Abstract
The aim of this study was to utilize magnetic resonance imaging (MRI) to image structural heterogeneity and mass transport inside a biofilm which was too thick for photon based imaging. MRI was used to map water diffusion and image the transport of the paramagnetically tagged macromolecule, Gd-DTPA, inside a 2.5 mm thick cyanobacterial biofilm. The structural heterogeneity of the biofilm was imaged at resolutions down to 22 × 22 μm, enabling the impact of biofilm architecture on the mass transport of both water and Gd-DTPA to be investigated. Higher density areas of the biofilm correlated with areas exhibiting lower relative water diffusion coefficients and slower transport of Gd-DTPA, highlighting the impact of biofilm structure on mass transport phenomena. This approach has potential for shedding light on heterogeneous mass transport of a range of molecular mass molecules in biofilms.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Barranguet C, van Beusekom SAM, Veuger B, Neu TR, Manders EMM, Sinke JJ, Admiraal W (2004) Studying undisturbed autotrophic biofilms: still a technical challenge. Aquat Microb Ecol 34(1):1–9. doi:10.3354/ame034001
Bartacek J, Vergeldt FJ, Gerkema E, Jenicek P, Lens PNL, Van As H (2009) Magnetic resonance microscopy of iron transport in methanogenic granules. J Magn Reson 200(2):303–312. doi:10.1016/j.jmr.2009.07.013
Batstone DJ, Keller J (2001) Variation of bulk properties of anaerobic granules with wastewater type. Water Res 35(7):1723–1729. doi:10.1016/s0043-1354(00)00446-2
Bishop PL, Gibbs JT, Cunningham BE (1997) Relationship between concentration and hydrodynamic boundary layers over biofilms. Environ Technol 18(4):375–385. doi:10.1080/09593331808616551
Buffiere P, Steyer JP, Fonade C, Moletta R (1995) Comprehensive modeling of methanogenic biofilms in fluidized-bed systems: mass-transfer limitations and multisubstrate aspects. Biotechnol Bioeng 48(6):725–736. doi:10.1002/bit.260480622
Callaghan PT (1993) Principles of nuclear magnetic resonance microscopy. Oxford University Press, Oxford
deBeer D, Stoodley P, Lewandowski Z (1997) Measurement of local diffusion coefficients in biofilms by microinjection and confocal microscopy. Biotechnol Bioeng 53(2):151–158. doi:10.1002/(sici)1097-0290(19970120)53:2<151:aid-bit4>3.0.co;2-n
Debeer D, Stoodley P, Roe F, Lewandowski Z (1994) Effects of biofilm structures on oxygen distribution and mass-transport. Biotechnol Bioeng 43(11):1131–1138. doi:10.1002/bit.260431118
Gordon MJ, Chu KC, Margaritis A, Martin AJ, Ethier CR, Rutt BK (1999) Measurement of Gd-DTPA diffusion through PVA hydrogel using a novel magnetic resonance imaging method. Biotechnol Bioeng 65(4):459–467. doi:10.1002/(sici)1097-0290(19991120)65:4<459:aid-bit10>3.0.co;2-o
McLean JS, Ona ON, Majors PD (2008) Correlated biofilm imaging, transport and metabolism measurements via combined nuclear magnetic resonance and confocal microscopy. ISME J 2(2):121–131. doi:10.1038/ismej.2007.107
Paramonova E, De Jong ED, Krom BP, Van der Mei HC, Busscher HJ, Sharma PK (2007) Low-load compression testing: a novel way of measuring Biofilm thickness. Appl Environ Microbiol 73(21):7023–7028. doi:10.1128/aem.00935-07
Phoenix VR, Holmes WM (2008) Magnetic resonance imaging of structure, diffusivity, and copper immobilization in a phototrophic biofilm. Appl Environ Microbiol 74(15):4934–4943. doi:10.1128/aem.02783-07
Phoenix VR, Holmes WM, Ramanan B (2008) Magnetic resonance imaging (MRI) of heavy-metal transport and fate in an artificial biofilm. Miner Mag 72(1):483–486. doi:10.1180/minmag.2008.072.1.483
Ramanan B, Holmes WM, Sloan WT, Phoenix VR (2010) Application of paramagnetically tagged molecules for magnetic resonance imaging of biofilm mass transport Processes. Appl Environ Microbiol 76(12):4027–4036. doi:10.1128/aem.03016-09
Renslow RS, Majors PD, McLean JS, Fredrickson JK, Ahmed B, Beyenal H (2010) In situ effective diffusion coefficient profiles in live biofilms using pulsed-field gradient nuclear magnetic resonance. Biotechnol Bioeng 106(6):928–937. doi:10.1002/bit.22755
Rippka R, Deruelles J, Waterbury JB, Herdman M, Stanier RY (1979) Generic assignments, strain histories and properties of pure cultures of cyanobacteria. J Gen Microbiol 111 (MAR):1–61
Roeselers G, van Loosdrecht MCM, Muyzer G (2008) Phototrophic biofilms and their potential applications. J Appl Phycol 20(3):227–235. doi:10.1007/s10811-007-9223-2
Sirlin CB, Vera DR, Corbeil JA, Caballero MB, Buxton RB, Mattrey RF (2004) Gadolinium-DTPA-dextran: a macromolecular MR blood pool contrast agent. Acad Radiol 11(12):1361–1369. doi:10.1016/j.acra.2004.10.048
Stewart PS (1998) A review of experimental measurements of effective diffusive permeabilities and effective diffusion coefficients in biofilms. Biotechnol Bioeng 59(3):261–272. doi:10.1002/(sici)1097-0290(19980805)59:3<261:aid-bit1>3.0.co;2-9
Wieland A, de Beer D, Damgaard LR, Kuhl M, van Dusschote D, Van As H (2001) Fine-scale measurement of diffusivity in a microbial mat with nuclear magnetic resonance imaging. Limnol Oceanogr 46(2):248–259
Zhang TC, Bishop PL (1994) Evaluation of tortuosity factors and effective diffusivities in biofilms. Water Res 28(11):2279–2287. doi:10.1016/0043-1354(94)90043-4
Acknowledgments
This work was funded by a Lord Kelvin and Adam Smith Scholarship, University of Glasgow and funding from the Engineering and Physical Sciences Research Council (EP/G028443/1). We thank Jim Mullen for his assistance with RF coil building and MRI experiments.
Author information
Authors and Affiliations
Corresponding author
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Ramanan, B., Holmes, W.M., Sloan, W.T. et al. Magnetic Resonance Imaging of Mass Transport and Structure Inside a Phototrophic Biofilm. Curr Microbiol 66, 456–461 (2013). https://doi.org/10.1007/s00284-012-0292-3
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00284-012-0292-3