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DAMICO-DISSERTATION-2014.Pdf Copyright by Lorenzo D’Amico 2014 The Dissertation Committee for Lorenzo D’Amico Certifies that this is the approved version of the following dissertation: Isolation of Microorganisms from Biological Specimens by Dielectrophoresis Committee: Peter R.C. Gascoyne, supervisor James Bankson, co-supervisor Javier A. Adachi Andrew Dunn Al Bovik Isolation of Microorganisms from Biological Specimens by Dielectrophoresis by Lorenzo D’Amico, B.S., M.S.E. Dissertation Presented to the Faculty of the Graduate School of The University of Texas at Austin in Partial Fulfillment of the Requirements for the Degree of Doctor of Philosophy The University of Texas at Austin May 2014 Acknowledgements This work was possible only through the efforts of so many people. I want to recognize my family for their unconditional love through this journey, and taught me that fortune favors the bold. My mentor and friend, Peter RC Gascoyne, offered far more than guidance; he gave me a world-class laboratory, complete with pre-historic electronics and blood-stained pumps. He taught me so much about science and about life. I cannot think of a better place to begin a career in bioengineering research. I owe so much to Javier Adachi. When not saving lives, Javier made time to help me understand the real challenges that clinicians face in managing infections. I want to acknowledge others in the lab: Fred Becker, Tom Anderson, Jamileh Noshari, Sangjo Shim, and Jason Haber for all the help they offered during my studies. I want to thank Mia Markey and Gary Rylander for awarding me the NIBIB Imaging Sciences training grant. The Whitaker Foundation sponsored my research in England, and for that I am very grateful. With their support, I had the chance to work with Hywel Morgan, who offered his excellent facilities and guidance. I would also like the thank the following who, in no specific order, contributed significantly to my doctoral training: Antonio Ramos, Pablo Garcia- Sanchez and Juan Arcenegui, Maria-Nefeli Tsaloglou, Katie Chamberlian, Santosh Devanallikar, Jeff Tarrand, Jason Sakamoto, Alex Lupulescu, and Leslie Silva. Nadim Ajami, Joseph Petrosino, Suzanne Kennedy and others at CMMR helped me complete my research and for that I am very grateful. I cannot forget all my friends in California, especially suite 400, and my good friends in Houston, including Henry Osorio, everyone from Casa Colquitt, Tio Odilon, and Joel Sturgeon. I want to recognize Laura Chen for her love and energy that helped me to finish these studies. I am indebted to those noted above. I take full responsibility for any errors or omissions in this work. iv Isolation of Microorganisms from Biological Specimens by Dielectrophoresis Lorenzo D’Amico, PhD The University of Texas at Austin, 2014 Supervisor: Peter R. C. Gascoyne Co-supervisor: James Bankson Every environment of the biosphere supports a particular mix of microorganisms called a microbiome. These diverse microbial communities play critical roles in the health of ecosystems and in higher organisms, including humans. Disruption or translocation of microbiomes may cause lethal infections, contaminate food and drug supplies, and adversely impact industrial activities. Microbiome detection and molecular characterization have emerged as priorities in many fields. Available methods cannot quickly and efficiently extract rare microorganisms in real specimens. Therefore, microbial detection and analysis require long incubation periods or the use of technically challenging molecular biotechnologies. These strategies are impractical in situations requiring immediate intervention. The intrinsic electric and dielectric properties of microbes permit their isolation by the phenomenon of dielectrophoresis in microfluidic devices. These microsystems have the potential to enhance microbial analysis but are plagued by low processing rates and the inability to interface with biological specimens containing high levels of interfering cells and debris. In this study, a method was created to discriminate between v target microbes and undesired cells on the basis of their differential susceptibility to permeabilizing agents that altered cell dielectrophoretic responses. Fabrication techniques were developed to manufacture high-aspect ratio microfluidic channels that allowed the physical forces of gravity, diffusion and dielectrophoresis to be exploited to control cell positions over microscale distances normal to a Poiseuille flow gradient. Because the positioning effects were exploited in only one dimension, the other two dimensions of the channels could be scaled up to create large channel cross-sectional areas that supported rapid specimen processing rates while maintaining high separation efficiencies expected for the microscale effects. These strategies were applied in various ways to isolate microbes from whole blood, platelets, stool, saliva, and skin specimens. The dielectrophoretic extraction of microbes enabled by this approach was used to enable electrical impedance detection of ~100 bacteria in less than five hours. As a result, important technological barriers that have limited the applicability of dielectrophoresis in clinical and industrial settings were overcome by increasing throughput and addressing sample preparation requirements. These proof-of-concept data demonstrate the potential for accelerating microbial isolation and detection in diagnostics, screening, and microbiome research. vi Table of Contents List of Tables ...........................................................................................................x List of Figures ........................................................................................................ xi INTRODUCTION ........................................................................................................1 Chapter 1: Electronic and dielectric properties of microorganisms ......................33 Fundamental aspects of electrodynamics......................................................34 Electromagnetic fields in media: magnetization, polarization and conduction ...................................................................................37 Quasi-electrostatic approximation .......................................................41 Electrical polarization in biological matter ...................................................43 Submolecular bioelectronics ................................................................44 Electrical polarization phenomena in biological cells .........................50 Interfacial polarization ................................................................51 Surface conduction effects ..........................................................57 Bioelectrics of microorganisms ....................................................................65 Dynamics of bioelectrical phenomena in microbes ......................................79 Stratified shell models for cells...................................................86 Concluding remarks ......................................................................................98 Chapter 2: Dielectrophoretic isolation of microorganisms ..................................100 Microelectrode designs and analysis .................................................110 Dielectrophoretic manipulation of bacteria .......................................121 Practical limitations of continuous-mode dielectrophoresis .......................130 Particle motive forces ........................................................................132 Electrophoresis ..........................................................................133 Gravity ......................................................................................134 Brownian motion ......................................................................136 Particle interactions ...................................................................139 Fluid motive forces at the microscale ................................................146 vii Hydrodynamic drag force .........................................................150 Hydrodynamic lift forces ..........................................................155 Enhancing DEP manipulation by geometric scaling ................160 Electrothermal effects ........................................................................167 Electrohydrodynamics ..............................................................187 Electrical power considerations .........................................................196 Fabrication and testing of a high-throughput DEP device ..........................202 Concluding remarks ....................................................................................212 Chapter 3: Sample preparation strategies for dielectrophoresis ..........................216 Selective alteration of the dielectrophoretic response of cells ....................217 Deionization to enable dielectrophoretic separation ...................................228 Microfluidic, membrane-less dialysis ................................................229 Modeling solute transport in membraneless dialysis ................231 A microfluidic, membraneless dialysis system .........................238 Scale up of the membraneless dialysis stage ............................245 Preliminary testing of the scaled up dialysis device .................254 Differential sedimentation ..........................................................................259 Concluding remarks ....................................................................................269
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