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Lab on a Chip Lab on a Chip View Article Online PAPER View Journal On-chip integration of droplet microfluidics and nanostructure-initiator mass spectrometry for Cite this: DOI: 10.1039/c6lc01182a enzyme screening† Joshua Heinemann,ab Kai Deng,ac Steve C. C. Shih,f Jian Gao,b Paul D. Adams,abe Anup K. Singhac and Trent R. Northen*abd Biological assays often require expensive reagents and tedious manipulations. These shortcomings can be overcome using digitally operated microfluidic devices that require reduced sample volumes to automate assays. One particular challenge is integrating bioassays with mass spectrometry based analysis. Towards this goal we have developed μNIMS, a highly sensitive and high throughput technique that integrates drop- let microfluidics with nanostructure-initiator mass spectrometry (NIMS). Enzyme reactions are carried out in droplets that can be arrayed on discrete NIMS elements at defined time intervals for subsequent mass spectrometry analysis, enabling time resolved enzyme activity assay. We apply the μNIMS platform for ki- Received 20th September 2016, netic characterization of a glycoside hydrolase enzyme (CelE-CMB3A), a chimeric enzyme capable of Accepted 2nd December 2016 deconstructing plant hemicellulose into monosaccharides for subsequent conversion to biofuel. This study reveals NIMS nanostructures can be fabricated into arrays for microfluidic droplet deposition, NIMS is com- DOI: 10.1039/c6lc01182a patible with droplet and digital microfluidics, and can be used on-chip to assay glycoside hydrolase enzyme www.rsc.org/loc in vitro. reactions and is broadly applicable to many molecule classes Introduction – including metabolites, drugs and peptides,6,10 12 and has Enzymes are frequently engineered to modify their function been developed to rapidly analyse enzyme activities to sup- – or catalytic efficiency1 3 to increase product yields signifi- port the development of improved biomass degrading en- cantly through the use of directed evolution or rational pro- zymes.13 NIMS uses liquid (initiator) coated silicon nano- tein design.4,5 Mass spectrometry is a label-free detection structures to generate gas phase ions from surface adsorbed technique for measuring biochemical activity and has for molecules upon laser irradiation. Hence it lends itself to Published on 05 December 2016. Downloaded by Lawrence Berkeley National Laboratory 16/12/2016 19:27:32. some become the method of choice for high throughput as- microfabrication allowing biochemical reactions as low as 1 says.6,7 Unfortunately, the traditional mass spectrometry ap- nl of deposited sample. The use of acoustic printing with proaches for screening samples are slow and require large NIMS has shown much promise for large-scale screening ef- sample volumes often making them cost prohibitive for high forts, in vitro expression and analysis of enzyme activi- throughput screening efforts.8,9 ties.6,13,14 One limitation of this approach, is the dead- Nanostructure-initiator mass spectrometry (NIMS) is a la- volume required to print from 384-well plates is approxi- ser desorption/ionization approach that offers very high mately 20 μl making it expensive to perform large-scale throughput and requires very small amounts of samples. It screening. Since NIMS is fabricated from silicon based mate- directly measures the substrates and products of enzymatic rial, it is well suited for integration with microfluidics, offer- ing the potential to conduct assays in picoliter droplets which – greatly reduces cost and increases throughput potential.15 17 a Joint Bioenergy Institute, Emeryville, California 94608, USA There are numerous examples of integrated microfluidic/ b Lawrence Berkeley National Laboratory, Berkeley, California 94720, USA. mass spectrometry, from electrospray ionization (ESI) to ma- E-mail: trnorthen@lbl.gov 18,19 c Sandia National Laboratories, Livermore, California 94551, USA trix assisted laser desorption ionization (MALDI). Two d Joint Genome Institute, Walnut creek, California, 94598, USA such approaches show integration of MALDI with micro- e Department of Bioengineering, University of California, Berkeley, California, fluidics is useful for both peptide,20 and protein identifica- 94720, USA tion.21 Programmable control of digital microfluidic func- f Department of Electrical and Computer Engineering, Concordia University, Montreal, Quebec, Canada tions enables droplet operations, which are likely † Electronic supplementary information (ESI) available. See DOI: 10.1039/ improvements for enzymatic functional screening, because of 22–24 c6lc01182a electronic timing and control. Typical NIMS assays This journal is © The Royal Society of Chemistry 2016 Lab Chip View Article Online Paper Lab on a Chip require a washing step to remove cell debris which often in- ing the droplet to minimize ion suppression from salts – terferes with mass spectrometry analysis,15,25 using micro- etc.28 30 Recent applications show combined droplet and digi- fluidics could allow automated sample processing using tal microfluidics is suitable for programming diverse bio- electro-wetting on dielectric (EWOD), to automate this pro- chemical operations including genomic assembly, transfor- cess.26,27 In addition, integrated digital droplet devices have mation and culture.27,31 the potential to effectively array droplets onto the NIMS sur- Here we integrate microfluidics with NIMS in a platform face, adsorbing the substrates and products, and then remov- we refer to as μNIMS. μNIMS enables digital control of Published on 05 December 2016. Downloaded by Lawrence Berkeley National Laboratory 16/12/2016 19:27:32. Fig. 1 μNIMS assembly and operation. A. Electrode and fluidics design, layer iii. Inset: 1. t-junction, arrows show direction of flow, 2. μNIMS pocket, B. Digital microfluidics chip, compression sealed to the NIMS array, C. the stack for holding the layers together. i. 3D printed top, ii. PDMS mounting layer for interfacing fluidics to microfluidics, iii. Chip containing the electrodes, dielectric and fluidics, iv. NIMS chip, v. bottom piece with dropbot adapter, D. operation workflow E. Inject: chip is filled with droplets, load: flow is stopped and droplets are loaded onto the NIMS array for incubation and probe deposition, eject: the droplets are incubated for 10, 20, 30, and 40 minutes over six successive pads and then actuated into the central chamber where they are then evacuated, F. workflow of NIMS array removal and analysis. Lab Chip This journal is © The Royal Society of Chemistry 2016 View Article Online Lab on a Chip Paper enzymatic time course for cellulose-degrading enzyme using period of time, this allowed G4 to be converted and sorbed to NIMS as a biosensor. The chip moves droplets onto a NIMS NIMS pad (Fig. 1E., incubate). At the specified time intervals, surface, incubates and then removes after a defined period of droplets were ejected from the pocket (Fig. 1E., eject). The in- time. Probe sorbs to the NIMS surface allowing mass spectral cubation of the droplet over the pads on the NIMS array kinetic characterization of cellulose degrading enzymes. This allowed substrates and products to sorb from the droplet. technology is appealing because it has programmable time The digital actuation functioned to move droplets from the resolution, scalable density, and can be more broadly central chamber, in and out of the pocket containing the applied. NIMS active pad allowing substrate and product to sorb. This is consistent with the normal operation of NIMS. Droplets Results are loaded after pausing flow in this experiment, but demon- Integrated microfluidics-NIMS device strations show droplets can also be removed directly from flow if desired (Supplementary Video†). MS imaging of the μ The major design objective for the NIMS device was to de- silicon wafer after exposure to standard revealed that posit sample solutions at specified two-dimensional locations fluorous tagged substrates stay adsorbed onto the NIMS pads on the NIMS array in a time dependent manner. The micro- in our microfluidic environment when incubating the droplet fluidics chip consisted of chrome electrodes over a central flu- over a pad, similar to traditional NIMzyme execution.15 idics channel (Fig. 1). The chip contained two basic functions, a t-junction for droplet generation (Fig. 1A. 1.), and 31 digital NIMS array arrayers for droplet actuation over NIMS pads (Fig. 1A. 2.). 34 The t-junction used pressure driven flow to break aqueous en- NIMS pads are fabricated using photopatternable PDMS as 2 zyme/substrate plugs into droplets of approximately 150 nl a protective gasket over a laser cut silicon wafer (5 × 5cm) 16 using immiscible oil phase similar to previous demonstra- before reactive ion etching (DRIE) very similar to the origi- 35 tion.32 The chip contained glass substrate, chrome electrodes, nal design of desorption ionization on silicon surfaces. Ex- dielectric, and fluidics made the top of the stack for interfac- posure etches the silicon wafer to create surface nanostruc- ing with the NIMS array, which also functioned as a ground tures (Fig. 2B. and C.), for NIMS analysis. To test the ability plate during digital actuation (Fig. 1B.). The PDMS fluidics to deposit samples onto the NIMS pads and subsequently layer sealed reversibly to the NIMS array allowing selective perform mass spectrometry analysis, the metabolite standard, droplet actuation onto each NIMS pad (Fig. 1A.). The final de- dextromethorphan was used, where droplets were deposited sign loaded droplets
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