):1392–1399. doi:10.1016/j.bpj.2011.01.065

  35. Santiago JG, Wereley ST, Meinhart CD, Beebe DJ, Adrian RJ (1998) A particle image velocimetry system for microfluidics. Exp Fluids 25(4):316–319

  36. Shen C, Floryan JM (1985) Low Reynolds-number flow over cavities. Phys Fluids 28(11):3191–3202

  37. Shrout JD, Tolker-Nielsen T, Givskov M, Parsek MR (2011) The contribution of cell–cell signaling and motility to bacterial biofilm formation. MRS Bull 36(5):367–373. doi:10.1557/mrs.2011.67

  38. Stewart PS, Franklin MJ (2008) Physiological heterogeneity in biofilms. Nat Rev Microbiol 6(3):199–210. doi:10.1038/nrmicro1838

  39. Stoodley P, Dodds I, Boyle JD, Lappin-Scott HM (1999) Influence of hydrodynamics and nutrients on biofilm structure. J Appl Microbiol 85:19S–28S

  40. Thormann KM, Saville RM, Shukla S, Pelletier DA, Spormann AM (2004) Initial phases of biofilm formation in Shewanella oneidensis MR-1. J Bacteriol 186(23):8096–8104. doi:10.1128/jb.186.23.8096-8104.2004

  41. Valiei A, Kumar A, Mukherjee PP, Liu Y, Thundat T (2012) A web of streamers: biofilm formation in a porous microfluidic device. Lab Chip 12(24):5133–5137

  42. Volfson D, Cookson S, Hasty J, Tsimring LS (2008) Biomechanical ordering of dense cell populations. Proc Natl Acad Sci USA 105(40):15346–15351. doi:10.1073/pnas.0706805105

  43. Wereley ST, Gui L, Meinhart CD (2002) Advanced algorithms for microscale particle image velocimetry. AIAA J 40(6):1047–1055

  44. Wierschem A, Aksel N (2004) Influence of inertia on eddies created in films creeping over strongly undulated substrates. Phys Fluids 16(12):4566–4574. doi:10.1063/1.1811673

  45. Wong GCL, O’Toole GA (2011) All together now: integrating biofilm research across disciplines. MRS Bull 36(5):339–345. doi:10.1557/mrs.2011.64

  46. Yawata Y, Toda K, Setoyama E, Fukuda J, Suzuki H, Uchiyama H, Nomura N (2010) Bacterial growth monitoring in a microfluidic device by confocal reflection microscopy. J Biosci Bioeng 110(1):130–133. doi:10.1016/j.jbiosc.2010.01.009

Download references

Acknowledgments

The authors would like to thank Dr. Alfred Spormann at Stanford University for providing the bacterial strains. A. Kumar performed the work as a Eugene P. Wigner Fellow at the Oak Ridge National Laboratory (ORNL). A portion of this research was conducted at the Center for Nanophase Materials Sciences, which is sponsored at ORNL by the Scientific User Facilities Division, US Department of Energy (US DOE). The authors acknowledge research support from the US DOE Office of Biological and Environmental Sciences. ORNL is managed by UT-Battelle, LLC, for the US DOE under contract no. DEAC05-00OR22725. The authors also acknowledge the Natural Sciences and Engineering Research Council of Canada for providing NSERC fellowship to Dr. Neethirajan.

Author information

Correspondence to Aloke Kumar.

Electronic supplementary material

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Kumar, A., Karig, D., Acharya, R. et al. Microscale confinement features can affect biofilm formation. Microfluid Nanofluid 14, 895–902 (2013). https://doi.org/10.1007/s10404-012-1120-6

Download citation

Keywords

  • Microfluidics
  • Biofilms
  • Secondary flows
  • Bacteria
  • Micro-vortices