Source: UNIV OF WISCONSIN submitted to NRP
ENGINEERED BACTERIOPHAGES AS BIOCONTROL AGENTS AGAINST FOODBORNE PATHOGENS
Sponsoring Institution
National Institute of Food and Agriculture
Project Status
COMPLETE
Funding Source
Reporting Frequency
Annual
Accession No.
1017523
Grant No.
(N/A)
Cumulative Award Amt.
(N/A)
Proposal No.
(N/A)
Multistate No.
(N/A)
Project Start Date
Oct 22, 2018
Project End Date
Oct 31, 2021
Grant Year
(N/A)
Program Code
[(N/A)]- (N/A)
Recipient Organization
UNIV OF WISCONSIN
21 N PARK ST STE 6401
MADISON,WI 53715-1218
Performing Department
Biochemistry
Non Technical Summary
Despite technological advances, microbial contamination is constant threat to the food industry. Over 50 million cases of food poisoning occurs in the United States annually, resulting in over a 100,000 hospital visits and several thousand fatalities. Cooking usually kills most pathogens. However, changes in lifestyle have increased demand for processed and ready-to-eat food, increasing the chances of food-borne pathogens. Processed meat, poultry, vegetables and dairy are carriers of common food-borne pathogens such as Salmonella, Listeria, Campylobacter and Escherichia and have been subject to product recalls several times in recent years. Besides health and well-being, microbial contamination also plays a major role in spoilage of food which is estimated at a staggering 40% of all food produced, adding a huge financial burden. As food travels increasing longer distances from farm to fork, the food industry is facing the challenge of ensuring product quality and shelf life over longer time frames. The threat of microbial contamination is highly exacerbated by the emergence of antibiotic resistant strains. Solving the antibiotic resistance crisis is one of the grand challenges of our time.We need to fundamentally rethink our approach to treating bacterial contamination. Ideally, we seek an antimicrobial solution that transcends these limitations and co-evolves with bacteria to remain effective as bacteria eventually evolve resistance to antibiotic drugs. Nature provides an elegant solution: bacteriophages (or 'phages'). Phages are viruses that specifically invade and destroy bacteria without harming eukaryotic cells. Discovered in 1915, phages were immediately recognized for their therapeutic potential and used to fight infectious diseases (i.e., 'phage therapy'), most notably in Eastern Europe. The arrival of penicillin--the first safe antibiotic in the late 1930's--was followed by a series of other molecular antibiotic discoveries that dampened interest in phage-based treatment of bacterial infections in humans. The availability of multiple new classes of antibiotics in the following decades enabled physicians to treat infections with a new class of antibiotics when the current drug was deemed ineffective. However, this is no longer sustainable. This research to bring phages to the forefront of antimicrobials agents against food-borne pathogens. By doing so, we will develop a broad technology platform for designing customized phages to kill pathogenic microbes using synthetic biology tools.
Animal Health Component
60%
Research Effort Categories
Basic
20%
Applied
60%
Developmental
20%
Classification

Knowledge Area (KA)Subject of Investigation (SOI)Field of Science (FOS)Percent
71240991100100%
Goals / Objectives
The objective of this research is to bring phages to the forefront of antimicrobials agents against food-borne pathogens. We will develop a broad technology platform for designing customized phages to kill pathogenic microbes using synthetic biology tools. As a proof-of-principle, we will design phages specifically against E. coli O157:H7 which is a enterohemorrhagic strain resident in ruminant animals. The beauty of our approach is that it can be broadly applied to kill other pathogens as well. Engineered phages can also be used for microbiome editing, pathogen detection, gene delivery and biofilm disruption.Aims: 1) To develop a yeast-based system to assemble recombinant phage genomes2) To modulate T7 phage host range by high-throughput tail fiber protein redesign3) To improve efficacy of engineered T7 phages and minimize bacterial resistance
Project Methods
Aim 1) To develop a yeast-based system to assemble recombinant phage genomesPhage infection is initiated by the phage adsorbing on to the surface of the host bacteria. The tail fiber protein at the distal tip of a phage plays a central role in host recognition and specificity. To engineer phages, we need a facile method to assemble new phage genomes. Bacteria are an unsuitable host for assembling obligate lytic phage genomes because the assembled phage particles would lyse the host. Homologous recombination in yeast has been used to assemble large pathways, and phage genomes. We are developing yeast as a non-infectable cloning host to assemble phage genomic libraries. Using a yeast-bacteria shuttle vector we assemble and store the genomic libraries in yeast. Phages can be subsequently "rebooted" by transfer into a susceptible host, like E. coli. Our initial results suggest that we can assemble a T7 phage genome (~40kb) by assembling eight 5kb fragments in yeast. Our preliminary data shows that approximately 40% of the yeast colonies (out 30 screened colonies) are positive based on a PCR screen of a single junction of the fragments.Aim 2) To modulate T7 phage host range by high-throughput tail fiber protein redesignWe show that a T7 phage whose native tail fiber is replaced with that of a T3 phage, adopts the host range of a T3 phage. Having established that the tail fiber is necessary and sufficient to switch host specificity (for the strains tested), we hypothesize that T7 could be made to infect non-native hosts by redesigning or replacing its tail fiber with variants that can adsorb on other hosts. We propose to develop a process we call host-agnostic propagation to facilitate creation of large amounts of designer phage with alternative tail fibers. Designer phages will be genetically engineered to include an operator to allow in trans repression. The genome of the designer phage will then be electroporated into 10G E. coli and will be capable of rebooting and initiating a normal replication cycle in the cell.During replication, the designer tail fiber is repressed in trans, while a wild type T7 tail fiber will be provided in trans. Progeny phage assemble with the wild type T7 tail fiber while maintaining the designer tail fiber in the genome. These phages will be propagated repeatedly using this in trans scheme to high titer. In the final replication cycle phages are propagated a single time without in trans repression or the T7 wild type tail fiber, resulting in a high titer of progeny designer phage expressing the new tail fiber. With this process, we expect to generate large amounts of designer phage agnostic of the targeted host for the phage toward the creation of unbiased libraries of phage variants. To change T7 specificity by high-throughput tail fiber engineering, we will build a large library of T7 variants by evolutionary recombination of thousands of natural tail fibers. Since tail fibers of natural phages sample large microbial diversity, we expect that by 'mixing-and-matching' them with T7 tail fiber, we can expand the host range of T7. Shuffling sequence homologs has been highly successful in changing the specificity of enzymes and protein-protein interactions. Only phage variants that can infect and lyse the host amplify. This is a simple and robust selection that can be linked to deep sequencing of the unselected and selected libraries to identify successful design variants.Aim 3) To improve efficacy of engineered T7 phages and minimize bacterial resistanceOnce we find initial 'hits', we will further evolve efficacy in order for the phage to be able to kill the pathogen at low phage dosage. The evolved phages will be efficacious at a lower multiplicity of infection (fewer phages required per bacterial cells) and absorb faster. As an empirical estimate, we will evolve engineered T7 phages through additional rounds of mutagenesis and selection to kill E. coli O157:H7 at 100-to-1000 fold greater efficacy than initial hits. As with traditional antibiotics, bacteria develop resistance to phage. Bacteria reduce their susceptibility to phage attack by mutating bacterial genes required for phage propagation. Phages typically bind to bacterial receptors or lipopolysaccharides expressed on cell surface. We hypothesize that bacterial resistance could be fully suppressed by the use of multiple phages each targeting a different receptor. We will build phage cocktails comprising three T7 variants and determine the frequency.

Progress 10/01/19 to 09/30/20

Outputs
Target Audience:Gave talks at the following venues: Dept of Chem. & Biol. Engg, UW-Madison, WI SACNAS, National Diversity in STEM conference (Under-represented minorities in STEM) Dept of Genetics, UW-Madison, Madison, WI Madison Microbiome Seminar, Madison, WI Changes/Problems: Nothing Reported What opportunities for training and professional development has the project provided?This project is training one graduate and one undergraduate student. How have the results been disseminated to communities of interest?Gave talks and published a paper (under review). What do you plan to do during the next reporting period to accomplish the goals?In the next reporting period, we will demonstrate efficacy of engineered phages against pathogenic microbes.

Impacts
What was accomplished under these goals? The interaction between a bacteriophage and its host is mediated by the phage's receptor binding protein (RBP). Despite its fundamental role in governing phage activity and host range, molecular rules of RBP function remain a mystery. Here, we systematically dissect the functional role of every residue in the tip domain of T7 phage RBP (1660 variants) by developing a high-throughput, locus-specific, phage engineering method. This rich dataset allowed us to cross compare functional profiles across hosts to precisely identify regions of functional importance, many which were previously unknown. Substitution patterns showed host-specific differences in position and physicochemical properties of mutations, revealing molecular adaptation to individual hosts. We discovered gain-of-function variants against resistant hosts and host-constricting variants that eliminated certain hosts. To demonstrate therapeutic utility, we engineered highly active T7 variants against urinary tract pathogen. Our approach presents a generalized framework for characterizing sequence-function relationships in phages on a large scale.

Publications

  • Type: Journal Articles Status: Under Review Year Published: 2021 Citation: "Mapping the functional lsndscape of the receptor binding domain of bacteriophage T7"


Progress 10/22/18 to 09/30/19

Outputs
Target Audience:We recently published a review article title "Engineered bacteriophages as programmable biocontrol agents". This article was published in the Current Opinion on Biotechnology, widely respected publications read by members of academia and industry. Changes/Problems: Nothing Reported What opportunities for training and professional development has the project provided?This grant has trained a microbiology graduate student in synthetic biology approaches including high-throughput technologies, protein design, and genome engineering. How have the results been disseminated to communities of interest?These results are not published yet. We are currently working on the manuscript and hope to submit it in the next month or so. What do you plan to do during the next reporting period to accomplish the goals?We have optimized the ORACLE method for high-throughput tail fiber redesign. In the next reporting period, we plan to test these phage variants against pathogenic strains.

Impacts
What was accomplished under these goals? We have accomplished Aim1 and are well on our way to completing Aim2. Our high-throughput phage engineering approach is termed ORACLE forOptimizedRecombination,Accumulation andLibraryExpression. ORACLE creates large libraries of phage variants at a targeted locus by recombinase-mediated insertion of a library member from a susceptible host bacterial cell to the phage genome during the infection cycle. This requires introducing recombinase acceptor sites on the phage genome, creating a library of donor bacterial hosts carrying phage gene variants for recombination, enriching recombined phages by eliminating unmodified phages, and deep sequencing phage library applied on target host before and after selection. ORACLE is carried out in four steps: (1) making acceptor phage (2) inserting gene variants (3) enriching recombined phages (4) expressing library for selection and sequencing. We briefly explain the four steps with RBP as the gene-of-interest, but the technique is generalizable to any phage gene. Making acceptor phage:We modify the T7 phage genome by introducing Cre recombinase sites to make an "acceptor phage". We assemble T7 phage genome on a yeast artificial chromosome (YAC) from constituent dsDNA parts each ~8kb long (T7 genome is ~40kb) with 50bp overlapping arms. Yeast spontaneously assembles T7 phage genome as a YAC which can be transformed into a susceptibleE. colistrain to "reboot" the phage. To make an acceptor phage, the target gene to be diversified (in this case the RBP) is replaced with unrelated DNA on the phage genome, and Cre-LoxP sites are on either end of the native RBP locus. Recombinase sites are mutated to allow only one-way recombination. We confirmed that the recombinase sites do not reduce T7 virulence by standard efficiency-of-plating assays. Inserting gene variants:To ensure that the acceptor phage remains viable, the YAC with modified T7 genome lacking RBP is transformed intoE. colicontaining a helper plasmid providing the wildtype RBPin trans, allowing acceptor phages to propagate without a genomic RBP copy. TheE. colihost acts as a donor by carrying a plasmid library of the RBP variants and Cre recombinase to facilitate insertion of gene variant cassette into the phage genome. We use commercially available oligonucleotide chip-DNA to build phage variant library. Chip-DNA allows us to build tens-to-hundreds of thousands of pre-defined, made-to-order gene variants for scanning mutagenesis and metagenomic mining. Acceptor phages are passaged with the donor host bacteria containing the library and helper plasmid over multiple infection cycles to increase fraction of recombined phages. A critical step for creation of an unbiased library is that both recombined and unrecombined phages express the wildtype RBP provided by the helper plasmid which ensures all phages remain viable on this host. Enriching recombined phages:We enrich recombined phages by directing Cas9 to cleave unrecombined phages using a guide RNA specifically targeting the synthetic sequence we introduced at RBP locus. Cas9 is directed to the unrecombined region of the phages, allowing recombined phages to replicate while unrecombined phages are killed or suppressed. After this step, lysate is highly enriched with recombined phages with a small fraction of unrecombined phages. Phages continue to be complemented with wildtype RBP from the helper plasmid to avoid library bias. Expressing library for selection and sequencing:In the final step, recombined phages infect anE. colihost that lacks any plasmid (no helper or Cas9), allowing the phage particles to express the RBP variant. This phage variant library can now be applied on many different hosts independently at low multiplicity-of-infection to allow sufficient amplification of viable phages. By deep sequencing phage population before-and-after selection, functional scores of each variant is determined by computing the ratio of relative abundance under both conditions. We have optimized the ORACLE method for high-throughput tail fiber redesign. We plan to test these phage variants against pathogenic strains in the few months.

Publications

  • Type: Journal Articles Status: Published Year Published: 2019 Citation: Engineered bacteriophages as programmable biocontrol agents doi: 10.1016/j.copbio.2019.11.013