Macroscopic similarities cloak microscopic differences in bacterial – host interactions

It’s plainly clear that sick hosts are fundamentally altered by infection and disease progression. However, it remains unknown how changes to the host create new and preferred niches for organisms beyond the infecting pathogen and influence bacterial dynamics as phytopathogenic bacteria arrive on a leaf as immigrants and then eventually establish themselves in the apoplast which they use as an infection court or encounter established populations. We study the single host, tomato, and dual pathosystems, bacterial spot caused by Xanthomonas gardneri and bacterial speck caused by Pseudomonas syringae pv. tomato. These phytopathogens lack cell wall degrading enzymes and abandon the leaf surface and enter the leaf interior via stomata prior to initiating infection. Although macroscopic symptoms are similar between these two pathogens, we found the timing of symptom development and microscopic differences in host physiology are pathogen-dependent. Furthermore these differences affect immigrants to the infected apoplast.

Fundamental changes to infection courts by pathogens create novel niches for other microbes.

 Although the primary purpose of altering the plant environment during infection is likely for the benefit of the pathogen, sweeping changes in physical and biochemical characteristics of the host undoubtedly also reshape the composition of the bacterial community in an infection court. We have found that the dramatic change to the apoplast as a result of X. gardneri infection creates an available and habitable niche for bacteria that are usually precluded from stomatal entry and exiled to the leaf surface, such as S. enterica.

Expanding our investigation of how leaf infection changes the host, we examined whether bacteria that create water congested apoplast during infection, in general, permit leaf surface bacteria entry to this altered niche. We recently discovered that P. syringae pv tomato infection failed to permit S. enterica entry to the apoplast but most surprising, a subsequent immigration population of P. syringae pv tomato could also not join the infecting population established in the apoplast. In contrast, immigrating X. gardneri cells successfully incorporate into an established X. gardneri apoplast infection. These results support two possible outcomes that we plan to investigate: 1) changes to the apoplast of a P. syringae-infected plant results in a different carrying capacity or temporal difference than one of a X. gardneri-infected plant and/or 2) changes to the apoplast of a X. gardneri-infected plant can host a variety of bacteria from the leaf surface whereas the apoplast of a P. syringae-infected plant is limited to supporting the infecting population.

(Dr. Vicky Lason Harrod, Megan Dixon, Ellie Guilemette, Soniz Zaacks, Dr. Jeri Barak, Dr. Kim Cowles, and Natalie Wieber)

Courses Taught by Dr. Jeri Barak

PP311 Global Food Security

PP 375,  Food Security Deep Dive, is the anchor course for the Global Food Security First-Year Interest Group and meets with PP 311. This learning community has a history of being dynamic and each year, a close knit group that often develops that lasts throughout their time at UW-Madison.

GFS FIG students bring their passion for food security in a myriad of ways, even after their first semester at UW-Madison. In 2013, GFS FIG students brought the documentary, Give a Damn? to UW-Madison. A feature length documentary about three friends, two idealistic activists and one skeptic, attempting to live in poverty, on $1.25 a day, across 3 continents. The adventure takes a devastating turn when two of them survive a deadly plane crash in Africa, and all three must fight to finish what they started.

Food insecurity is a local issue too, including UW-Madison. Food assistance is available in several forms on campus: Food Recovery Network, Slow Food UW featuring 2014 GFS FIG student volunteer, Harvest Handouts, and The Open Seat.

In 2019, the Student Organic Farm UW Organic Collaborative was born, thanks to the hard work of GFS FIG student, Sofia Weinstein, the word is spreading. 2021-2022 Sofia took charge of the collaborative’s media presence and merged her skills developed as a double major, Plant Pathology and Agriculture & Applied Economics, to demonstrate the feasibility of a food truck as a buyer for the Student Organic Farm which will contribute to UW-Madison’s sustainability and local food system. Thus, the UW Electric Food Truck will launch April, 2022.

A GFS FIG student (2016) was motivated to secure a Wisconsin Idea Fellowship from UW–Madison’s Morgridge Center for Public Service to fund her Patio Tomato Project with the objective to bring container gardening to food insecure folks in Madison, focusing on kids.

Kimberly N Cowles, Arjun S Iyer, Iain McConnell, Ellie G Guillemette, Dharshita Nellore, Sonia C Zaacks, Jeri D Barak. Established Pseudomonas syringae pv. tomato infection disrupts immigration of leaf surface bacteria to the apoplast. bioRxiv. Link

Megan H. Dixon, Dharshita Nellore, Sonia C. Zaacks, Jeri D. Barak. 2024. Time of arrival during disease progression and humidity additively influence Salmonella enterica colonization of lettuce. Appl. Environ. Microbiol. Link.

Megan H. Dixon, Victoria L. Harrod, Russell Groves, Ellie Guillemette, Jeri Barak. 2023. The “friends” that help dangerous bacteria get into your salad. Front Young Minds. Link

Adam F. Bigott, Samuel F. Hutton, Gary Vallad, Richard Lankau, Jeri D. Barak. 2023. Narrow, but not broad, spectrum resistance and disease reshape phyllosphere bacterial communities. bioRxiv. Link.

Megan H. Dixon, Kimberly N. Cowles, Sonia C. Zaacks, Isabel N. Marciniak, Jeri D. Barak. 2022. Xanthomonas infection transforms the apoplast into an accessible and habitable niche for Salmonella enterica. Appl. Environ. Microbiol. Link.

Victoria L. Harrod, Russell Groves, Ellie Guillemette, Jeri Barak. 2022. Give and Take: Salmonella enterica alters Macrosteles auadrilineatus feeding behaviors resulting in altered S. enterica populations and distribution on leaves. Sci Rep 12, 8544 Link.

Kimberly N. Cowles, Anna K. Block, Jeri D. Barak. 2022. Xanthomonas hortorum pv. gardneri TAL effector AvrHah1 is necessary and sufficient for increased persistence of Salmonella enterica on tomato leaves. Sci Rep 12, 7313. Link

Harrod, V.L., Groves, R.L., Maurice, M.A., and Barak J.D. 2021. Frankliniella occidentalis facilitate Salmonella enterica survival in the phyllosphere. PLoS ONE 16(2): e0247325. Link.

Nicola Holden, László Kredics, Jeri Barak. 2020. Editorial for the thematic issue, “Human Pathogens in the Environment.” FEMS Microbiol Letters Link

Cowles, K.N, Groves, R.L., and Barak, J.D. 2018. Leafhopper-induced activation of the jasmonic acid response benefits Salmonella enterica in a flagellum-dependent manner. Front. Microbiol. doi: 10.3389/fmicb.2018.01987 Link

Grace Kwan, Brett Plagenz, Kimberly Cowles, Tippapha Pisithkul, Daniel Amador-Noguez, and Jeri D. Barak. 2018. Few Differences in metabolic network use found between Salmonella enterica colonization of plants and typhoidal mice. Front. Microbiol. doi: 10.3389/fmicb.2018.00695 Link

Dundore-Arias JP and Barak JD. 2017. “Plant Associated Foodborne Pathogens.” In: A.P. Keinath, W.M. Wintermantel, and T.A. Zitter (Eds.), Compendium of Cucurbit Diseases and Pests (pp. 17-19). APS Press, St. Paul.

Jeri D. Barak, Taca Vancheva, Pierre Lefeuvre, Jeffrey B. Jones, Sujan Timilsina, Gerald V. Minisavage, Gary E. Vallad, and Ralf Koebnik. 2016. Whole-genome sequences of Xanthomonas euvesicatoria strains clarify taxonomy and reveal a stepwise erosion of type 3 effectors. Front. Plant  Sci.doi: 10.3389/fpls.2016.01805 Link

Cowles KN, Willis DK, Engel TN, Jones JB, and Barak J.D. 2016. Diguanylate cyclases, AdrA and STM1987, regulate Salmonella enterica exopolysaccharide production during plant colonization in an environment-dependent manner. Appl Environ Microbiol. 82(4): 1237-1248. Link

Dundore-Arias JP and Barak JD.2015. “Food Safety.” In: K.V. Subbarao, R.M. Davis, R.L. Gilbertson, and R.N. Raid (Eds.), Compendium of Lettuce Diseases and Pests (pp. 22-24). APS Press, St. Paul.

Potnis, N., Colee, J., Jones, J.B., and Barak, J.D. 2015. Plant pathogen induced watersoaking promotes Salmonella enterica growth on tomato leaves. Appl. Environ. Microbiol. 81(23): 8126-34. Link

Dundore-Arias, J.P., Groves, R.L. and Barak, J.D. 2015. Influence of prgH on the persistence of ingested Salmonella enterica in the leafhopper Macrosteles quadrilineatus. Appl. Environ. Microbiol. 81 (18): 6345-6354. Link

Schwartz AR, Potnis N, Timilsina S, Wilson M, Patané J, Martins J Jr., Minsavage GV, Dahlbeck D, Akhunova A, Almeida N, Vallad GE, Barak JD, White FF, Miller SA, Ritchie D, Goss E, Bart RS, Setubal JC, Jones JB and Staskawicz BJ 2015. Phylogenomics of Xanthomonas field strains infecting pepper and tomato reveals diversity in effector repertoires and identifies determinants of host specificity. Front. Microbiol. 6:535. Link

Potnis, N., Timilsina, S., Strayer, A., Shantharaj, D., Barak, J.D., Paret, M.L., Vallad, G.E., and Jones, J.B. 2015. Bacterial spot of tomato and pepper: diverse Xanthomonas species with a wide variety of virulence factors posing a worldwide challenge. Mol. Plant Pathol. Link

Kwan, G., Pisithkul, T., Amador-Noguez, D., and Barak, J.D. 2015. De novo amino acid biosynthesis contributes to Salmonella enterica growth in alfalfa seedling exudates.  Appl. Environ. Microbiol. 81(3): 861-73  Link

Soto-Arias, J.P., Groves, R.L., and Barak, J.D. 2014. Transmission and retention of Salmonella enterica by phytophagous hemipteran insects.  Appl. Environ. Microbiol. 80(17): 5447-5456. Link

Potnis, N., Soto-Arias, J.P., Cowles, K., van Bruggen, A.H.C., Jones, J.B., and Barak, J.D. 2014. Xanthomonas perforans colonization influences Salmonella enterica in the tomato phyllosphere. Appl. Environ. Microbiol. 80(10): 3173-3180. Link

Pollard, S., Barak, J.D., Royer, R., Grabau, E., Reiter, M., Gu, G., and Rideout, S. 2014. Potential interactions between Salmonella enterica and Ralstonia solanacearum in tomato plants. J. Food Prot 77(2): 320-324. Link

Soto-Arias, J.P., Groves, R.L., and Barak, J.D. 2013. Benefits of piercing and sucking, enhanced persistence of Salmonella enterica on plants due to phytophagous hemipterans. PLoS ONE 8(10): e79404. Link

Kwan, G., Charkowski, A.O., and Barak, J.D. 2013. Salmonella enterica moderates Pectobacterium carotovorum populations and virulence on lettuce. mBio. 4:e00557-12. Link

Jeri D. Barak and Brenda Schroeder. 2012. Interrelationships of Food Safety and Plant Pathology: The Life Cycle of Human Pathogens. Ann Rev Phytopathol 50: 241-266. Link

Hao, L., H. Andrews-Polymenis, M. McClelland, D. K. Willis, J. D. Barak. 2012. Salmonella enterica requires siderophore biosynthesis to colonize plants. Appl. Environ. Microbiol. 13:4561-4570. Link

Barak, J. D. 2012. The biggest food safety threat from the tiniest of crops. Cereal Foods World. 57(3): 123-124. Link

Courtney E. Jahn, Dija A. Selimi, Jeri D. Barak, and Amy O. Charkowski. 2011. The Dickeya dadantii biofilm matrix consists of cellulose nanofibers and is an emergent property dependent upon the type III secretion system and the cellulose synthesis operon. Microbiol. 157: 2733-2744. Link

Jeri D. Barak, Kramer, L., and Hao, L. 2011. Plant cultivar alters Salmonella enterica colonization of tomato and Type 1 trichomes are preferential colonization sites. Appl. Environ. Microbiol. 77(2): 498-504. Link

Jeri D. Barak, L. Gorski, Anita S. Liang, and Kohn-Eun Narm. 2009. Previously uncharacterized Salmonella enterica genes required for swarming play a role in plant colonization. Microbiol. 155: 3701-3709. Link

Teplitski, M., Barak, J., and Schneider, K. R. 2009. Human enteric pathogens in produce: un-answered ecological questions with direct implications for food safety. Curr. Opin. Biotech. 20(2): 166-71. Link

Csordas, A.T., M.J. Delwiche and J.D. Barak. 2008. Nucleic acid sensor and fluid handling for detection of bacterial pathogens. Sensors and Actuators B: Chemical. 134: 1-8. Link

Csordas, A.T., M.J. Delwiche and J.D. Barak. 2008. Automatic detection of Salmonella enterica in sprout irrigation water using a nucleic acid sensor. Sensors and Actuators B: Chemical. 134: 9-17. Link

Barak, J.D., A. S. Liang and K. Narm. 2008. Differential attachment and subsequent contamination of agricultural crops by Salmonella enterica. Appl. Environ. Microbiol. 74(17): 5568-5570. Link

Jeri D. Barak and Anita S. Liang. 2008. Role of soil, crop debris, and a plant pathogen in Salmonella enterica contamination of tomato plants. PLoS ONE 3(2): e1657. Link

Lermo, A., E. Zacco, J. Barak, M. Delwiche, S. Campoy, J. Barbe, S. Alegret and M.I. Pividor. 2008. Towards q-PCR of pathogenic bacteria with improved electrochemical double-tagged genosensing detection. Biosensors Bioelectronics. 23(12):1805-1811. Link

Mohle-Boetani, J., J. Farrar, P. Bradley, J. Barak, M. Miller, R. Mandrel, P. Mead, W. Keen, K. Cummings, S. Abbott and S. Benson Werner. 2008. Salmonella infections associated with mung bean sprouts: epidemiology and environmental investigations. Epidemiol. Inf. doi: 10.1017/S0950268808000411. Link

Barak, J.D., C.E. Jahn, D.L. Gibson and A.O. Charkowski. 2007. The role of cellulose, lipopolysaccharide O-polysaccharide, and O-antigen capsule in the colonization of plants by Salmonella enterica. Mol. Plant-Microbe Interact. 20:1083-1091. *Faculty of 1,000 recommended. Link

Barak, J., L. Gorski, P. Naraghi-Arani and A.O. Charkowski. 2005. Salmonella enterica virulence genes are required for bacterial attachment to plant tissue. Appl. Environ. Microbiol. 71:5685-5691. Link

Yap, M.-N, C.-H. Yang, J.D. Barak, C.E. Jahn and A.O. Charkowski. 2005. The Erwinia chrysanthemi type III secretion system is required for multicellular behavior. J. Bacteriol. 187:639-648. Link

Barak, J.D., K. Sananikone and M.J. Delwiche. 2005. Comparison of primers for detection of pathogenic E. coli using real-time PCR. Lett. Appl. Microbiol. 41:112-118. Link

Yap, M. N., Barak, J. D., and Charkowski, A. O. 2004. Genomic diversity of Erwinia carotovora subsp. carotovora and its correlation with virulence. Appl. Environ. Microbiol. 70: 3013-3023. Link

Csordas, A. T., Barak, J. D., and Delwiche, M. J. 2004. Comparison of primers for the detection of Salmonella enterica serovars using real-time PCR. Lett. Appl. Microbiol. 39: 187-193. Link

Barak, J. D., Chue, B., and Mills, D. 2003. Recovery of surface bacteria from and surface sanitization of cantaloupes. J. Food Prot. 66: 1805-1810. Link

Barak, J. D. and Gilbertson, R. L. 2003. Genetic diversity of Xanthomonas campestris pv. vitians, the causal agent of bacterial leafspot of lettuce. Phytopathology 93: 596-603. Link

Barak, J. D., Whitehand, L. C., and Charkowski, A. O. 2002. Differences in attachment of Salmonella enterica serovars and Escherichia coli O157:H7 to alfalfa sprouts. Appl. Environ. Microbiol. 68: 4758-4763. Link

Charkowski, A. O., Barak, J. D., Sarreal, C. Z., and Mandrell, R. E. 2002. Growth and colonization of Salmonella enterica and Escherichia coli O157:H7 on alfalfa sprouts and the effects of sprouting temperature, inoculum dose, and frequency of irrigation on bacterial levels. Appl. Environ. Microbiol. 68: 3114-3120. Link

Barak, J. D., Koike, S. T, and Gilbertson, R. L. 2002. Long-distance movement of Xanthomonas campestris pv. vitians in the stems of lettuce plants. Plant Pathology 51: 506-512. Link

Barak, J. D., Koike, S. T, and Gilbertson, R. L. 2001. Role of crop debris and weeds in the epidemiology of bacterial leaf spot of lettuce, caused by Xanthomonas campestris pv. vitians, in California. Plant Disease 85: 169-178. Link

Koike, S. T. *, Barak, J. D. *, Henderson, D. M., and Gilbertson, R. L. 1999. Bacterial blight of leek: a new disease in California caused by Pseudomonas syringae. Plant Disease 83: 165-170. *co-first authors. Link

Tomasky, G; Barak, J; Valiela, I; Behr, P; Soucy, L; Foreman, K. 1999. Nutrient limitation of phytoplankton growth in Waquoit Bay, Massachusetts, USA: a nutrient enrichment study. Aquat. Ecol. 33(2):147-155. Link