EDUCATION IN GENOMICS-BASED MICROBIAL FORENSICS

• Sponsoring Institution: National Institute of Food and Agriculture
• Project Status: COMPLETE
• Funding Source: AFRI COMPETITIVE GRANT
• Reporting Frequency: Annual
• Accession No.: 0220673
• Grant No.: 2010-65110-20488
• Cumulative Award Amt.: $999,900.00
• Proposal No.: 2009-03005
• Project Start Date: Jan 15, 2010
• Project End Date: Jan 14, 2015
• Grant Year: 2010
• Program Code: [91312]- Microbial Genomics Functional Genomics

Recipient Organization
PENNSYLVANIA STATE UNIVERSITY
208 MUELLER LABORATORY
UNIVERSITY PARK,PA 16802

Performing Department
Plant Pathology & Environmental Microbiology

Non Technical Summary
Microbes exert a far-reaching influence on the earth's biosphere both negatively and positively, and thus have been a major focus of research. Particularly, advances in genomics and informatics are rapidly expanding our knowledge of the genetic makeup and evolution of various microbes. To fully harness the power of microbial genomics for understanding the traits of practical importance and their evolution, we need to integrate genomics with perspectives and knowledge from other areas of science, particularly evolutionary biology, ecology, and informatics. Without such integration, translation of the data from microbial genomics into enhanced understanding of microbiology and practical problem solving will be severely hampered. This integration requires concerted efforts by researchers and educators. The goal of this graduate training program is to educate the next generation of researchers and educators who are well versed in integrating data and tools in microbial genomics with those from other areas of science to answer fundamental microbiology questions and to solve practical microbe-related problems faced by the nation's agricultural, food and environmental systems, and who also possess adequate professional skills and ethics to work effectively in diverse professions. Training in microbial genomics should be multidisciplinary in nature and requires a broad understanding of biological systems. However, given the exponential increase in data and tools in genomics and other areas of science, it is unrealistic to educate generalists who can do it all. Instead, we will help our students become specialists in a few specific areas and at the same time, learn and practice the basic scientific languages of other disciplines so that they can work effectively with other specialists with disparate expertise toward a common goal. The curricula, human resources, and physical infrastructures offered by the established Penn State graduate programs in Bioinformatics & Genomics, Plant Pathology, Veterinary Science, Food Science, and Genetics, as well as a new course developed for this program, will be utilized to broaden and strengthen the students' learning experience. Multiple approaches will be utilized to nurture students' ability of utilizing diverse genomics data and tools in solving complex problems through synthesis and teamwork.

Animal Health Component

40%

Research Effort Categories

Basic

60%

Applied

40%

Developmental

(N/A)

Classification

Knowledge Area (KA)	Subject of Investigation (SOI)	Field of Science (FOS)	Percent
903	4099	1040	100%

Knowledge Area
903 - Communication, Education, and Information Delivery;

Subject Of Investigation
4099 - Microorganisms, general/other;

Field Of Science
1040 - Molecular biology;

Keywords

education

evolution

informatics

microbial genomics

outreach

problem solving

professional development

Goals / Objectives
The goal of this graduate training program is to train students in microbial functional and evolutionary genomics and informatics, while providing opportunities for learning about and solving current and emerging problems faced by the nation's agricultural, food and environmental systems. The project directors and other participants, working in industry, state and federal research and regulatory agencies, and academia, bring disparate yet complementary expertise, experience and perspectives to this program. The program participants will help students gain broad perspectives in microbial genomics, evolutionary biology and informatics, conduct learning and problem solving via peer collaboration and synthesis, and develop professional skills and ethics. The curricula, human resources, and physical infrastructures offered by the established Penn State graduate programs in Bioinformatics & Genomics, Plant Pathology, Veterinary Science, Food Science, and Genetics, as well as a new course developed for this program, will be utilized to broaden and strengthen the students' learning experience. The students in this program will develop a thesis project based on one or more of the following topics: (i) what are the evolutionary relationships and species boundaries within important microbial pathogen groups; (ii) which genes contribute to microbial traits that affect agricultural, food, and environmental systems; (iii) how do fitness costs associated with human intervention, such as application of chemicals, introduction of new varieties, and changes in management practice, affect the evolution and variation of microbial pathogens; (iv) what are the mechanisms driving the microbial genome evolution with the focus on pathogens; and (v) how do genes in different microbes respond to stimuli from other organisms and environments and how do these changes relate to important microbial traits.

Project Methods
The focus of students' thesis research is on the application of genomic data and tools, and informatics, to study the biology, diversity and evolution of microbial groups important for the health of plants and/or animals and food safety and to solve practical problems. We will design and implement several program activities to enhance students' skill in the following four areas. (A) Problem solving through multidisciplinary collaboration: As the complexity of biological inquiries increases, the importance of and need for team-based problem solving is quickly amplified. Major breakthroughs in science increasingly result from collaborations among researchers with different expertise, and the importance of such collaborative efforts will continue to escalate. Given the nearly impossible task of educating generalists who can do it all, we should help the next generation of researchers and educators learn and practice how to work effectively with other specialists toward a common goal. We will employ several activities to nurture students' ability of utilizing diverse genomics data and tools in solving complex problems through synthesis and teamwork. (B) Bioinformatics: In this age of information overload, the problem we typically encounter is not the lack of data, but the difficulty of synthesizing rapidly accumulating data to build global pictures. Recent developments in information science provide computational tools that can aid biologists in managing and integrating their data, sharing their methods and data, and even in distributing their computing infrastructure. We will help our students learn and use various bioinformatics tools through their course work, research, and outreach. Well-established informatics platforms and expertise at Penn State will facilitate and support this training. (C) Outreach via the web: The internet and web technology are rapidly evolving and have fundamentally transformed many aspects of our lives and society, one of which is how we interact and work with other people. The "web 2.0" social networking models and tools, once integrated with appropriate human capital and knowledge bases, offer huge potential for enhancing our capability to solve many problems in research, education, and outreach via mass collaboration. Incorporation of web technology in research, education, and outreach will be an integral part of this program. (D) Professional development and ethics: Students will need more than scientific knowledge and skills to make a successful career. Most graduate students often learn professional skills and ethics in an ad hoc manner, or through trial by fire. To help our students make a smooth transition from graduate school to a professional career, we will mentor them to acquire key skills, such as professional ethics, effective communication, efficient management of time and resources, and the ability to communicate and work productively with a diverse group of coworkers.

Progress 01/15/10 to 01/14/15

Outputs
Target Audience: The main group served by this project is >20 PhD students that have been supported by this training grant. These students, chosen from nine graduate programs at Penn State, have investigated the evolution and ecology of agriculturally important microbes and the mechanisms underpinning diverse molecular and cellular processes affecting the agricultural and environmental systems using a combination of technologies with a focus on genomic data/tools and informatics tools. They also have learned to formulate solutions for microbe-related practical problems that impact the nation's agricultural, food and environmental systems as teams. Two other groups served by this project include: The Project Directors, other Penn State participants and their collaborators: This project has facilitated the development of collaborative research projects and has also supported explorations of new ideas and research topics. Several undergrad students at Lafayette College (advised by CoPD Ospina-Giraldo) and Franklin & Marshal College (advised by CoPD Blair):These students have gained research experience through this project. They have engaged in research on identifying and characterizing the Phytophthora genes encoding carbohydrate-active enzymes, survey of local Oomycete diversity, and/or genomic data mining for the identification of new molecular markers for population genetics and phylogenetic analyses of Phytophthora. Changes/Problems: Nothing Reported What opportunities for training and professional development has the project provided? See above. How have the results been disseminated to communities of interest? Data resulted from individual student research have been shared with members of relevant scientific communities mainly through publication and also through meeting presentations. What do you plan to do during the next reporting period to accomplish the goals? This is the final report. We will share our experiences with others who plan to develop a similar training program.

Impacts
What was accomplished under these goals? The main goal of this graduate training program was to educate broadly-trained researchers in microbiology with a focus on microbial functional and evolutionary genomics and bioinformatics so that they contribute to solving current and emerging problems faced by the nation's agricultural, food and environmental systems. The PDs, other participants and their collaborators have brought diverse expertise and perspectives to this program, which helped students to gain broad perspectives in microbial genomics, evolutionary biology and informatics and develop professional skills and ethics. More than 20 Ph.D. students in nine graduate programs at Penn State have been supported by this training grant. Matching funds from various programs at Penn State enabled us to support this many students. Many of them completed their degree and currently work as a postdoc in a university or USDA-ARS. One graduate found a job in a biotech company.

Publications

• Type: Journal Articles Status: Published Year Published: 2014 Citation: Kang, S. (2014) Plant Pathology 2.0. Molecular Plant Pathology 15: 315318.
• Type: Journal Articles Status: Published Year Published: 2014 Citation: Short, D.P.G., ODonnell, K., and Geiser, D.M. (2014) Clonality, recombination, and hybridization in the plumbing-inhabiting human pathogen Fusarium keratoplasticum inferred from multilocus sequence typing. BMC Evolutionary Biology 14: 91.
• Type: Journal Articles Status: Published Year Published: 2014 Citation: Ramos, L.S., Lehman, B.L., Peter, K.A., and McNellis, T.W. (2014) Mutation of the Erwinia amylovora argD gene causes arginine auxotrophy, nonpathogenicity in apples, and reduced virulence in pears. Applied and Environmental Microbiology 80: 6739-6749
• Type: Journal Articles Status: Published Year Published: 2014 Citation: Demers, J.E., Garzon, C.D., and Jim�nez-Gasco, M.M. (2014) Striking genetic similarity between races of Fusarium oxysporum f. sp. ciceris confirms a monophyletic origin and clonal evolution of the chickpea vascular wilt pathogen. European Journal of Plant Pathology 139: 303-318.
• Type: Journal Articles Status: Published Year Published: 2014 Citation: Scully, E.D., Geib, S.M., Carlson, J.E., Tien, M., and Hoover, K. (2014) Functional genomics and microbiome profiling of the Asian longhorned beetle (Anoplophora glabripennis) reveal new insights into the digestive physiology and nutritional ecology of wood feeding beetles. BMC Genomics 15: 1096.
• Type: Book Chapters Status: Published Year Published: 2014 Citation: Kang, S., Demers, J., Jamenez-Gasco, M., and Rep, M. (2014) Fusarium oxysporum. pp. 99-119. In: R. Dean, A. Lichens-Park and K. Chittaranjan (eds.) Genomics of Plant-Associated Fungi and Oomycetes: Dicot Pathogens. Springer-Verlag, Berlin Heidelberg.

Progress 01/15/13 to 01/14/14

Outputs
Target Audience: The main group served by this training grant has been the Penn State PhD students supported by this training program. A few undergraduate students at Lafayette College and Franklin & Marshall College have been supported by this grant. The research questions, target organisms and approaches brought by the students in the program have been quite broad. Through this broadly-defined program, these students have acquired skills and knowledge to investigate the mechanisms underpinning the evolution and molecular and cellular processes of agriculturally important microbes using a combination of genomic data/tools and informatics tools. They also have learned to formulate solutions for practical problems that impact the nation’s agricultural, food and environmental systems as teams. Another group served by this project has been the PDs and their collaborators. This project has helped some of the participants in developing collaborative research projects and exploring new ideas. Changes/Problems: Nothing Reported What opportunities for training and professional development has the project provided? Meetings attended: 1. Erin Scully presented a poster entitled “Multitrophic Interactions Contribute to Lignocellulose Digestion and Nutritional Ecology in Larval Asian Longhorned Beetle (Anoplophora glabripennis)” at USDA-ARS-GFBRU, Lincoln, NE. 2. Erin Scully gave a seminar entitled “Plasticity of the Asian Longhorned Beetle (Cerambycidae: Anoplophora glabripennis) Gut Microbiome is Shaped by Plant-Insect Interactions” at Arkarachai Fungtammasan presented a poster entitled “RNA-DNA Differences at Microsatellites” at the 2013 Society for Molecular Biology and Evolution (SMBE) annual meeting in Chicago. 3. Joe Loquasto presented a poster entitled “Bifidobacterium animalis subsp. lactis ATCC 27673 is a genomically unique strain within this conserved subspecies” at the 2013 American Dairy Science Association (ADSA) Annual Meeting, Dairy Foods Division (Indianapolis, IN). 4. Laura Ramos presented a poster entitled “The fire blight pathogen Erwinia amylovora requires the rpoN gene for pathogenicity in apple” at the American Phytopathological Society Northeast Division conference, October 23-25, 2013, in Southbury, CT. 5. Josh Herr attended the 98th ESA Annual Meeting, August 4-9, 2013, Minneapolis Convention Center, Minneapolis, MN and presented a talk entitled “Managing for fungi in agroecosystems: What we know and where we will go.” 6. Vasileios Bitas presented a poster entitled “Fusarium oxysporum produces volatile organic compounds that enhance the growth and stress resistance of Arabidopsis thaliana” at the 2013 Fungal Genetics Conference, Asilomar, CA. 7. Venky Moktali and Bongsoo Park presented a poster entitled “Fungal Calcium Signaling Database (FCSD)” at the 2013 Fungal Genetics Conference, Asilomar, CA. 8. Venky Moktali presented a poster entitled “Evolutionary genomic analysis of cytochrome P450 proteins in the subphyla Pezizomycotina” at the 2013 Fungal Genetics Conference, Asilomar, CA. 9. Two undergraduate students at Franklin & Marshall College, LS Coffua and ST Veterano, under the supervision of PD Jaime Blair presented a poster entitled “Biodiversity and potential pathogenicity of field collected oomycetes from asymptomatic soybeans in southeastern PA” at the 2013 APS meeting, Austin, TX. Others: 1. A campus-wide interdisciplinary symposium on Environmental Microbiology sponsored by the Department of Plant Pathology and Environmental Microbiology, the College of Agricultural Sciences, and the Huck Institute of the Life Sciences was held in 2013. More than 90 students, postdocs, and faculty from four colleges and two satellite campuses of Penn State attended the symposium, with 24 oral presentations by faculty and 35 posters. Dr. Rita Colwell, Distinguished Professor at the University of Maryland and at John Hopkins University, and Director of the National Science Foundation from 1998-2004, presented the morning keynote address. The afternoon keynote address was presented by Dr. Regina Redman, the founder of Adaptive Symbiotic Technologies. Most students and PDs participating in the training program attended this symposium. 2. Jihye Park earned the graduate school teaching certificate from Penn State University in 2013. How have the results been disseminated to communities of interest? Research findings have been published in peer reviewed journals or presented during scientific meetings. Three databases have been developed or updated, and two of them are open to the public. What do you plan to do during the next reporting period to accomplish the goals? 1. The training grant will support the second campus-wide interdisciplinary symposium on Environmental Microbiology in 2014. 2. Support student travels to professional meetings and outreach activities. 3. Invite speakers who can help students’ professional development.

Impacts
What was accomplished under these goals? Graduation: Eight students supported by the training program successfully defended their PhD thesis in 2013. These included Bongsoo Park, Jihye Park and Venky Moktali (Bioinformatics & Genomics), Jill Demers (Plant Pathology), Josh Herr (Plant Biology), Lori Shapiro (Entomology), Joe Loquasto (Food Science), and Erin Scully (Genetics). They currently work as postdoc in universities (B. Park, J. Park, J. Herr, J. Loquasto and V. Moktali) and USDA-ARS (J. Demers and E. Scully). Awards & Services: 1. Erin Scully taught a workshop entitled “Analysis of metagenomic data using the programmother” at University of Hawaii-Hilo in2013. 2. Erin Scully received Sahakian Family Travel award $300 for travel to Entomological Society of America and two Genetics travel awards at $900 and $250. 3. Arkarachai Fungtammasan received two travel awards, which supported his attendance to 2013 Society for Molecular Biology and Evolution (SMBE) annual meeting in Chicago. 4. Arkarachai Fungtammasan served as president of the student organization of Bioinformatics and Genomics at Penn State (GENOMIX). 5. Jihye Park gave an invited talk for the workshop in the Food Science Department at Penn State on comparative phylogenomic analysis tools and beyond in 2013. 6. Laura Ramos received a 2013-14 Penn State College of Agricultural Sciences' Graduate Student Competitive Grant. Laura's proposal, entitled Novel Virulence Genes in Erwinia amylovoa, the Fire Blight Pathogen, was selected as one of ten proposals throughout the College to receive this award.

Publications

• Type: Journal Articles Status: Published Year Published: 2013 Citation: Park, B., Martin, F., Geiser, D. M., Kim, H.-S., Mansfield, M. A., Nikolaeva, E., Park, S.-Y., Coffey, M. D., Russo, J., Kim, S. H., Abad, G., Burgess, T., Gr�nwald, N., K., Cheong, J., Choi, J., Lee, Y.-H., and Kang, S. (2013) Phytophthora Database 2.0: Update and future direction. Phytopathology 103: 1204-1208.
• Type: Journal Articles Status: Published Year Published: 2013 Citation: Bitas, V., Kim, H.-S., Bennett, J., and Kang, S. (2013) Sniffing on microbes: Diverse roles of microbial volatile organic compounds in plant health. Molecular Plant-Microbe Interactions 26: 835843.
• Type: Journal Articles Status: Published Year Published: 2013 Citation: Ramos, L. S., Lehman, B. L., Sinn, J. P., Pfeufer, E. E., Halbrendt, N. O., and McNellis, T. W. (2013) The fire blight pathogen Erwinia amylovora requires the rpoN gene for pathogenicity in apple. Molecular Plant Pathology 14:838-843
• Type: Journal Articles Status: Published Year Published: 2013 Citation: Loquasto JR, Barrangou R, Stahl B, Dudley EG, Roberts RF. (2013). Bifidobacterium animalis subsp. lactis ATCC 27673 is a genomically unique strain within this conserved subspecies. Applied and Environmental Microbiology 79 (22): 6903-6910.
• Type: Journal Articles Status: Published Year Published: 2013 Citation: Scully, ED, Hoover, K, Carlson, JE, Tien, M, and Geib, SM. (2013) Midgut transcriptome profiling of Anoplophora glabripennis, a lignocellulose degrading, wood-boring cerambycid. BMC Genomics, 14 (850): doi:10.1186/1471-2164-14-850.
• Type: Journal Articles Status: Published Year Published: 2013 Citation: Scully, ED, Geib, SM, Hoover, K, Tien, M, Tringe, S, Barry, K, Herr, JR, and Carlson, JE. 2013. Comparative metagenomic profiling reveals lignocellulose degrading system in microbial community associated with a wood-feeding beetle. PLoS One 8(9): e73827.
• Type: Journal Articles Status: Published Year Published: 2013 Citation: Chung, S.H., Rosa, C., Scully, E.D., Peiffer, M., Tooker, J.F., Hoover, K., Luthe, D.S., Felton, G.W., (2013) Herbivore exploits orally secreted bacteria to suppress plant defenses. Proceedings of the National Academy of Sciences USA 110, 15728-15733.
• Type: Book Chapters Status: Published Year Published: 2013 Citation: Herr, JR and Carlson, JE. (2013) Traditional Breeding, Genomics-Assisted Breeding, and Biotechnological Modification of Forest Trees and Short Rotation Woody Crops. In Wood-Based Energy in the Northern Forests (pp. 69-89). Springer New York.
• Type: Journal Articles Status: Published Year Published: 2013 Citation: Emilie Tisserant, Mathilde Malbreil, Alan Kuo, Annegret Kohler, Aikaterini Symeonidi, Raffaella Balestrini, Philippe Charron, Nina Duensing, Nicolas Frei dit Frey, Vivienne Gianinazzi-Pearson, Luz B Gilbert, Yoshihiro Handa, Joshua R Herr, Mohamed Hijri, Raman Koul, Masayoshi Kawaguchi, Franziska Krajinski, Peter J Lammers, Frederic G Masclaux, Claude Murat, Emmanuelle Morin, Steve Ndikumana, Marco Pagni, Denis Petitpierre, Natalia Requena, Pawel Rosikiewicz, Rohan Riley, Katsuharu Saito, H�l�ne San Clemente, Harris Shapiro, Diederik Van Tuinen, Guillaume B�card, Paola Bonfante, Uta Paszkowski, Yair Y Shachar-Hill, Gerald A Tuskan, Peter W Young, Ian R Sanders, Bernard Henrissat, Stefan A Rensing, Igor V Grigoriev, Nicolas Corradi, Christophe Roux, Francis Martin. (2013) Genome of an arbuscular mycorrhizal fungus provides insight into the oldest plant symbiosis. Proceedings of the National Academy of Sciences USA 110: 20117-20122.
• Type: Journal Articles Status: Published Year Published: 2013 Citation: Yin, S., Faustman, C., Tatiyaborworntham, N., Ramanathan, R., Sun. Q., Maheswarappa, N.B., Mancini, R.A. (2013) The effects of HNE on ovine oxymyoglobin redox stability in a microsome model. Meat Sci. 95:224-228.
• Type: Journal Articles Status: Published Year Published: 2013 Citation: Hester, S.E., Park, J., Goodfield, L.L., Feaga, H.A., Preston, A., and Harvill, E.T. Horizontally acquired divergent O-antigen contributes to escape from cross-immunity in the classical bordetellae (2013) BMC Evolutionary Biology. 13(1): 209.
• Type: Journal Articles Status: Published Year Published: 2013 Citation: Shabbir, M.Z., Park, J., Muhammad, K., Rabbani, M., Rana, M.Y., and Harvill, E.T. Culture independent analysis of respiratory microbiome of houbara bustard (Chlamydotis undulata) revealed organisms of public health significance (2013) International Journal of Agriculture & Biology. 16: 222-226
• Type: Journal Articles Status: Published Year Published: 2013 Citation: Heyman F, Blair JE, Persson L, Wikstrom M. (2013) Root rot of pea and faba bean in southern Sweden caused by Phytophthora pisi, sp. nov. Plant Disease 97(4): 462-471.
• Type: Journal Articles Status: Published Year Published: 2013 Citation: Yin, S., Jensen, M. A., Bai, J., DebRoy, C., Barrangou, R. and Dudley, E. G. (2013) Evolutionary divergence of Shiga toxin-producing Escherichia coliis reflected in CRISPR spacer composition. Applied and Environmental Microbiology 79:5710-5720.

Progress 01/15/12 to 01/14/13

Outputs
OUTPUTS: Among the first group of 11 students, two graduated in 2011, four graduated in 2012, and three will graduate in May 2013. A request for proposal was sent out to select new students in 2012. Each proposal was evaluated by 3-4 graduate students as well the Project Directors based on the following criteria: i) innovation and intellectual merit of the proposed research; ii) relevance of the proposed research to the program goals; and iii) potential for success and resulting impact (e.g., past accomplishment, practical and/or fundamental importance of the problem(s) studied, how resulting data will help others). Seven students in six graduate programs were selected as the second cadre of this training program and will be supported for up to four semesters. One of the students, Laura Ramos (Ph.D. candidate in Plant Pathology) came from an underrepresented group. Besides publishing 10 peer-reviewed journal articles and one book chapter (see Publications), they have engaged in diverse service and professional development activities and have been recognized: 1. Liron Bendor served as Treasurer for the Genetics Graduate Student Association from 2011-2012 and currently is President of the Genetics Graduate Student Association. She received the Pathobiology Poster Presentation Award at the Penn State Pathobiology Retreat and the College of Agricultural Science grant. 2. Jill Demers received American Phytopathology Society Foundation travel award. 3. Heather Feaga received an honorable mention for her NSF fellowship proposal. She also conducted a workshop in microbiology for underprivileged middle schoolers. 4. Josh Herr received the Laurel Haven Endowment Scholarship, a Partner University Fund, Research Extension Award, and a New Phytologist Symposium Travel Award. 5. Venky Moktali was a member of the finalist team at the Dow Sustainability Innovation Challenge Award 2012 for the project titled "Mycoremediation: Decontaminating the Niger Delta." 6. Bongsoo Park received a CyberScience Summer Student Research award from the Penn State Institute for CyberScience. 7. Jihye Park served as co-founder and president of the student organization of Bioinformatics and Genomics at Penn State (GENOMIX). 8. Laura Ramos received a Sloan Scholarship. PARTICIPANTS: Seogchan Kang as Project Director (PD) has managed the project in consultation with the four CoPDs at Penn state, including Ed Dudley (Food Science), John Carlson (Forest Resources), Eric Harvill (Veterinary & Biomedical Sciences), and Kateryna Makova (Biology). They have advised one or more of the students in the program. Two outside CoPDs include Jaime Blair (Biology at Franklin & Marshall College) and Manuel Ospina-Giraldo (Biology at Lafayette College) and have advised research projects by undergraduate students. Three faculty members at Penn State also participated in all program activities: Chobi DebRoy (E. coli Reference Center Director, Dept. Veterinary & Biomedical Sciences), David M. Geiser (Plant Pathology), and Vivek Kapur (Veterinary & Biomedical Sciences). The graduate students in the program during this report period are: Liron Bendor (Genetics; new student selected in 2012), Josh Herr (Plant Biology), Sara Hester (Molecular, Cellular, and Microbiology), Arkarachai Fungtammasan (Bioinformatics & Genomics; new student selected in 2012), Alexia T. Karanikas (Cell and Developmental Biology), Joe Loquasto (Food Science), Venky Moktali (Bioinformatics & Genomics), Bongsoo Park (Bioinformatics & Genomics; new student selected in 2012), Jihye Park (Bioinformatics & Genomics), Laura Ramos (Plant Pathology; new student selected in 2012), Erin Scully (Genetics; new student selected in 2012), Lori Shapiro (Entomology), Will Smallridge (Immunology and Infectious Diseases; new student selected in 2012), and Shuang Yin (Food Science; new student selected in 2012). TARGET AUDIENCES: The main group served by this project is the PhD students participating in this training program. The research questions, target organisms and approaches brought by the students in the program are quite broad. Through this broadly-defined program, these students have developed the ability to investigate the mechanisms underpinning the evolution and molecular and cellular processes of agriculturally important microbes using a combination of genomic data/tools and informatics tools. They also have learned to formulate solutions for microbe-related practical problems that impact the nation's agricultural, food and environmental systems as teams, using a combination of genomic data/tools and informatics tools. Another group served by this project is the PDs and their collaborators. This project has helped some of the participants in developing collaborative research projects and exploring new ideas. PROJECT MODIFICATIONS: Nothing significant to report during this reporting period.

Impacts
To fully harness the power of genomics for understanding the microbial traits of agricultural and environmental importance and their evolution, we need to integrate genomics with perspectives, knowledge and tools from other areas of science, particularly evolutionary biology, ecology, and informatics. Without such integration, translation of the data from microbial genomics into enhanced understanding of microbial processes and evolution and practical problem solving will be hampered. The research questions, target organisms and experimental approaches brought by the students and faculty into this training program are quite diverse, providing a multidisciplinary and collaborative learning environment. This environment has been conducive for educating the next generation of researchers and educators who are well versed in integrating data and tools in microbial genomics and informatics with those from other areas of science to answer fundamental questions and solve practical microbe-related problems. As demonstrated by the publication record and other accomplishments, many of the participating students have made an excellent progress. Our experience from this project will serve other institutions that aim to develop similar training programs.

Publications

• Ahuja, U., M. Liu, S. Tomida, J. Park, P. Souda, J. Whitelegge, H. Li, E. T. Harvill, J. Parkhill, and J. F. Miller. 2012. Phenotypic and Genomic Analysis of Hypervirulent Human-associated Bordetella bronchiseptica. BMC Microbiology 12: 167.
• Fedorova, N. D., V. Moktali, and M. H. Medema. 2012. Bioinformatics approaches and software for detection of secondary metabolic gene clusters. Fungal Secondary Metabolism. Methods in Molecular Biology. Springer Publications. ISBN 978-1-62703-121-9.
• Fungtammasan, A., E. Walsh, F. Chiaromonte, K. A. Eckert, and K. D. Makova. 2012. A Genome-wide Analysis of Common Fragile Sites: What Features Determine Chromosomal Instability in the Human Genome Genome Research 22: 993-1005.
• Geib, S. M., E. D. Scully, M. M. Jimenez-Gasco, J. E. Carlson, M. Tien, and K. Hoover. 2012. Phylogenetic analysis of Fusarium solani associated with the Asian longhorned beetle, Anoplophora glabripennis. Insects 3: 141-160.
• Herr, J. R. 2012. Cryptococcus: From Human Pathogen To Model Yeast. Inoculum 63: 22.
• Moktali, V., J. Park, N. Fedorova-Abrams, B. Park, J. Choi, Y-H. Lee, and S. Kang. 2012. Systematic and searchable classification of cytochrome P450 proteins encoded by fungal and oomycete genomes. BMC Genomics 13: 525. http://dx.doi.org/10.1186/1471-2164-13-525.
• O'Donnell, K., R. A. Humber, D. M. Geiser, S. Kang, B. Park, V. A. Robert, P. W. Crous, P. R. Johnston, T. Aoki, A. P. Rooney, and S. A. Rehner. 2012. Phylogenetic diversity of insecticolous fusaria inferred from multilocus DNA sequence data and their molecular identification via FUSARIUM-ID and Fusarium MLST. Mycologia 104(2): 427-445.
• Park, J., Y. Zhang, A. Buboltz, X. Zhang, S. C. Schuster, U. Ahuja, M. Liu, J. F. Miller, M. Sebaihia, S. D. Bentley, J. Parkhill, and E. T. Harvill. 2012. Comparative Genomics of the Classical Bordetella Subspecies: the Evolution and Exchange of Virulence-Associated Diversity amongst Closely Related Pathogens. BMC Genomics 13: 545.
• Scully, E. D., K. Hoover, J. Carlson, M. Tien, and S. M. Geib. 2012. Proteomic analysis of Fusaruim solani isolated from the Asian longhorned beetle, Anoplophora glabripennis. PLoS One 7: e32990.
• Shapiro, L. R., C. M. De Moraes, A. G. Stephenson, and M. C. Mescher. 2012. Pathogen effects on vegetative and floral odours mediate vector attraction and host exposure in a complex pathosystem. Ecology Letters 15: 1430-1438.
• Weyrich, L. S., O. Y. Rolin, S. J. Muse, J. Park, N. A. Spindale, M. J. Kennett, S. E. Hester, C. Chen, E. G. Dudley, and E. T. Harvill. 2012. A Type VI Secretion System Encoding Locus in Required for Bordetella bronchiseptica Immunomodulation and Persistence In Vivo. PLoS ONE 7: e45892.

Progress 01/15/11 to 01/14/12

Outputs
OUTPUTS: To fully harness the power of microbial genomics for understanding the traits of practical importance and their evolution, we need to integrate genomics with perspectives and knowledge from other areas of science, particularly evolutionary biology, ecology, and informatics. Without such integration, translation of the data from microbial genomics into enhanced understanding of microbiology and practical problem solving will be hampered. The goal of this graduate training program is to train PhD students in microbial functional and evolutionary genomics and informatics, while providing opportunities for learning about and solving current and emerging problems faced by the nation's agricultural, food and environmental systems. Among the first group of 11 Ph.D. students (seven graduate programs) in the program, three students graduated in 2011. A new request for proposal (RFP) was sent out to select current Penn State graduate students who use genomics and/or informatics approaches to study the biology of agriculturally important microbes (ranging from viruses to eukaryotic microbes) and/or microbe-associated problems faced by the nation's agricultural, food and environmental systems. In response to this RFP, we received 12 applications. Each proposal was reviewed by 3-5 graduate students as well the project directors of the project. Proposals were evaluated based on the following criteria: (1) Innovation and intellectual merit of the proposed research; (2) Relevance of the proposed research to the program goals; (3) Potential for success and resulting impact (e.g., past accomplishment, practical and/or fundamental importance of the problem(s) studied, how resulting data will help others); and (4) Preference is given to applicants who passed the candidacy exam and proposals involving collaborative research. Six students from five graduate programs were chosen as the second cadre of the program and started the program in 2012. PARTICIPANTS: Seogchan Kang as the lead project director (PD) managed the project. The four CoPDs at Penn state are Ed Dudley (Food Science), John Carlson (Forest Resources), Eric Harvill (Veterinary & Biomedical Sciences), and Kateryna Makova (Biology). They advise student(s) in the program and participate in managing the program. Two outside CoPDs include Jaime Blair (Biology at Franklin & Marshall College) and Manuel Ospina-Giraldo (Biology at Lafayette College) and advise research projects by undergraduate students. Three faculty members at Penn State also participate in all program activities: Chobi DebRoy (E. coli Reference Center Director, Dept. Veterinary & Biomedical Sciences), David M. Geiser (Plant Pathology), Vivek Kapur (Veterinary & Biomedical Sciences). Outside collaborators include Kirk Czymmek (University of Delaware), Reid Frederick (USDA-ARS), Venu Kalavacharla (Delaware State University), Seong H. Kim (PA Department of Agriculture), Yong-Hwan Lee (Seoul National University), Yin-Won Lee (Seoul National University), Laurene Levy (APHIS- PPQ-CPHST), Xingzhong Liu (Chinese Academy of Sciences), Zhaowei Liu (APHIS-PPQ-CPHST), Kerry Pedley (USDA-ARS), James Sweigard (DuPont), and Wei Zhang (National Center for Food Safety and Technology). Each participant represents one or more of the following five research focus areas: plant health (Blair, Carlson, Czymmek, Geiser, Frederick, Kalavacharla, Kang, Kim, YH Lee, X Liu, Z Liu, Levy, Ospina-Giraldo, Pedley, Sweigard), animal health (Czymmek, DebRoy, Geiser, Harvill, Kapur, YW Lee), food safety (DebRoy, Dudley, Geiser, Kapur, YW Lee, Zhang), metagenomics and phylogenomics (Carlson, Dudley, Geiser, Harvill, Kang, Kapur, X Liu, Makova), and evolutionary biology (Blair, Carlson, Dudley, Frederick, Geiser, Harvill, Kang, Makova, Ospina-Giraldo). TARGET AUDIENCES: The main group served by this project is the students participating in the program. Through this broadly-defined program, students will develop the ability to investigate the mechanisms underpinning the evolution and molecular and cellular processes of agriculturally important microbes using a combination of genomic data/tools and informatics tools. They will also formulate solutions for microbe-related practical problems that impact the nation's agricultural, food and environmental systems as teams, using a combination of genomic data/tools and informatics tools. Another group served by this project is the PDs and their collaborators. This project has helped this group develop collaborative research projects. Our experience from this project will also serve other at Penn State and other institutions in developing similar training programs. PROJECT MODIFICATIONS: Nothing significant to report during this reporting period.

Impacts
The research questions, target organisms and experimental approaches brought by the students and faculty in the program are quite diverse, providing a multidisciplinary and innovative learning environment. This environment is conducive for educating the next generation of researchers and educators who are well versed in integrating data and tools in microbial genomics and informatics with those from other areas of science to answer fundamental questions and solve practical microbe-related problems. Besides the publications listed here, the students in the program accomplished the following: (1) Alexia T. Karanikas made four presentations and mentored a undergrad student; (2) Lori Shapiro and Jihye Park worked together to annotate the genome of the bacterial wilt pathogen Erwinia tracheiphila and presented a poster during the 2011 Penn State Bioinformatics & Genomics program retrea; (3) Jihye Park taught students from different graduate programs how to use new bioinformatics and genomics tools; (4) Jill Demers received an award through the Penn State College of Agricultural Sciences competitive grants program; (5) Dylan Short supervised a high school student research on the diversity of fungi isolated from eye infections in India; (6) Joe Loquasto won 3rd place in the Graduate Student Oral Paper Competition at the American Dairy Science Association annual meeting in New Orleans; (7) Venky Moktali was selected to attend the Otto Warburg Summer School and Research Symposium (OWS) on Evolutionary Genomics at the Max Planck Institute for Molecular Genetics, Berlin, Germany and presented a poster titled "Phylogenomic Analysis of Cytochrome P450 Proteins Using Fungal Cytochrome P450 Database (FCPD) 1.2." Venky also interned at J. Craig Venter Institute during May-August. He worked on identifying heterokaryon incompatibility (HET) genes in eight strains of Aspergillus fumigatus and carried out genome annotation of Aspergillus parasiticus; and (8) Josh Herr received five awards, including American Association for the Advancement of Science Program for Graduate Excellence in Science Award, New Phytologist Symposium Award from the New Phytologist Trust, Tag Along International Travel Award from Penn State, and Young Investigator Award from the American Association for Diabetes & Keystone Symposia on Molecular & Cellular Biology.

Publications

• Barakat, A., N. B. M. Yassin, J. Park, A. Choi, J. R. Herr, and J. E. Carlson. 2011. Comparative and phylogenomic analyses of cinnamoyl-CoA reductase and cinnamoyl-CoA-reductase-like gene family in land plants. Plant Science 181:249-257.
• Herr, J. R. 2011. Bioenergy From Trees. New Phytologist 192(2):313-315.
• Loquasto, J. R., R. Barrangou, E. G. Dudley, and R. F. Roberts. 2011. The complete genome sequence of Bifidobacterium animalis subspecies animalis ATCC 25527(T) and comparative analysis of growth in milk with B. animalis subspecies lactis DSM 10140(T). J Dairy Sci. 94(12):5864-5670.
• Rhodes, M. E., J. R. Spare, A. Oren, and C. M. House. 2011. Differences in lateral gene transfer in hypersaline versus thermal environments, BMC Evolutionary Biology, 2011 11:199.
• Short, D. P. G., K. O'Donnell, N. Zhang, J. H. Juba, and D. M. Geiser. 2011. Widespread occurrence of human pathogenic types of the fungus Fusarium detected in plumbing drains, J. of Clin Microbiology, 2011 49(12):4264-4272.

Progress 01/15/10 to 01/14/11

Outputs
OUTPUTS: To jump-start the program, we issued a request for proposal (RFP) to current Penn State graduate students. In response to this RFP, we received 17 applications. Proposals were evaluated based on the following criteria: (i) relevance of the proposed research to the program goals; (ii) innovation and intellectual merit of the proposed research; (iii) potential for success and scientific and practical impact of the proposed research; and (iv) past accomplishment. Eleven students from seven graduate programs in three colleges were chosen as the first cadre of the program and are supported for up to two years based on academic performance and contribution to the program goals. Some of the chosen students are supported by the matching assistantships from Penn State. Penn State committed a significant amount of matching funds (6.5 assistantships each year for four years) to support this program, which allowed us to support more students than the project budget allows. We began meeting every other week for three months to learn about the scope of research in each of the participating labs and students and to stimulate the development of collaborative projects among them. The program also began supporting professional development of the students (short-term visits to outside labs or meetings and cosponsoring a minisymposium titled Challenges in Understanding and Managing Oomycetes on May 27, 2010). CoPD Ospina-Giraldo at Lafayette College recruited two undergrad students who worked on identifying the genes coding for carbohydrate-active enzymes (CAZymes) from Phytophthora during Summer 2010. CoPD Blair at Franklin & Marshal College has advised three undergrad students in a survey of local Oomycete diversity. CoPD Blair has also recruited two students to perform genomic data mining for the identification of new molecular markers for population genetics and phylogenetic analyses of Phytophthora. PARTICIPANTS: Seogchan Kang as the lead project director managed the project. The four CoPDs at Penn state are Ed Dudley (Food Science), John Carlson (Forest Resources), Eric Harvill (Veterinary & Biomedical Sciences), and Kateryna Makova (Biology). They advised one or more of the students in the program and participated in managing the program. Two outside CoPDs include Jaime Blair (Biology at Franklin & Marshall College) and Manuel Ospina-Giraldo (Biology at Lafayette College) and advised research projects by undergraduate students. Three faculty members at Penn State also participate in all program activities: Chobi DebRoy (E. coli Reference Center Director, Dept. Veterinary & Biomedical Sciences), David M. Geiser (Plant Pathology), Vivek Kapur (Veterinary & Biomedical Sciences). Outside collaborators include Kirk Czymmek (University of Delaware), Reid Frederick (USDA-ARS), Venu Kalavacharla (Delaware State University), Seong H. Kim (PA Department of Agriculture), Yong-Hwan Lee (Seoul National University), Yin-Won Lee (Seoul National University), Laurene Levy (APHIS- PPQ-CPHST), Xingzhong Liu (Chinese Academy of Sciences), Zhaowei Liu (APHIS-PPQ-CPHST), Kerry Pedley (USDA-ARS), James Sweigard (DuPont), and Wei Zhang (National Center for Food Safety and Technology). Each participant represents one or more of the following five research focus areas: plant health (Blair, Carlson, Czymmek, Geiser, Frederick, Kalavacharla, Kang, Kim, YH Lee, X Liu, Z Liu, Levy, Ospina-Giraldo, Pedley, Sweigard), animal health (Czymmek, DebRoy, Geiser, Harvill, Kapur, YW Lee), food safety (DebRoy, Dudley, Geiser, Kapur, YW Lee, Zhang), metagenomics and phylogenomics (Carlson, Dudley, Geiser, Harvill, Kang, Kapur, X Liu, Makova), and evolutionary biology (Blair, Carlson, Dudley, Frederick, Geiser, Harvill, Kang, Makova, Ospina-Giraldo). The outside Co-PDs and collaborators are expected to work with the Penn State participants and students to integrate their research interests with our students' thesis projects, and will host students as short- and long-term interns. During this period, their involvement was limited, mainly because the focus has been on initiating the program. TARGET AUDIENCES: The main group served by this project is the students participating in the program. Through this broadly-defined program, students will develop the ability to investigate the mechanisms underpinning the evolution and molecular and cellular processes of agriculturally important microbes using a combination of genomic data/tools and informatics tools. They will also formulate solutions for microbe-related practical problems that impact the nation's agricultural, food and environmental systems as teams, using a combination of genomic data/tools and informatics tools. Another group served by this project is the PDs and their collaborators. This project will help this group to develop collaborative research projects and a formal graduate degree program in microbiology at Penn Sate. Our experience from this project will serve other institutions that have similar educational interests, as we would be happy to share our experience. PROJECT MODIFICATIONS: Nothing significant to report during this reporting period.

Impacts
The research questions, target organisms and experimental approaches brought by the students and faculty in the program are quite diverse, providing a multidisciplinary and innovative learning environment. This environment is conducive for educating the next generation of researchers and educators who are well versed in integrating data and tools in microbial genomics and informatics with those from other areas of science to answer fundamental questions and solve practical microbe-related problems. Besides the publications listed here, the students in the program accomplished the following: (1) Alexia T. Karanikas received an American Heart Association Predoctoral fellowship and presented a poster at the 2010 International Bordetella Symposium; (2) Jihye Park presented her work at the 9th International Bordetella Symposium. She received Wellcome Trust Travel Award, Huck Institutes Travel Award, and International Bordetella Symposium Travel Award. In addition, she visited the Wellcome Trust Sanger Institute in England. She taught students from different graduate programs how to use new bioinformatics and genomics tools; (3) Jill Demers received the L. Earl and Veronica Casida Scholarship in Plant Pathology and conducted a summer internship in a potato breeding program; (4) Matthew Rhodes was a panel speaker on origin of life to the public and the University of Colorado Boulder Astrobiology club and gave a seminar at Colorado School of Mines; (5) Josh Herr spent four months studying the microbial diversity of forest soils using high-throughput genome sequencing techniques at Nancy-INRA (France) and received a competitive grants program award from the College of Agricultural Sciences at Penn State; (6) Dylan Short presented his research on the widespread occurrence of human pathogenic Fusarium species in plumbing systems in the U.S. at the Mycological Society of America's annual meeting and also began working on a collaborative research project with scientists in the Department of Ophthalmology at Case Western Reserve University investigating the diversity of fungi isolated from eye infections in India; and (6) Venky Moktali visited Seoul National University in Korea for three months to conduct research on the evolution of fungal P450 enzymes. We plan to develop projects that these students can work together to experience team-based problem solving. The first project will likely to be annotating genome sequences of >100 strains of pathogenic E. coli and Erwinia tracheiphila, which have been generated by two labs participating in this program. We plan to recruit a few more students from the incoming class of graduate students.

Publications

• Long, G. H., A. T. Karanikas, E. T. Harvill, A. F. Read, and P. J. Hudson. 2010. Acellular pertussis vaccination facilitates Bordetella parapertussis infection in a rodent model of bordetellosis. Prococeedings of the Royal Society. Biological Sciences 277:2017-2025.
• Wolfe, D. N., A. T. Karanikas, S. E. Hester, M. J. Kennett, and E. T. Harvill. 2010. Interleukin-10 Induction by Bordetella parapertussis Limits a Protective Interferon Response. Journal of Immunology 184:1392-1400.
• Rhodes, M.E., S. T. Fitz-Gibbon, A. Oren, and C. H. House. 2010. Amino acid signatures of salinity on an environmental scale with a focus on the Dead Sea. Environmental Microbiology 12:2613-2623.