Source: TEXAS A&M UNIVERSITY submitted to
CONSERVED HYPOTHETICAL GENES IMPORTANT FOR CAMPYLOBACTER VIRULENCE
Sponsoring Institution
National Institute of Food and Agriculture
Project Status
COMPLETE
Funding Source
Reporting Frequency
Annual
Accession No.
1001592
Grant No.
(N/A)
Cumulative Award Amt.
(N/A)
Proposal No.
(N/A)
Multistate No.
(N/A)
Project Start Date
Jan 6, 2014
Project End Date
Sep 30, 2018
Grant Year
(N/A)
Program Code
[(N/A)]- (N/A)
Project Director
Threadgill, DE, S.
Recipient Organization
TEXAS A&M UNIVERSITY
750 AGRONOMY RD STE 2701
COLLEGE STATION,TX 77843-0001
Performing Department
Veterinary Pathobiology
Non Technical Summary
Campylobacter species, especially C. jejuni, are leading causes of foodborne diarrheal illness in the United States. Active surveillance data provided by the Foodborne Diseases Active Surveillance Network known as FoodNet suggests that about 14 cases of Campylobacter induced gastroenteritis are diagnosed each year per 100,000 people in the U.S. population. Since many more cases go undiagnosed or unreported, campylobacteriosis is estimated to affect over 1.3 million people every year. The most common sources of Campylobacter in the food supply are chicken and chicken products followed by unpasteurized cow's milk. Based on estimates of the infection of chicken flocks with C. jejuni, up to 90% of chicken flocks in the US are colonized . Because of the high degree of prevalence in chicken flocks, methods aimed at reducing the frequency and/or duration of colonization by C. jejuni are desirable. We recently completed transcriptional profiling studies aimed at assessing genes differentially expressed in the human host versus the chicken host, and we observed that genes designated as Cj0371 and Cj0372 from the first sequenced strain of were upregulated at 42 °C, the body temperature of chickens . In other studies by collaborators (Dr. Alain Stintzi, Ottawa Institute of Systems Biology), these genes were also upregulated in a rabbit illeal loop model (39°C body temp) suggesting that they might be important for survival/colonization in non-human hosts . To test the hypothesis that one or more of the genes upregulated at 42°C might be important for survival/persistence in the chicken host, we created a null mutant for the Cj0372 gene (no functional Cj0372 protein produced) in strain NCTC 11168 and found that the mutant strain is non-motile and invasion defective. Motility and the ability to invade eukaryotic cells are important virulence determinants for C. jejuni. Additionally, the strain lacking Cj0372 produces a large amount of an unidentified secreted substance and so is prone to autoagglutination especially at 42C, because the substance is either produced earlier in the growth cycle or is secreted to higher levels at that temperature. Autoagglutination results in precipitation in vitro and thus is viewed as negative for optimal growth. Mutants lacking Cj0372 are also 30% smaller on average than wild-type C. jejuni . Because these mutants are non-motile we have been unable to look at the in vivo effects of the mutation (successful animal colonization requires motility, but based on the in vitro results, this gene is a potential target to attack with non-antibiotic treatments to reduce and possibly eliminate C. jejuni from infected chickens and livestock species. Although Cj0371 and Cj0372 were originally annotated as conserved hypothetical genes, we have made substantial progress in our understanding of the function of Cj0372 and now believe it is a glutathionylspermidine synthetase (GspS). GspS's have been identified in other bacterial species previously, in particular in E. coli. Until recently, little was known of the importance of these enzymes to bacteria, although a similar enzyme from trypanosome species (trypanothione synthetase-amidase) is being investigated by several groups as a drug target against these organisms. Since the null mutant strain lacking Cj0372 has severe phenotypes, we decided to investigate the effect of a null mutation in the same gene on a more clinically relevant strain and thus chose strain 81-176, a human vaccine candidate strain that causes severe and often bloody diarrhea. In this new project, we want to extend and expand our studies of both of these mutated strains in order to determine how the mutation of a single gene like Cj0372 can impact very different pathways. A more complete understanding of how the Cj0372 gene functions will allow us to focus future studies on potentially new and more effective ways to control and/or eliminate C. jejuni from the chicken host and/or from poultry derived food products.
Animal Health Component
10%
Research Effort Categories
Basic
85%
Applied
10%
Developmental
5%
Classification

Knowledge Area (KA)Subject of Investigation (SOI)Field of Science (FOS)Percent
71232601040100%
Goals / Objectives
In previous studies we created and characterized a mutant C. jejuni strain deficient in an unknown hypothetical protein that appeared to be important for survival and/or maintenance in non-human hosts including the chicken. We will complete the examination of the Cj0372 mutant strains and determine mechanism(s) to explain the observed phenotypes. Aim 1, Assay the recombinant Cj0372 protein to determine if it is a GspS using assays developed for E. coli GspS. Verify that the C. jejuni protein has GspS function in order to better understand why loss of this protein results in the observed phenotypes. In Aim 2, we will sequence the genomes of both the wild-type parental strains and the mutant strains to verify that the only mutations impacting the observed phenotypes are those resulting from the creation of the null mutations and that there are no other mutations that could be responsible. In Aim 3, we will assess the transcriptional changes of the Cj0372 mutant strains and their respective parental strains using microarrays to determine what effect this mutation has on the expression of other genes in the mutants. This will allow us to investigate possible mechanisms to explain why the loss of the GspS enzyme results in a loss of motility and the other observed phenotypes. In Aim 4 we will quantify the severity of the phenotypes observed in 81-176 with those in 11168. With specific phenotypes quantified more precisely, we will have a more informed approach to the analysis of the microarray data as well as the sequencing data. In Aim 5, we will determine the identity of the secreted substance that accumulates in Cj0372 mutant strains. In particular, does the identity of this substance help explain the observed phenotypes and/or mechanism underlying the observed phenotypes? In Aim 6, we will use the antibodies we have for Cj0372 to determine the location of this protein in C. jejuni, i.e., does its location suggest a mechanism of action?
Project Methods
For Specific Aim 1, we have already cloned Cj0372 from strain 11168 and expressed the protein for antibody production. Although we did not need active enzyme to create antibodies, we need to purify protein with optimal enzymatic function in order to fully assay for enzyme activity. Methods describing the assay for the E. coli enzyme have only recently been published, and we plan to follow this new assay to measure function of the C. jejuni enzyme. The manuscript describing the function of the E. coli enzyme demonstrated that two other putative E. coli gsp genes encoded phosphatases but not glutathionylspermidine synthetases. In Aim 2, we will sequence the genomes of both the wild-type parental strains and the mutant strains using standard sequencing methods (454) to verify that the only mutations impacting the observed phenotypes are those resulting from the creation of the null mutations and that there are no other mutations that could be responsible for the observed phenotypes. This is necessary since we have not been able to successfully complement the Cj0372 mutation. While we believe that this is because the mutation impacts the uptake of DNA and/or impacts the homologous recombination process we cannot rule out the possibility of a secondary mutation without sequencing the genome. Complementation is the gold standard for assigning phenotypes to a single gene mutation. For Aim 3, we will assess the transcriptional changes of the Cj0372 mutant strains and their respective parental strains using microarrays. This will allow us to investigate possible mechanisms to explain why the loss of the GspS enzyme results in a loss of motility and other observed phenotypes. There is no demonstrated effect on motility in E. coli mutants lacking GspS (KN Delaney and DS Threadgill, unpublished) and thus there is no a priori way to know whether this is an outcome expected for loss of this enzyme in C. jejuni. We previously identified Cj0372 as a gene upregulated at 42 °C using microarrays, and many or all of the genes impacting motility in C. jejuni have been identified so it should be straightforward to determine whether the loss of Cj0372 directly impacts transcription of motility-related genes or whether the effect is indirect. Microarray analysis will also allow us to determine if other genes/pathways may be impacted in the mutant strains thus helping explain the mechanism(s) of action. In Aim 4 we will quantify the severity of the phenotypes observed in 81-176 with those in 11168. With specific phenotypes quantified more precisely, we will have a more informed approach to the analysis of the microarray data as well as the sequencing data. To approach the question of the importance of additional glutathione-related genes to the observed phenotypes, we will generate a targeted mutation in those genes in 81-176. If the presence of these glutathione-related genes is responsible for the worsened outcomes in the 81-176 mutant strain, we anticipate removal of these genes would ameliorate the defects back to what is seen with the 11168 mutant strain. If however the glutathione-related genes do not play a major role in the observed worsened outcomes, we expect no or minimal amelioration in the double mutant. For Aim 5, the secreted substance that accumulates in Cj0372 mutant strain will be purified and identified through biochemical methods. We will first determine whether the substance is sensitive to digestion by proteases, nucleases and polysaccharide lyases. This will help to suggest the nature of the substance and what type of assistance to seek for identification. For example core facilities that specialize in proteomics are not always adept at polysaccharide analysis, so having a better idea about the biochemical nature of the unknown substance will guide us to the appropriate expertise. For Aim 6, we will use the antibodies we have for Cj0372 with both electron microscopy and fractionation techniques to establish protein location. The location of this protein in the cell will help to suggest how the loss of this single protein is causing the pleotropic effects we observe. In particular, we will address what other protein or proteins may interact directly with Cj0372 based on its cellular location. This could be enhanced by the microarray data indicating particular pathways that are impacted in the mutant strains.

Progress 01/06/14 to 09/30/18

Outputs
Target Audience: Nothing Reported Changes/Problems:Loss of graduate student who was to continue the studies meant that no additional studies were being undertaken. Was unable to hire research staff to replace students who were leaving, and teaching load was high for 1/2 the academic year. Manuscript will be revised and resubmitted and hopefully will be able to publish in peer reviewed journal. What opportunities for training and professional development has the project provided?Graduate student who was supposed to be involved with the project opted to complete a MS non-thesis and depart the graduate program. Tried to hire a research staff member but was outbid by her company so was unable to hire her. How have the results been disseminated to communities of interest? Nothing Reported What do you plan to do during the next reporting period to accomplish the goals? Nothing Reported

Impacts
What was accomplished under these goals? Still preparing to resubmit the manuscript regarding these studies. Had hoped to complete some additional studies to add to the manuscript but graduate student and staff turnover issues prevented this. Other authors are no longeractively engaged in research as primarily at undergraduate teaching institutions now, so manuscript will be resubmitted as is and published as permitted.

Publications


    Progress 10/01/15 to 09/30/16

    Outputs
    Target Audience: Nothing Reported Changes/Problems: Nothing Reported What opportunities for training and professional development has the project provided?Unfortunately, the graduate student that was orginally assigned to this project was unable to make any progress on the goals of the project and has nowbeen terminated from the graduate program due to poor performance and low motivation. How have the results been disseminated to communities of interest?Manuscript preparation in progress by the PI and will be submitted to appropriate scientific journals dealing with organisms of importance to foodborne illness. What do you plan to do during the next reporting period to accomplish the goals?Assuming we are able to get the first manuscript successfully published, there will be the opportunity to apply for funding for this project to federal funding sources to then recruit a graduate student or preferentially a postdoctoral fellow who can address the goals of the Hatch project.

    Impacts
    What was accomplished under these goals? Unfortunately, the graduate student who was to approach these goals for her PhD proved to be a poor candidate for graduate school. She was unable to do well in her classes while also pursuing research and has now been asked to complete a MS non-thesis and exit the program.

    Publications


      Progress 10/01/14 to 09/30/15

      Outputs
      Target Audience: Nothing Reported Changes/Problems:Termination of ill-equipped and inappropriate technician and replacement with a highly motivated and eager graduate student. Previous graduate studentnot involvedwithC. jejuni research studies or any bacterial research(mammalian genomics) so therefore no one in laboratory to work on the goals of Hatch project until recent grad student identified. What opportunities for training and professional development has the project provided? Nothing Reported How have the results been disseminated to communities of interest? Nothing Reported What do you plan to do during the next reporting period to accomplish the goals?New graduate student joining the lab (Michelle Gorman)is very interested in the project and is planning to complete as part of her dissertation research. She will begin in June 2016 and already is planning and preparing for the initial experiments.

      Impacts
      What was accomplished under these goals? The technician hired to perform the research tasks for the project was not capable of accomplishing the tasks. She has subsequently found other employment, but due to the lack of a probationary period for employment, the delay in her separation was substantial and there were not additional funds to replace her and begin again. Have recently identified a PhD graduate student who is very interested in this project and will be pursuing the aims once she is officallly a member of the laboratory, June 2016 expected. The first publication has been delayed because of a serious illness of the first author (Dr. Kristen Delaney), but this should be revised and resubmitted by July 2016 or August 2016.

      Publications

      • Type: Journal Articles Status: Other Year Published: 2016 Citation: Delaney KN, Andrus JM, Jaehrig A, Carroll IM, Wang J, LaGier MJ, Stintzi A, Threadgill DS. Campylobacter jejuni gene Cj0372 (ortholog of E.coli gspS) is temperature regulated and plays a role in cell size, motility and host cell invasion.


      Progress 01/06/14 to 09/30/14

      Outputs
      Target Audience: For this project's first year, the target audience is primarily other researchers since the project has been started but not widely publicized. Ultimately assuming the project is successful, the target audience would expand to potentially include poultry producers since the project is aimed at reduction of Campylobacter jejuni a known human pathogen frequently found in chickens and turkeys and therefore in food products derived from poultry. Changes/Problems: Nothing Reported What opportunities for training and professional development has the project provided? This project was initiated with two previous postdocs (Dr. Kristen Delaney and Dr. Jason Andrus) who have now gone on to tenure-track or tenured faculty positions at other universities. Other postdocs and graduate students also participated in the early stages of the project including Dr. Ian Carroll (clinical faculty now) and Dr. Michael LaGier (tenure-track faculty). Ms. Angelika Jaehrig was an MS student who had an important role in the generation of the mutant strain. Both Dr. Delaney and Dr. Andrus presented the research at scientific meetings at both the national and international level as well as the local level. Undergraduate students worked alongside both Dr. Delaney and Dr. Andrus in the laboratory and thus were engaged in the scientific process. How have the results been disseminated to communities of interest? Because the research has been presented at scientific meetings the main communities to know of the results are those either attending those meetings or accessing the abstracts from them. Abstracts are generally available on the internet preceding the meetings and for some time afterward and thus available to anyone who is searching the web. What do you plan to do during the next reporting period to accomplish the goals? Hire a more technically compotent technician or a postdoc that will have graduate students and undergrads as additional support. When the laboratory moved from NC to TX in August 2013, two very valuable researchers (postdoc and lab manager) were lost and have not yet been able to replace these positions but will accelerate the search process in 2015. Will utilize the multitude of resources at TAMU to do those projects that can be done without additional support staff, i.e. genome sequencing, enzymatic assays.

      Impacts
      What was accomplished under these goals? For Aim 1 We have obtained a positive control E. coli strain that expresses a GspS that is more similar to C. jejuni GspS in that it lacks the amidase function associated with the bi-functional enzyme. We did this because we assume that the C. jejuni gene is not bi-functional as it lacks the amidase domain and produces a much smaller protein therefore. We have also arranged to have the products of these assays confirmed by Dr. William Russell in the Department of Chemistry (TAMU). He will use published protocols to separate the products by HPLC after we have run the assays. For Aim 2 We have identified the appropriate personnel at TAMU to assist with the sequencing and analysis of the mutant and parental genomes. This will be accomplished in short order in 2015. Lack of adequate research personnel has hampered the initiation of the project. The research technician hired in May 2014 at TAMU has proven unable to accomplish the basic tasks and has now left the laboratory (Jan. 2015). Either a new technician or preferably a talented postdoc will be hired in 2015 to faciliate the increased pace of the project.

      Publications

      • Type: Journal Articles Status: Submitted Year Published: 2015 Citation: Delaney KN, Andrus JM, Jaehrig A, Carroll IM, Wang J, LaGier MJ, Stintzi A, Threadgill DS. Campylobacter jejuni gene Cj0372 (ortholog of E. coli gspS) is temperature regulated and plays a role in cell size, motility and host cell invasion. Submitted to Canadian J of Microbiol.