Source: UNIVERSITY OF NORTH TEXAS submitted to NRP
EXAMINING THE VIABILITY OF THE USE OF SAROCLADIUM ZEAE AS A BIOCONTROL AGENT IN THE AGRICULTURAL PRODUCTION OF MAIZE
Sponsoring Institution
National Institute of Food and Agriculture
Project Status
ACTIVE
Funding Source
Reporting Frequency
Annual
Accession No.
1030814
Grant No.
2023-67011-40393
Cumulative Award Amt.
$180,000.00
Proposal No.
2022-11420
Multistate No.
(N/A)
Project Start Date
Jun 1, 2023
Project End Date
May 31, 2026
Grant Year
2023
Program Code
[A7101]- AFRI Predoctoral Fellowships
Recipient Organization
UNIVERSITY OF NORTH TEXAS
1155 UNION CIR #305250
DENTON,TX 76203-5017
Performing Department
(N/A)
Non Technical Summary
One third of the global corn supply is produced in the United States, making maize the largest American agricultural product. Fungal pathogens are a major threat to the production of this crop by causing rot and producing toxic compounds. Corn showing signs of fungal pathogen growth are discarded, but levels of these compounds above the accepted safe threshold have been detected in recent studies. This implies that not only can there be a decreased crop yield from these toxic fungi, but that there are still traces of toxins that make it into the food supply. Additionally, lower crop yield may result in higher costs of corn products, including animal feed. This may cause an economic ripple effect as higher animal feed costs may lead to increased costs of meat and animal products. These are significant consequences for the general consumer.The fungus Sarocladium zeae grows within corn and produces antibacterial compounds, pyrrocidines, that naturally inhibit the production of the toxic compounds. Besides pyrrocidines, most compounds propagated by S. zeae are not known. The natural inhibition of the harmful fungi makes S. zeae an attractive candidate for a biocontrol agent. However, it must first be established that there are no toxins produced by S. zeae that simply have not been discovered yet. As it is impossible to test every single possible set of growing conditions, analysis of natural product-producing subsets of its fungal DNA will be done instead. These otherwise inactive DNA subsets will be activated with genetic modification in a fungal host, the modified fungus will be grown, and the new compounds will be identified. Once identified, the potential toxicity of the compounds can be determined, beginning to answer the question of whether S. zeae can be applied as a targeted biocontrol agent in the growth of corn.
Animal Health Component
(N/A)
Research Effort Categories
Basic
100%
Applied
(N/A)
Developmental
(N/A)
Classification

Knowledge Area (KA)Subject of Investigation (SOI)Field of Science (FOS)Percent
7124020110275%
7124020200025%
Goals / Objectives
Major Goal 1: The purpose of this project is to characterize secondary metabolite-producing biosynthetic gene clusters (BGCs) of Sarocladium zeae due to its production of antibacterial compounds that inhibit aflatoxins and fumonisins, two major microbiological threats to corn. As the selective action of S. zeae against mycotoxins has incurred an interest in its use as a targeted biocontrol agent, all other possible metabolites must be characterized to ensure no toxins can be produced under any conditions. As only two of the 29 bioinformatically detected BGCs have been studied, the intention of the proposed work is to characterize metabolites produced by 17 of the remaining BGCs.Project objectives to attain this goal:Perform heterologous expression (HEx) with non-native host Aspergillus oryzae on the six terpene synthase and one non-ribosomal peptide synthase-polyketide synthase (NRPS-PKS) hybrid megasynthase-containing BGCs.Develop a transformation method for S. zeae using the translation elongation factor (TEF) promoter, which has been reported to be successful with S. zeae.Perform transcription factor (TF) overexpression on the 12 BGCs containing TFs.Elucidate the structures of all discovered compounds through HEx and TF overexpression work.Determine potential toxicity of elucidated structures.Report this new knowledge to the scientific and agricultural communities through conference presentations and peer-reviewed publications.Major Goal 2: Another major goal to be realized over the duration of this project is the enrichment of knowledge and professional development of the graduate student acting as the project director (PD).Project objectives to attain this goal:Teaching and training of any undergraduate student mentees involved in the completion of the proposed work and ensuring subsequent completion of mentee responsibilities. Undergraduate students Ian Sartor, Tram Nguyen, and Timothy Lim are going to be involved in the heterologous expression of terpene synthase genes in the coming months.Communication of project progress and findings through at least two conference presentations per year.Weekly meetings with the primary mentor and research group for the evaluation of project successes, possible improved methods, and practice for professional presentation of progress made for the PD.Biannual meetings with the doctoral committee for the purpose of obtaining expert advice and effective accountability on all listed objectives. As it stands, the doctoral committee is composed of the primary mentor and fungal natural products chemist, Dr. Elizabeth Skellam an analytical chemist, Dr. Jeffry Kelber; and a bioanalytical chemist with a specialty in mass spectrometry, Dr. Guido Verbeck IV. The addition of a biologist is planned before the end of 2023 to ensure an expert biological perspective is able to be given as well.Completion and submission of annual project updates to the USDA-NIFA-EWD program through REEport as an additional level of accountability.Completion of the doctoral dissertation and subsequent graduation.Major Goal 3: Lastly, the training of an earlier-stage graduate student by the PD will be completed in order to ensure the remaining BGCs that are not characterized through the course of this project will begin immediately upon award termination.Project objectives to attain this goal:Selection of a graduate student interested in continuing the work of identifying remaining secondary metabolites from S. zeae 1.5-2 years into the progress of this work.Training of the selected graduate student on relevant methods and project background already completed by the PD.Training of the selected graduate student on HEx with a specific focus on uncharacterized BGCs that will be the responsibility of the new student after the completion of the proposed work by the PD.Establishment and commitment to regular meetings with the PD and primary mentor to assess progress.
Project Methods
The methods to be employed in this work are as follows:Bioinformatic analyses to be performed periodically to stay up to date with advances in literature methods as they are developed and published.In vitro work will begin with plasmid building for a projected 21 expression plasmids as described in the literature.1Performance of fungal PEG-mediated protoplast transformation via heterologous expression in Aspergillus oryzae as described in the literature.1Application and/or possible development of a transformation method based on those described in the literature2,3 with the use of a previously successful promoter4 in place of previous promoters attempted.Transcription factor (TF) overexpression of TF-containing biosynthetic gene clusters (BGCs) using the described transformation method.Solid phase microextraction (SPME) and Liquid-liquid extraction (LLE) of secondary metabolites from the media and cells of transformed fungus as described in the literature.5,6Instrumental analysis. These methods must be designed at the appropriate stage of the research i.e., when peaks have been isolated for compound identification. Instruments projected for use include HS-SPME-GC-MS, LCMS, HR-LCMS, MS/MS, NMR, and 2D NMR.Efforts to be performed under this work:Laboratory instruction for undergraduates and graduates involved in the procession of this work.In-lab workshops hosted monthly as opportunities for peer-to-peer instruction.Applications to workshops and conferences, such as those submitted already to the NPLinker bioinformatics workshop (not selected) and Gordon Research Symposium and Conference on Mycotoxins and Phycotoxins (selected for attendance in June 2023)Publications submitted when structures are identified and evaluated.Evaluation of the success of this work:Successful elucidation of structures.Successful elucidation of BGCs.Entries to publicly available databases such as MIBiG, NPAtlas, and GenBank of sequence data of the BGCs and associated compounds.An estimated four peer-reviewed publications successfully reaching fungal, agricultural, biochemical, and/or chemical journals.Successful training and completion of tasks by undergraduates measured by level of understanding reflected in submitted lab reports, successful transformants, and the development of a measure of independence in experimental work.Graduate students selected to carry on the work.Meetings, conferences, and presentations given. A minimum of two conferences per year as well as presentations outside of these conferences to local scientists at the university.Literature Referenced in MethodsDe Mattos-Shipley, K. M. J.; Lazarus, C. M.; Williams, K. Investigating Fungal Biosynthetic Pathways Using Heterologous Gene Expression: Aspergillus Oryzae as a Heterologous Host. In Engineering Natural Product Biosynthesis; Skellam, E., Ed.; Methods in Molecular Biology; Springer US: New York, NY, 2022; Vol. 2489, pp 23-39. https://doi.org/10.1007/978-1-0716-2273-5_2.Liu, Q.; Johnson, L. J.; Applegate, E. R.; Arfmann, K.; Jauregui, R.; Larking, A.; Mace, W. J.; Maclean, P.; Walker, T.; Johnson, R. D. Identification of Genetic Diversity, Pyrrocidine-Producing Strains and Transmission Modes of Endophytic Sarocladium Zeae Fungi from Zea Crops. Microorganisms 2022, 10 (7), 1415. https://doi.org/10.3390/microorganisms10071415.Johnson, L. J.; Koulman, A.; Christensen, M.; Lane, G. A.; Fraser, K.; Forester, N.; Johnson, R. D.; Bryan, G. T.; Rasmussen, S. An Extracellular Siderophore Is Required to Maintain the Mutualistic Interaction of Epichloë Festucae with Lolium Perenne. PLOS Pathog. 2013, 9 (5), e1003332. https://doi.org/10.1371/journal.ppat.1003332.Thornewell, S. J.; Peery, R. B.; Skatrud, P. L. Cloning and Characterization of the Gene Encoding Translation Elongation Factor 1α from Aureobasidium Pullulans. Gene 1995, 162 (1), 105-110. https://doi.org/10.1016/0378-1119(95)00312-T.Jiang, L.; Lv, K.; Zhu, G.; Lin, Z.; Zhang, X.; Xing, C.; Yang, H.; Zhang, W.; Wang, Z.; Liu, C.; Qu, X.; Hsiang, T.; Zhang, L.; Liu, X. Norditerpenoids Biosynthesized by Variediene Synthase-Associated P450 Machinery along with Modifications by the Host Cell Aspergillus Oryzae. Synth. Syst. Biotechnol. 2022, 7 (4), 1142-1147. https://doi.org/10.1016/j.synbio.2022.08.002.Turner, N. W.; Subrahmanyam, S.; Piletsky, S. A. Analytical Methods for Determination of Mycotoxins: A Review. Anal. Chim. Acta 2009, 632 (2), 168-180. https://doi.org/10.1016/j.aca.2008.11.010.

Progress 06/01/23 to 05/31/24

Outputs
Target Audience:During this reporting period, target audiences reached included scientific peers as well as students engaged both directly and indirectly in the project. Reaching scientists in similar fields is crucial as new knowledge about the largely unstudied fungus is obtained through this work. With the discovery and dissemination of novel results, understanding of this fungus may potentially lead to discovery of similar results in other living systems, a greater understanding of the mechanisms within natural products as a whole, and greater insight into the viability of developing the fungus into a biocontrol agent. Outside of the PD, a total of three undergraduate students were directly involved in this work completed at the University of North Texas, an emerging Hispanic-serving institution. These were students in biology and biochemistry who each were trained to oversee the design and completion of the heterologous expression of terpene synthase genes. In doing so, the students were able to gain practical lab experience, critical thinking skills, problem solving abilities, and a deeper understanding of multiple disciplines within STEM. They performed experiments often seen in labs focused on molecular biology, organic chemistry, analytical chemistry, and bioinformatics. This acts to not only give them lab-relevant experience, but transferrable skills that will be useful to them as they proceed in their planned graduate studies in medical and graduate school. Changes/Problems: Nothing Reported What opportunities for training and professional development has the project provided?Training for the PD has been extensive under the purview of this award. In a direct sense, biosafety, chemical safety, and other laboratory research trainings are completed and refreshed annually by the PD. Additionally, the biosafety component of the work allows for the PD to interface with the Institutional Biosafety Committee (IBC) and be involved in the refining of IBC protocols under direct supervision of the primary mentor. Besides the discussed opportunities for professional development from the major goals of the project, there has also been the added benefit of the PD being able to step into the role of trainer for undergraduate students. Training itself requires depth of knowledge to ensure complete understanding for the trainees, leadership skills, and soft skills transferrable to all career types. With this, the opportunity to train and lead a small team of three undergraduates has been crucial to the professional development of the PD. How have the results been disseminated to communities of interest?Results have been disseminated to communities of interest through presentations at scientific conferences to reach a broader scientific audience. This has allowed for external input into the research being done and any recommendations from scientists in similar fields who are working on similar research, as well as scientists in completely different fields providing alternative perspectives. Notably, the presentation of this work at the American Chemical Society Division of Professional Relation's LGBTQIA+ inclusive PRIDE session was able to reach underrepresented populations in science. Additionally, undergraduate students enrolled in the rising Hispanic-serving institution of the University of North Texas have engaged in training for both the dissemination of and collection of results under this work. What do you plan to do during the next reporting period to accomplish the goals? Remaining work to explore potential terpene compounds will be completed to fully characterize these 6 BGCs and demystify what natural products are produced. Remaining compounds being produced by the wildtype S. zeae which can be collected and analyzed using scientific instruments will be identified. These findings will be submitted to peer-reviewed journals for publication. The PD will engage in the development of scientific knowledge and professional development by continuing to attend conferences. This allows for input from the greater scientific community while also providing opportunities for networking and attendance at professional development events present at many of the major scientific conferences. The graduate student who will be taking over the work in this project after the PD graduates will be selected. This is to ensure that thorough training and preparation may be completed during the remaining two years of the project's timeline.

Impacts
What was accomplished under these goals? Major goals identified for this project are to determine and disseminate results of 17 sets of compounds produced by the fungus Sarocladium zeae, academically and professionally develop the PhD candidate acting as PD, and to train a graduate student to continue this work after the PD graduates. Accomplishments have been reached toward the first two major goals. Under the first major goal of characterizing products that can be produced by S. zeae, a variety of experimental strides have been made. Methods have been improved for the study of approximately one third of the sets of compounds that this project aims to identify. Improvements were made to the lab conditions for the growth of the host producing the compounds, additional validation steps that ensure the host has the necessary biological machinery to produce the compounds, and extensive procedures to collect compounds with varying structures and properties. This allows for more efficiency in characterizing the final compounds and publishing the results to disseminate among target audiences. Additionally, methods have been designed and validated for the identification of the remaining 12 sets of compounds that are goaled to be determined. Previously, the PD was not able to successfully genetically modify S. zeae, which was the initial step required for moving forward on the study of these 12 sets of compounds. Now, with this first milestone successfully met, examination and determination of these compounds may be completed, followed by the publication of the results. For the second major goal of enriching the knowledge of the PD and engaging in activities for professional development, significant progress has been made. The development and optimization of the above discussed experimental methods was an incredibly valuable learning experience. The PD was able to perform independent critical thinking to mitigate challenges under the supervision of the advisory committee, made up of leaders in the biological and chemical fields. Additionally, the PD was awarded the American Chemical Society PRIDE-Merck Graduate Research Award. This involved the assignation of an industry mentor from Merck Chemical who has been instrumental in professional development. Additionally, the award included a stipend for attendance at the Spring 2024 American Chemical Society National Meeting and a chance to present research. This, in turn, opened opportunities for networking and, hence, further professional development.

Publications

  • Type: Conference Papers and Presentations Status: Published Year Published: 2024 Citation: Schoellhorn, S. Bioinformatically informed evaluation of Sarocladium zeae biocontrol agent viability. https://doi.org/10.1021/scimeetings.4c10650.