Source: UNIV OF MASSACHUSETTS submitted to NRP
SEPARATION OF PATHOGENS FROM FOOD MATRICES
Sponsoring Institution
National Institute of Food and Agriculture
Project Status
COMPLETE
Funding Source
AFRI COMPETITIVE GRANT
Reporting Frequency
Annual
Accession No.
1001323
Grant No.
2013-67017-21273
Cumulative Award Amt.
$495,950.00
Proposal No.
2013-02037
Multistate No.
(N/A)
Project Start Date
Sep 1, 2013
Project End Date
Aug 31, 2018
Grant Year
2013
Program Code
[A1331]- Improving Food Safety
Recipient Organization
UNIV OF MASSACHUSETTS
(N/A)
AMHERST,MA 01003
Performing Department
Food Science
Non Technical Summary
This Standard Research Grant proposal is in response to the USDA NIFA's AFRI Foundational Program A1331; "Physical and Molecular Mechanisms of Food Contamination". The separation of bacteria from a food sample remains the major obstacle for rapid detection. Although significant work has been performed in the area of rapid detection, these methods often require a concentrated clean sample. The field of rapid sample preparation has not received as much attention and therefore pre-enrichment of food samples remains the standard. If a reliable method for separation was developed, the time from analysis to results could be minimized resulting in a reduction in potential illness and costs. We have devised a method for bacterial separation using cobalt nanoparticles tagged with pathogen-specific bacteriophages. The uses of nanoparticles as compared to micro-scaled particles have previously demonstrated to have a significant increase in capture efficiency due to increased surface area. The binding affinity between phage and host has been demonstrated to be higher than that of antibodies allowing for a more reliable separation. The use of cobalt over iron allows for a much more rapid separation due to an increased magnetic pull. The ability to continuously collect samples from grains and nuts would be a tremendous benefit to their respective industries. We have developed a continuous sampling system designed to collect samples from the products as they transport on a conveyor. The system will pull the fines from interstitial spaces around the product and filter it. The particles are then pulled into a wetted cyclone which produces a 5 mL buffered sample.
Animal Health Component
30%
Research Effort Categories
Basic
20%
Applied
30%
Developmental
50%
Classification

Knowledge Area (KA)Subject of Investigation (SOI)Field of Science (FOS)Percent
71250101100100%
Knowledge Area
712 - Protect Food from Contamination by Pathogenic Microorganisms, Parasites, and Naturally Occurring Toxins;

Subject Of Investigation
5010 - Food;

Field Of Science
1100 - Bacteriology;
Goals / Objectives
This Standard Research Grant proposal is in response to the USDA NIFA's AFRI Foundational Program A1331; "Physical and Molecular Mechanisms of Food Contamination". The separation of pathogens from a food matrix remains the major obstacle for rapid detection. Although significant work has been performed in the area of rapid detection, these methods often require a concentrated clean sample. The field of rapid sample preparation has not received as much attention and therefore pre-enrichment of food samples remains the standard. If a reliable method for separation was developed, the time from analysis to results could be minimized resulting in a reduction in potential illness and costs. We have devised a method for bacterial separation using cobalt nanoparticles tagged with pathogen-specific bacteriophages. The uses of nanoparticles as compared to micro-scaled particles have previously demonstrated to have a significant increase in capture efficiency due to increased surface area. The binding affinity between phage and host has been demonstrated to be higher than that of antibodies allowing for a more reliable separation. The use of cobalt over iron allows for a much more rapid separation due to an increased magnetic pull. The ability to continuously collect samples from grains and nuts would be a tremendous benefit to their respective industries. We have developed a continuous sampling system designed to collect samples from the products as they transport on a conveyor. The system will pull the fines from interstitial spaces around the product and filter it. The particles are then pulled into a wetted cyclone which produces a 5 mL buffered sample. 1. Objective 1: Screening of bacteriophage for high binding kinetics/affinity and specificity. Although acceptable phages have already been identified, additional screening of phages for will improve the performance of the separation step in Objective 2. Phages for Salmonella, Listeria, and E. coli will be screened for cross reactivity with related and ubiquitous organisms. 2. Objective 2: Separation from wet foods using nanoparticles and bacteriophage; the bacteriophages which we have already screened will be covalently immobilized to magnetic cobalt nanoparticles. Using the nanoparticles, we will separate Salmonella, Listeria and E. coli from unpasteurized whole milk and produce rinse water and determine the increase in capture efficiency over micron scale particles. 3. Objective 3: An aerosol-based separation from dry foods; Using a wetted cyclone continuous filtration system, we will collect headspace over ready-to-eat breakfast cereal (containing Listeria and E. coli). The particles are continuously filtered by particle size and then placed into a buffer solution. The bacteriophage-nanoparticle system will then be used on the wet collected sample to determine capture efficiency.
Project Methods
Objective 1: Screening of bacteriophage for high binding kinetics/affinity and specificity. Although acceptable phages have already been identified, additional screening of phages for will improve the performance of the separation step in Objective 2. Phages for Salmonella, Listeria, and E. coli will be screened for cross reactivity with related and ubiquitous organisms. Although usable phages have already been identified, additional screening of phages for E. coli, Salmonella, and Listeria will identify those with optimal specificity, burst size and cycle time. Specificity tests will be conducted using plaque assays and binding constants will be determined with Surface Plasmon Resonance (SPR). Objective 2: Separation from wet foods using nanoparticles and bacteriophage. During this objective, a method for the separation of pathogens from an aqueous sample will be developed and optimized. The bacteriophages which we have already screened will be covalently immobilized to magnetic cobalt nanoparticles. We have demonstrated this principle with micron scale particles already. Using the nanoparticles, we will separate Salmonella, Listeria and E. coli from unpasteurized whole milk and produce rinse water to determine the increase in capture efficiency over micron scale particles. Objective 3: An aerosol-based separation from dry foods. An aerosol-based separation from dry foods; Using a wetted cyclone continuous filtration system, we will collect headspace over ready-to-eat breakfast cereal (containing Listeria and E. coli). The process will simulate cereal being transported in a plant. The particles will be continuously filtered by size and then placed into a buffer solution. The both the bacteriophage-nanoparticle system will then be used to separate the bacteria from the buffer sample. The separated complex can then be separated on differential media.

Progress 09/01/13 to 08/31/18

Outputs
Target Audience:During this reporting period, we have participated in several oral and poster presentations. This includes several very relevant conferences including Pittcon and American Chemical Society. Additionally, the technology has garnered interest from industry and we have been advising those partners on technical aspects of the project to allow for commercialization. Our target auditnce has been scientists working in the field of food safety, especially those developing tools to rapidly detect bacteria. Changes/Problems: Nothing Reported What opportunities for training and professional development has the project provided?In addition to the research learning provided from this project, students and staff have been working on their scientific communication skills. We have identified this as a weakness of many students and therefore have put together a monthly podcast where our students summerize recent publications in Food Microbiology. The Podcast is called "Food Micro Minutes" and requires students to read current literature, summerize it, and then write a script allowing the papers to be explained in approximately 5 minutes. We have noted a significant improvement in their ability to communicate scientific principles without visual aids. How have the results been disseminated to communities of interest?We have used several methods to communicate the progress of this project. In addition to both international and national presentations, the work have been covered in several popular press articles such as Forbes, Science Daily, Science News and trade magazines such as Chemical & Engineering News. What do you plan to do during the next reporting period to accomplish the goals? Nothing Reported

Impacts
What was accomplished under these goals? During this reporting peiod, we have developed two advanced methods to engineer bacteriophages using either 1) CRISPR or 2) PCR fragments followed by in vitro DNA assembly. These methods were developed in order to better allow us to improve the host range of phages and quantify the binding kinetics of tail fiber types. We have made significant improvements in the ability to bind bacteriophages to magnetic nanoparticles (report in preparation) using a much lower lost method. Although effective, our previous method which utilized biotin-streptavidin binding, required the used of costly streptavidin-coated magnetic perticles. We have also made significant efforts to increase the sample size of the starting matrix. We have successfully used 100 mL samples of water using a filter based method. This has allowed us to improve the final detection limit of E. coli to 1-10 CFU/100 mL. These types of improvement in sensitivity allow the products of this project to more rapidly approach commercialization.

Publications

  • Type: Journal Articles Status: Published Year Published: 2018 Citation: Hinkley TC, Singh S, Garing S, et al. A phage-based assay for the rapid, quantitative, and single CFU visualization of E. coli (ECOR #13) in drinking water. Scientific Reports 2018; 8(1): 14630.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2018 Citation: Hinkley, Troy, Joey Talbert, and Sam Nugen. "Phage-based biosensors for rapid testing of agricultural and process water." ABSTRACTS OF PAPERS OF THE AMERICAN CHEMICAL SOCIETY. Vol. 256. 1155 16TH ST, NW, WASHINGTON, DC 20036 USA: AMER CHEMICAL SOC, 2018.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2018 Citation: Zurier, Hannah, Julie Goddard, and Sam Nugen. "Engineering a click-functional T7 bacteriophage for rapid pathogen detection." ABSTRACTS OF PAPERS OF THE AMERICAN CHEMICAL SOCIETY. Vol. 256. 1155 16TH ST, NW, WASHINGTON, DC 20036 USA: AMER CHEMICAL SOC, 2018.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2018 Citation: Hinkley, Troy, Joey Talbert, and Sam Nugen. "Phage-based lab-on-a-filter for the rapid, quantitative, and single cell detection of E. coli in drinking water." ABSTRACTS OF PAPERS OF THE AMERICAN CHEMICAL SOCIETY. Vol. 256. 1155 16TH ST, NW, WASHINGTON, DC 20036 USA: AMER CHEMICAL SOC, 2018.
  • Type: Journal Articles Status: Published Year Published: 2018 Citation: Hinkley TC, Singh S, Garing S, et al. Reporter bacteriophage T7NLC utilizes a novel NanoLuc::CBM fusion for the ultrasensitive detection of Escherichia coli in water. Analyst 2018; 143: 9.
  • Type: Journal Articles Status: Submitted Year Published: 2018 Citation: Wang D, Hinkley TC, Chen J, Talbert JN, Nugen SR. Engineered-phage based electrochemical detection of Escherichia coli in drinking water using affinity reporter probes. 2018 Submitted
  • Type: Journal Articles Status: Submitted Year Published: 2018 Citation: Pulkkinen EM, Hinkley TC, Nugen SR. Engineering of bacteriophages using in vitro DNA assembly and creating a T7 Nanoluc reporter phage for Escherichia coli detection. 2018 Submitted
  • Type: Journal Articles Status: Published Year Published: 2017 Citation: Chen J, Picard RA, Wang D, Sam R. N. Lyophilized Engineered Phages for Escherichia coli Detection in Food Matrices. ACS Sensors 2017; 2(11): 5.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2018 Citation: Nugen SR. Designing First Generation Nanobots for Food Safety via Phage Engineering. PITTCON, Orlando, FL


Progress 09/01/16 to 08/31/17

Outputs
Target Audience:During this reporting period, we have participated in several oral and poster presentations. This includes several very relevant conferences including The International Association for Food Protection, American Chemical Society, and the BioDefense World Summit. Additionally, the technology has garnered interest from industry and we have been advising those partners on technical aspects of the project to allow for commercialization. Changes/Problems: Nothing Reported What opportunities for training and professional development has the project provided?Similar to the previous reporting period, several graduate students have been working under this project. The combination of practical and applied research along with opportunities for oral and poster presentations has been beneficial for their development as scientists. Additionally, the students have received significant exposure to communicating and collaborating directly with industry partners. As a result, two of the recently graduated Ph.D. students received faculty position offers prior to receiving their degree. This suggests a high degree of preparation and development. How have the results been disseminated to communities of interest?Similar to the previous period, the results of the projects have been disseminated to several communities through multiple mechanisms. While students and faculty have made several oral presentations through both invited and applied talks, press releases have allowed a wider distribution of the results. In addition, we have met with several companies who are interested in developing these technologies. Additionally, Professor Nugen spent 6 months in Copnhagen, Denmark working with another bacteriophage lab. The purpose of the trip was to share techniques and knowledge. What do you plan to do during the next reporting period to accomplish the goals?In the next reporting period, we hope to be executing objective 3. The discussions with the collaborating company are closer. This agreement needs to be finalized with Cornell University.

Impacts
What was accomplished under these goals? We hve been developing models to predict phage/host specificity. This will allow more specific binding and separation of bacteria. In order to do this, we have been developing a phage scaffold which can allow the facile swapping of tail fibers from other phages. We have also been investigating a more low-cost and pragmatic method for the conjugation of phages to nanoparticles using "click" chemistry. This is facilitated by the use of unnatural amino acids. Additionally, we have been looking at the combination of phage-based separation and detection of bacteria.

Publications

  • Type: Journal Articles Status: Awaiting Publication Year Published: 2017 Citation: Chen J, Picard RA, Wang D, Nugen SR. Lyophilized Engineered Phages for Escherichia coli Detection in Food Matrices. ACS Sens. 2017 Oct 20. doi: 10.1021/acssensors.7b00561.
  • Type: Journal Articles Status: Published Year Published: 2017 Citation: Chen J, Alcaine SD, Jackson AA, Rotello VM, Nugen SR. Development of Engineered Bacteriophages for Escherichia coli Detection and High-Throughput Antibiotic Resistance Determination. ACS Sens. 2017 Apr 28;2(4):484-489. doi: 10.1021/acssensors.7b00021.
  • Type: Journal Articles Status: Published Year Published: 2017 Citation: Wang D, Chen J, Nugen SR. Electrochemical Detection of Escherichia coli from Aqueous Samples Using Engineered Phages. Anal Chem. 2017 Feb 7;89(3):1650-1657. doi: 10.1021/acs.analchem.6b03752
  • Type: Journal Articles Status: Published Year Published: 2016 Citation: Koo CK, Senecal K, Senecal A, Nugen SR. Dehydration of bacteriophages in electrospun nanofibers: effect of excipients in polymeric solutions. Nanotechnology. 2016 Dec 2;27(48):485102.
  • Type: Journal Articles Status: Published Year Published: 2016 Citation: Chen J, Pang S, He L, Nugen SR. Highly sensitive and selective detection of nitrite ions using Fe3O4@SiO2/Au magnetic nanoparticles by surface-enhanced Raman spectroscopy. Biosens Bioelectron. 2016 Nov 15;85:726-733. doi: 10.1016/j.bios.2016.05.068.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2017 Citation: Emma Farquharson, Nugen, SR. "Bacteriophage engineering for the onsite detection of pathogens and indicators". Oral Presentation. June 27th, 2017. BioDefense World Summit conference 2017. Alexandria, VA.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2017 Citation: Emma Farquharson and Troy Hinkley. "A Cautionary Tale: The Dark Side of Food Outbreaks". Oral Presentation. May 25th, 2017. CYNAFP Conference.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2017 Citation: Hinkley, TC; Nugen SR.�Recombinant bacteriophages serve as sensitive bacterial recognition elements" 253rd American Chemical Society Annual Meeting. April 2-6 2017. San Francisco, CA.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2017 Citation: Wang, D., Nugen, SR.Improvement of bacteria separation from leaf vegetables by enzymatic digestion, 2017 IAFP Annual Meeting. Tampa, FL


Progress 09/01/15 to 08/31/16

Outputs
Target Audience:During this reporting period, we have participated in several oral and poster presentations. This includes several very relevant conferences including The International Association for Food Protection, American Chemical Society, and the International Association of Environmental Analytical Chemistry (IAEAC). Additionally, the technology has garnered interest from industry and we have been advising those partners on technical aspects of the project to allow for commercialization. ? Changes/Problems: Nothing Reported What opportunities for training and professional development has the project provided?Several graduate students have been working under this project. The combination of practical and applied research along with opportunities for oral and poster presentations has been beneficial for their development as scientists. Additionally, the students have received significant exposure to communicating and collaborating directly with industry partners. As a result, two of the recently graduated Ph.D. students received faculty position offers prior to receiving their degree. This suggests a high degree of preparation and development. How have the results been disseminated to communities of interest?The results of the projects have been disseminated to several communities through multiple mechanisms. While students and faculty have made several oral presentations through both invited and applied talks, press releases have allowed a wider distribution of the results. In addition, we have met with several companies who are interested in developing these technologies. ? What do you plan to do during the next reporting period to accomplish the goals?In the next reporting period, we will be executing objective 3. The discussions with the collaborating company are currently underway.

Impacts
What was accomplished under these goals? We have completed objective 1 and identified appropriate bacteriophages. We currently have numerous bacteriophages targeting E. coli, Listeria, and Salmonella. We have also identified host ranges for some of the phages. We have Performed bacteria-based separation using magnetic beads. A comparison was made between nano and micro-scale beads and the nanoparticles were identified and superior. Additionally, a comparison was made between magnetic beads with attached phages and commercially available magnetic beads with antibodies. The results indicated the phages are superior in the capturing of E. coli. This is especially true when separating the bacteria from liquid samples which are outside biological conditions. Therfore, the majority of Objective 2 has also been demonstrated. We are currently waiting on our collaborator (Hollison Technologies) for objective 3.

Publications

  • Type: Journal Articles Status: Published Year Published: 2016 Citation: Chen J, Jackson AA, Rotello VM, Nugen SR. Colorimetric Detection of Escherichia coli Based on the Enzyme-Induced Metallization of Gold Nanorods. Small 2016; 12(18): 2469-75.
  • Type: Journal Articles Status: Published Year Published: 2015 Citation: Chen J, Duncan B, Wang Z, Wang L-S, Rotello VM, Nugen SR. Bacteriophage-based nanoprobes for rapid bacteria separation. Nanoscale 2015; 7(39): 16230-6.
  • Type: Journal Articles Status: Published Year Published: 2016 Citation: Wang Z, Wang D, Kinchla AJ, Sela DA, Nugen SR. Rapid screening of waterborne pathogens using phage-mediated separation coupled with real-time PCR detection. Anal Bioanal Chem 2016; 408(15): 4169-78.
  • Type: Journal Articles Status: Published Year Published: 2016 Citation: Wang Z, Wang D, Chen J, Sela DA, Nugen SR. Development of a novel bacteriophage based biomagnetic separation method as an aid for sensitive detection of viable Escherichia coli. Analyst 2016; 141(3): 1009-16.
  • Type: Journal Articles Status: Published Year Published: 2015 Citation: Chen J, Alcaine SD, Jiang Z, Rotello VM, Nugen SR. Detection of Escherichia coli in Drinking Water Using T7 Bacteriophage-Conjugated Magnetic Probe. Analytical Chemistry 2015; 87(17): 8977-84.


Progress 09/01/14 to 08/31/15

Outputs
Target Audience:Our target audience has been a combination of undergraduate, graduate and visiting students. We have setup a tiered mentorship program for the students to enhance their research experience. Graduate students are given the added resposibilities of guiding undergraduates through research projects. All students are expacted to present their work both locally and nationally Changes/Problems:Our major challenge has been completion of the aerosolization device from the collaborating compay. This should be oversome soon as the device is finalized. What opportunities for training and professional development has the project provided?We have sent 5 graduate students to intnational conferences in order to present their findings. These oral talks are considered extremely important for the development of our scientists.One graduatre student won the graduate Student Oral competition at the Anual ACS meeting. While another won the Department oral competition. In addition, our graduate students have been involved in mentoring for undergraduate students in order to prepare them for furure leadership roles. A student who worked on this grant just received a faculty position offer prior to completion of his Ph.D. This is good evidence of the students preparation. How have the results been disseminated to communities of interest?We have sent 5 graduate students to intnational conferences in order to present their findings. One graduatre student won the graduate Student Oral competition at the Anual ACS meeting. What do you plan to do during the next reporting period to accomplish the goals?We will durther develop the aerosolization experiments. The collaborating company has been finishing manufacturing optimization and the instrument is soon to be finalized.

Impacts
What was accomplished under these goals? Objective 1: We have compared a comparison of the separation efficienciies when using bacteriophages on magnetic nanoparticles vs. magnetic microparticles.We have developed nanoscale bacteriophage-tagged magnetic probes, where T7 bacteriophages were bound to magnetic nanoparticles. The nanoprobe allowed the specific recognition and attachment to E. coli cells. The phage magnetic nanprobes were directly compared to antibody-conjugated magnetic nanoprobes. The capture efficiencies of bacteriophages and antibodies on nanoparticles for the separation of E. coli K12 at varying concentrations were determined. The results indicated a similar bacteria capture efficiency between the two nanoprobes. Objective 2:Here, we report a novel bacteriophage mediated detection of E. coli O157:H7 which utilizes the specific recognition between phages and their host cell as well as the natural lysis component of the infection cycle for DNA release. Carboxylic acid functionalized magnetic beads were conjugated with bacteriophage and used to separate and concentrate E. coli O157:H7. The effects of bead incubation time, salinity, pH and temperature on the bio-magnetic separation were investigated and compared to an antibody-based counterpart. The conditions of 0.01M PBS, pH 7.0 and 20 minutes of reaction at 37 °C were found to be optimal. The capture efficiency of the coupled assay was approximately 20% higher than that of antibody based separation under extreme conditions. The resulting bead-phage-bacteria complexes were quantitatively detected by following real-time PCR (qPCR). Our results demonstrated that the use of phage-based magnetic separation coupled with qPCR improved the sensitivity of detection by 2 orders of magnitude compared that without phage-based pre-concentration. Specificity and selectivity of the assay system were evaluated and no cross-reactivity occurred when Salmonella typhimurium, Staphylococcus aureus and Pseudomonas aeruginosa were tested. The total assay time was less than 2 hours.? Objective 3: In preparation

Publications

  • Type: Journal Articles Status: Published Year Published: 2016 Citation: Wang, Z., Wang, D., Chen, J., Sela, D.A., Nugen, S.R. Development of a Novel Bacteriophage Based Biomagnetic Separation Method as an Aid for the Sensitive Detection of Viable Escherichia coli 2015 Analyst. 141(3) 1009-1016
  • Type: Journal Articles Status: Published Year Published: 2015 Citation: Chen, J., Alcaine, S.D., Ziwen, J., Rotello, V.M., Nugen, S.R. Detection of Escherichia coli in Drinking Water Using T7 Bacteriophage-conjugated Magnetic Probes 2015 Analytical Chemistry 87(17), 8977-8984
  • Type: Journal Articles Status: Published Year Published: 2015 Citation: Chen, J., Duncan, B., Wang, L., Rotello, V.M., Nugen, S.R. Bacteriophage-based nanoprobes for rapid bacteria separation 2015 Nanoscale 7(30), 16230-16236. DOI: 10.1039/C5NR03779D.
  • Type: Journal Articles Status: Awaiting Publication Year Published: 2016 Citation: Wang, Z., Wang, D., Kinchla, A.J., Sela, D.A., Nugen, S.R. "Rapid screening of waterborne pathogens using phage-mediated separation coupled with real time PCR detection" Analytical & Bioanalytical Chemistry (Accepted)


Progress 09/01/13 to 08/31/14

Outputs
Target Audience: Our target audience has been a combination of undergraduate, graduate and visiting students. We have setup a tiered mentorship program for the students to enhance their research experience. Graduate students are given the added resposibilities of guiding undergraduates through research projects. All students are expacted to present their work both locally and nationally. Changes/Problems: The creation of "ghost phages" for separation has resulted in some damage tot he tail fibers and we are therefore investigating the use of engineered phages as a silumtaneous strategy. What opportunities for training and professional development has the project provided? The students funded have both presented their research at international meetings (Gordon Research Conference). The PI's have worked with both students on writing and research methods to improve their techncal abilities. Both students have seen significant improvements in both their oral and written abilities. How have the results been disseminated to communities of interest? The students funded have both presented their research at international meetings (Gordon Research Conference). Additionally, both have written or are currently in the process of writing manuscripts to report their findings. What do you plan to do during the next reporting period to accomplish the goals? We are continuing to optimize the nanoparticles for separation. In addition, we are engineering bacteriophages to allow attachement without infection. This method will improve the ability to separate without lysing the bacterial cell. During the next year we also plan to begin the headspace collector work outlined in the objectives.

Impacts
What was accomplished under these goals? While we are still screening bacteriophages from objective 1, we have been successfully separating bacteria from food samples as outlined in objective 2. This process is now being optimized but has demonstrated significant improvement over the current standard of Immuno Magnetic Separation (IMS).

Publications

  • Type: Journal Articles Status: Submitted Year Published: 2014 Citation: Chen, J., Duncan, B., Wang, L., Rotello, V.M., Nugen, S.R. Rapid Separation of Bacteria Using Phage Affinity and Magnetic Nanoparticles 2014
  • Type: Conference Papers and Presentations Status: Published Year Published: 2014 Citation: Chen, J., Duncan, B., Wang, L., Rotello, V.M. Nugen, S.R. "Rapid Separation of Bacteria Using Phage Affinity and Magnetic Nanoparticles" Gordon Research Conference, 2014 Newport, RI