Microbiology Doctoral Training Program

Publications

The Microbiology Doctoral Training Program is a research-intensive academic program.  Our students are integral members of research teams, leading to a constant stream of well-respected published work.

Please see below for a list of papers published during the academic year 2019-2020 authored by MDTP students.

*Bold – Student; Underlined – PI

  1. Oh, J.-H., Alexander, L.M., Pan, M., Schueler, K.L., Keller, M.P., Attie, A.D., Walter, J., van Pijkeren, J.-P., 2019. Dietary Fructose and Microbiota-Derived Short-Chain Fatty Acids Promote Bacteriophage Production in the Gut Symbiont Lactobacillus reuteri. Cell Host Microbe 25, 273-284.e6. https://doi.org/10.1016/j.chom.2018.11.016
  2. Hendrikx, T., Duan, Y., Wang, Y., Oh, J.-H., Alexander, L.M., Huang, W., Stärkel, P., Ho, S.B., Gao, B., Fiehn, O., Emond, P., Sokol, H., van Pijkeren, J.-P., Schnabl, B., 2019. Bacteria engineered to produce IL-22 in intestine induce expression of REG3G to reduce ethanol-induced liver disease in mice. Gut 68, 1504–1515. https://doi.org/10.1136/gutjnl-2018-317232
  3. Oh, J.-H., Schueler, K.L., Stapleton, D.S., Alexander, L.M., Yen, C.-L.E., Keller, M.P., Attie, A.D., van Pijkeren, J.-P., 2020. Secretion of Recombinant Interleukin-22 by Engineered Lactobacillus reuteri Reduces Fatty Liver Disease in a Mouse Model of Diet-Induced Obesity. mSphere 5. https://doi.org/10.1128/mSphere.00183-20
  4. Romero-Masters, J.C., Huebner, S.M., Ohashi, M., Bristol, J.A., Benner, B.E., Barlow, E.A., Turk, G.L., Nelson, S.E., Baiu, D.C., Van Sciver, N., Ranheim, E.A., Gumperz, J., Sherer, N.M., Farrell, P.J., Johannsen, E.C., Kenney, S.C., 2020. B cells infected with Type 2 Epstein-Barr virus (EBV) have increased NFATc1/NFATc2 activity and enhanced lytic gene expression in comparison to Type 1 EBV infection. PLoS Pathog 16, e1008365. https://doi.org/10.1371/journal.ppat.1008365
  5. Bohr, L.L., Mortimer, T.D., Pepperell, C.S., 2020. Lateral Gene Transfer Shapes Diversity of Gardnerella spp. Front Cell Infect Microbiol 10, 293. https://doi.org/10.3389/fcimb.2020.00293
  6. Chevrette, M.G., Bratburd, J.R., Currie, C.R., Stubbendieck, R.M., 2019. Experimental Microbiomes: Models Not to Scale. mSystems 4. https://doi.org/10.1128/mSystems.00175-19
  7. Bultman, K.M., Cecere, A.G., Miyashiro, T., Septer, A.N., Mandel, M.J., 2019. Draft Genome Sequences of Type VI Secretion System-Encoding Vibrio fischeri Strains FQ-A001 and ES401. Microbiol Resour Announc 8. https://doi.org/10.1128/MRA.00385-19
  8. Guckes, K.R., Cecere, A.G., Wasilko, N.P., Williams, A.L., Bultman, K.M., Mandel, M.J., Miyashiro, T., 2019. Incompatibility of Vibrio fischeri Strains during Symbiosis Establishment Depends on Two Functionally Redundant hcp Genes. J Bacteriol 201. https://doi.org/10.1128/JB.00221-19
  9. Rotman, E.R., Bultman, K.M., Brooks, J.F., Gyllborg, M.C., Burgos, H.L., Wollenberg, M.S., Mandel, M.J., 2019. Natural Strain Variation Reveals Diverse Biofilm Regulation in Squid-Colonizing Vibrio fischeri. J Bacteriol 201. https://doi.org/10.1128/JB.00033-19
  10. Callaghan, M.M., Dillard, J.P., 2019a. Mucus Is a Key Factor in Neisseria meningitidis Commensalism. mSphere 4. https://doi.org/10.1128/mSphere.00777-19
  11. Callaghan, M.M., Dillard, J.P., 2019b. Transformation in Neisseria gonorrhoeae. Methods Mol Biol 1997, 143–162. https://doi.org/10.1007/978-1-4939-9496-0_10
  12. Voter, A.F., Callaghan, M.M., Tippana, R., Myong, S., Dillard, J.P., Keck, J.L., 2020. Antigenic Variation in Neisseria gonorrhoeae Occurs Independently of RecQ-Mediated Unwinding of the pilE G Quadruplex. J Bacteriol 202. https://doi.org/10.1128/JB.00607-19
  13. Koch, B., Callaghan, M.M., Tellechea-Luzardo, J., Seeger, A.Y., Dillard, J.P., Krasnogor, N., 2020. Protein interactions within and between two F-type type IV secretion systems. Mol Microbiol. https://doi.org/10.1111/mmi.14582
  14. Bi, Y., Cox, M.S., Zhang, F., Suen, G., Zhang, N., Tu, Y., Diao, Q., 2019. Feeding modes shape the acquisition and structure of the initial gut microbiota in newborn lambs. Environ Microbiol 21, 2333–2346. https://doi.org/10.1111/1462-2920.14614
  15. Li, W., Edwards, A., Riehle, C., Cox, M.S., Raabis, S., Skarlupka, J.H., Steinberger, A.J., Walling, J., Bickhart, D., Suen, G., 2019. Transcriptomics analysis of host liver and meta-transcriptome analysis of rumen epimural microbial community in young calves treated with artificial dosing of rumen content from adult donor cow. Sci Rep 9, 790. https://doi.org/10.1038/s41598-018-37033-4
  16. Sbardellati, D.L., Fischer, A., Cox, M.S., Li, W., Kalscheur, K.F., Suen, G., 2020. The bovine epimural microbiota displays compositional and structural heterogeneity across different ruminal locations. J Dairy Sci 103, 3636–3647. https://doi.org/10.3168/jds.2019-17649
  17. Firmino, F.C., Porcellato, D., Cox, M., Suen, G., Broadbent, J.R., Steele, J.L., 2020. Characterization of microbial communities in ethanol biorefineries. J Ind Microbiol Biotechnol 47, 183–195. https://doi.org/10.1007/s10295-019-02254-7
  18. Li, W., Edwards, A., Cox, M.S., Raabis, S.M., Skarlupka, J.H., Steinberger, A.J., Murphy, B., Larsen, A., Suen, G., 2020. Changes in the host transcriptome and microbial metatranscriptome of the ileum of dairy calves subjected to artificial dosing of exogenous rumen contents. Physiol Genomics 52, 333–346. https://doi.org/10.1152/physiolgenomics.00005.2020
  19. Jaeger, A.S., Murrieta, R.A., Goren, L.R., Crooks, C.M., Moriarty, R.V., Weiler, A.M., Rybarczyk, S., Semler, M.R., Huffman, C., Mejia, A., Simmons, H.A., Fritsch, M., Osorio, J.E., Eickhoff, J.C., O’Connor, S.L., Ebel, G.D., Friedrich, T.C., Aliota, M.T., 2019. Zika viruses of African and Asian lineages cause fetal harm in a mouse model of vertical transmission. PLoS Negl Trop Dis 13, e0007343. https://doi.org/10.1371/journal.pntd.0007343
  20. Breitbach, M.E., Newman, C.M., Dudley, D.M., Stewart, L.M., Aliota, M.T., Koenig, M.R., Shepherd, P.M., Yamamoto, K., Crooks, C.M., Young, G., Semler, M.R., Weiler, A.M., Barry, G.L., Heimsath, H., Mohr, E.L., Eichkoff, J., Newton, W., Peterson, E., Schultz-Darken, N., Permar, S.R., Dean, H., Capuano, S., Osorio, J.E., Friedrich, T.C., O’Connor, D.H., 2019. Primary infection with dengue or Zika virus does not affect the severity of heterologous secondary infection in macaques. PLoS Pathog 15, e1007766. https://doi.org/10.1371/journal.ppat.1007766
  21. Moreno, G.K., Braun, K.M., Riemersma, K.K., Martin, M.A., Halfmann, P.J., Crooks, C.M., Prall, T., Baker, D., Baczenas, J.J., Heffron, A.S., Ramuta, M., Khubbar, M., Weiler, A.M., Accola, M.A., Rehrauer, W.M., O’Connor, S.L., Safdar, N., Pepperell, C.S., Dasu, T., Bhattacharyya, S., Kawaoka, Y., Koelle, K., O’Connor, H., Friedrich, T.C., 2020. Distinct patterns of SARS-CoV-2 transmission in two nearby communities in Wisconsin, USA. medRxiv. https://doi.org/10.1101/2020.07.09.20149104
  22. Eix, E.F., Nett, J.E., 2020. How Biofilm Growth Affects Candida-Host Interactions. Front Microbiol 11, 1437. https://doi.org/10.3389/fmicb.2020.01437
  23. Francoeur, C.B., Khadempour, L., Moreira-Soto, R.D., Gotting, K., Book, A.J., Pinto-Tomás, A.A., Keefover-Ring, K., Currie, C.R., 2020. Bacteria Contribute to Plant Secondary Compound Degradation in a Generalist Herbivore System. mBio 11. https://doi.org/10.1128/mBio.02146-20
  24. Thomas, N.C., Hendrich, C.G., Gill, U.S., Allen, C., Hutton, S.F., Schultink, A., 2020. The Immune Receptor Roq1 Confers Resistance to the Bacterial Pathogens Xanthomonas, Pseudomonas syringae, and Ralstonia in Tomato. Front Plant Sci 11, 463. https://doi.org/10.3389/fpls.2020.00463
  25. Horton, M.V., Johnson, C.J., Kernien, J.F., Patel, T.D., Lam, B.C., Cheong, J.Z.A., Meudt, J.J., Shanmuganayagam, D., Kalan, L.R., Nett, J.E., 2020. Candida auris Forms High-Burden Biofilms in Skin Niche Conditions and on Porcine Skin. mSphere 5. https://doi.org/10.1128/mSphere.00910-19
  26. Jacobson, T.B., Adamczyk, P.A., Stevenson, D.M., Regner, M., Ralph, J., Reed, J.L., Amador-Noguez, D., 2019. 2H and 13C metabolic flux analysis elucidates in vivo thermodynamics of the ED pathway in Zymomonas mobilis. Metab Eng 54, 301–316. https://doi.org/10.1016/j.ymben.2019.05.006
  27. Jacobson, T.B., Korosh, T.K., Stevenson, D.M., Foster, C., Maranas, C., Olson, D.G., Lynd, L.R., Amador-Noguez, D., 2020. In Vivo Thermodynamic Analysis of Glycolysis in Clostridium thermocellum and Thermoanaerobacterium saccharolyticum Using 13C and 2H Tracers. mSystems 5. https://doi.org/10.1128/mSystems.00736-19
  28. Felczak, M.M., Jacobson, T.B., Ong, W.K., Amador-Noguez, D., TerAvest, M.A., 2019. Expression of Phosphofructokinase Is Not Sufficient to Enable Embden-Meyerhof-Parnas Glycolysis in Zymomonas mobilis ZM4. Front Microbiol 10, 2270. https://doi.org/10.3389/fmicb.2019.02270
  29. Lawson, C.E., Nuijten, G.H.L., de Graaf, R.M., Jacobson, T.B., Pabst, M., Stevenson, D.M., Jetten, M.S.M., Noguera, D.R., McMahon, K.D., Amador-Noguez, D., Lücker, S., 2020. Autotrophic and mixotrophic metabolism of an anammox bacterium revealed by in vivo 13C and 2H metabolic network mapping. ISME J. https://doi.org/10.1038/s41396-020-00805-w
  30. Park, J.O., Tanner, L.B., Wei, M.H., Khana, D.B., Jacobson, T.B., Zhang, Z., Rubin, S.A., Li, S.H.-J., Higgins, M.B., Stevenson, D.M., Amador-Noguez, D., Rabinowitz, J.D., 2019. Near-equilibrium glycolysis supports metabolic homeostasis and energy yield. Nat Chem Biol 15, 1001–1008. https://doi.org/10.1038/s41589-019-0364-9
  31. Kieft, K., Zhou, Z., U, 2020. VIBRANT: automated recovery, annotation and curation of microbial viruses, and evaluation of viral community function from genomic sequences. Microbiome 8, 90. https://doi.org/10.1186/s40168-020-00867-0
  32. Zhou, Z., Tran, P.Q., Kieft, K., Anantharaman, K., 2020. Genome diversification in globally distributed novel marine Proteobacteria is linked to environmental adaptation. ISME J 14, 2060–2077. https://doi.org/10.1038/s41396-020-0669-4
  33. Larson, G.P., Tran, V., Yú, S., Caì, Y., Higgins, C.A., Smith, D.M., Baker, S.F., Radoshitzky, S.R., Kuhn, J.H., Mehle, A., 2019. EPS8 Facilitates Uncoating of Influenza A Virus. Cell Rep 29, 2175-2183.e4. https://doi.org/10.1016/j.celrep.2019.10.064
  34. MacIntyre, A.M., Barth, J.X., Pellitteri Hahn, M.C., Scarlett, C.O., Genin, S., Allen, C., 2020. Trehalose Synthesis Contributes to Osmotic Stress Tolerance and Virulence of the Bacterial Wilt Pathogen Ralstonia solanacearum. Mol Plant Microbe Interact 33, 462–473. https://doi.org/10.1094/MPMI-08-19-0218-R
  35. Martien, J.I., Hebert, A.S., Stevenson, D.M., Regner, M.R., Khana, D.B., Coon, J.J., Amador-Noguez, D., 2019. Systems-Level Analysis of Oxygen Exposure in Zymomonas mobilis: Implications for Isoprenoid Production. mSystems 4. https://doi.org/10.1128/mSystems.00284-18
  36. Ghosh, I.N., Martien, J., Hebert, A.S., Zhang, Y., Coon, J.J., Amador-Noguez, D., Landick, R., 2019. OptSSeq explores enzyme expression and function landscapes to maximize isobutanol production rate. Metab Eng 52, 324–340. https://doi.org/10.1016/j.ymben.2018.12.008
  37. Ostrem Loss, E.M., Lee, M.-K., Wu, M.-Y., Martien, J., Chen, W., Amador-Noguez, D., Jefcoate, C., Remucal, C., Jung, S., Kim, S.-C., Yu, J.-H., 2019. Cytochrome P450 Monooxygenase-Mediated Metabolic Utilization of Benzo[a]Pyrene by Aspergillus Species. mBio 10. https://doi.org/10.1128/mBio.00558-19
  38. Liu, Y., Ghosh, I.N., Martien, J., Zhang, Y., Amador-Noguez, D., Landick, R., 2020. Regulated redirection of central carbon flux enhances anaerobic production of bioproducts in Zymomonas mobilis. Metab Eng 61, 261–274. https://doi.org/10.1016/j.ymben.2020.06.005
  39. Xu, J., Martien, J., Gilbertson, C., Ma, J., Amador-Noguez, D., Park, J.O., 2020. Metabolic flux analysis and fluxomics-driven determination of reaction free energy using multiple isotopes. Curr Opin Biotechnol 64, 151–160. https://doi.org/10.1016/j.copbio.2020.02.018
  40. Niu, M., Keller, N.P., 2019. Co-opting oxylipin signals in microbial disease. Cell Microbiol 21, e13025. https://doi.org/10.1111/cmi.13025
  41. Niu, M., Steffan, B.N., Fischer, G.J., Venkatesh, , Raffa, N.L., Wettstein, M.A., Bok, J.W., Greco, C., Zhao, C., Berthier, E., Oliw, E., Beebe, D., Bromley, M., Keller, N.P., 2020. Fungal oxylipins direct programmed developmental switches in filamentous fungi. Nat Commun 11, 5158. https://doi.org/10.1038/s41467-020-18999-0
  42. Wiesner, D.L., Merkhofer, R.M., Ober, C., Kujoth, G.C., Niu, M., Keller, N.P., Gern, J.E., Brockman-Schneider, R.A., Evans, M.D., Jackson, D.J., Warner, T., Jarjour, N.N., Esnault, S.J., Feldman, M.B., Freeman, M., Mou, H., Vyas, J.M., Klein, B.S., 2020. Club Cell TRPV4 Serves as a Damage Sensor Driving Lung Allergic Inflammation. Cell Host Microbe 27, 614-628.e6. https://doi.org/10.1016/j.chom.2020.02.006
  43. Gahan, C.G., Patel, S.J., Boursier, M.E., Nyffeler, K.E., Jennings, J., Abbott, N.L., Blackwell, H.E., Van Lehn, R.C., Lynn, D.M., 2020. Bacterial Quorum Sensing Signals Self-Assemble in Aqueous Media to Form Micelles and Vesicles: An Integrated Experimental and Molecular Dynamics Study. J Phys Chem B 124, 3616–3628. https://doi.org/10.1021/acs.jpcb.0c00496
  44. Manson, D.E., O’Reilly, M.C., Nyffeler, K.E., Blackwell, H.E., 2020. Design, Synthesis, and Biochemical Characterization of Non-Native Antagonists of the Pseudomonas aeruginosa Quorum Sensing Receptor LasR with Nanomolar IC50 Values. ACS Infect Dis 6, 649–661. https://doi.org/10.1021/acsinfecdis.9b00518
  45. Dillard, J., Perez, M., Chen, B., 2020. Therapies that enhance pulmonary vascular NO-signaling in the neonate. Nitric Oxide 95, 45–54. https://doi.org/10.1016/j.niox.2019.12.003
  46. Hose, J., Escalante, L.E., Clowers, K.J., Dutcher, H.A., Robinson, D., Bouriakov, V., Coon, J.J., Shishkova, E., Gasch, A.P., 2020. The genetic basis of aneuploidy tolerance in wild yeast. Elife 9. https://doi.org/10.7554/eLife.52063
  47. Raffa, N., Keller, N.P., 2019. A call to arms: Mustering secondary metabolites for success and survival of an opportunistic pathogen. PLoS Pathog 15, e1007606. https://doi.org/10.1371/journal.ppat.1007606
  48. Raffa, N., Osherov, N., Keller, N.P., 2019. Copper Utilization, Regulation, and Acquisition by Aspergillus fumigatus. Int J Mol Sci 20. https://doi.org/10.3390/ijms20081980
  49. Blachowicz, A., Raffa, N., Bok, J.W., Choera, T., Knox, B., Lim, F.Y., Huttenlocher, A., Wang, C.C.C., Venkateswaran, K., Keller, N.P., 2020. Contributions of Spore Secondary Metabolites to UV-C Protection and Virulence Vary in Different Aspergillus fumigatus Strains. mBio 11. https://doi.org/10.1128/mBio.03415-19
  50. Saba, J., Chua, X.Y., Mishanina, T.V., Nayak, D., Windgassen, T.A., Mooney, R.A., Landick, R., 2019. The elemental mechanism of transcriptional pausing. Elife 8. https://doi.org/10.7554/eLife.40981
  51. Massa, S.M., Sharma, A.D., Siletti, C., Tu, Z., Godfrey, J.J., Gutheil, W.G., Huynh, T.N., 2020. C-di-AMP accumulation impairs muropeptide synthesis in Listeria monocytogenes. J Bacteriol. https://doi.org/10.1128/JB.00307-20
  52. Skarlupka, J.H., Kamenetsky, M.E., Jewell, K.A., Suen, G., 2019. The ruminal bacterial community in lactating dairy cows has limited variation on a day-to-day basis. J Anim Sci Biotechnol 10, 66. https://doi.org/10.1186/s40104-019-0375-0
  53. Eggers, S., Safdar, N., Sethi, A.K., Suen, G., Peppard, P.E., Kates, A.E., Skarlupka, J.H., Kanarek, M., Malecki, K.M.C., 2019. Urinary lead concentration and composition of the adult gut microbiota in a cross-sectional population-based sample. Environ Int 133, 105122. https://doi.org/10.1016/j.envint.2019.105122
  54. Hillel, A.T., Tang, S.S., Carlos, C., Skarlupka, J.H., Gowda, M., Yin, L.X., Motz, K., Currie, C.R., Suen, G., Thibeault, S.L., 2019. Laryngotracheal Microbiota in Adult Laryngotracheal Stenosis. mSphere 4. https://doi.org/10.1128/mSphereDirect.00211-19
  55. Mote, R.S., Hill, N.S., Skarlupka, J.H., Turner, Z.B., Sanders, Z.P., Jones, D.P., Suen, G., Filipov, N.M., 2019. Response of Beef Cattle Fecal Microbiota to Grazing on Toxic Tall Fescue. Appl Environ Microbiol 85. https://doi.org/10.1128/AEM.00032-19
  56. Mote, R.S., Hill, N.S., Skarlupka, J.H., Tran, V.T., Walker, D.I., Turner, Z.B., Sanders, Z.P., Jones, D.P., Suen, G., Filipov, N.M., 2020. Toxic tall fescue grazing increases susceptibility of the Angus steer fecal microbiota and plasma/urine metabolome to environmental effects. Sci Rep 10, 2497. https://doi.org/10.1038/s41598-020-59104-1
  57. Kates, A.E., Jarrett, O., Skarlupka, J.H., Sethi, A., Duster, M., Watson, L., Suen, G., Poulsen, K., Safdar, N., 2020. Household Pet Ownership and the Microbial Diversity of the Human Gut Microbiota. Front Cell Infect Microbiol 10, 73. https://doi.org/10.3389/fcimb.2020.00073
  58. Pinto, A.C.J., Bertoldi, G.P., Felizari, L.D., Dias, E.F.F., Demartini, B.L., Nunes, A.B.C.P., Squizatti, M.M., Silvestre, A.M., Oliveira, L.F.R., Skarlupka, J.H., Rodrigues, P.H.M., Cruz, G.D., Suen, G., Millen, D.D., 2020. Ruminal Fermentation Pattern, Bacterial Community Composition, and Nutrient Digestibility of Nellore Cattle Submitted to Either Nutritional Restriction or Intake of Concentrate Feedstuffs Prior to Adaptation Period. Front Microbiol 11, 1865. https://doi.org/10.3389/fmicb.2020.01865
  59. Young, J., Skarlupka, J.H., Cox, M.S., Resende, R.T., Fischer, A., Kalscheur, K.F., McClure, J.C., Cole, J.B., Suen, G., Bickhart, D.M., 2020. Validating the Use of Bovine Buccal Sampling as a Proxy for the Rumen Microbiota by Using a Time Course and Random Forest Classification Approach. Appl Environ Microbiol 86. https://doi.org/10.1128/AEM.00861-20
  60. Stanton, E., Wagner, S., Florek, K.R., Kaspar, C.W., 2020a. Genome Sequences of 14 Escherichia coli O157:H7 Strains Isolated before and during the Time Frame of the 2018 Multistate Outbreak Associated with Romaine Lettuce. Microbiol Resour Announc 9. https://doi.org/10.1128/MRA.00458-20
  61. Stanton, E., Wahlig, T.A., Park, D., Kaspar, C.W., 2020b. Chronological set of E. coli O157:H7 bovine strains establishes a role for repeat sequences and mobile genetic elements in genome diversification. BMC Genomics 21, 562. https://doi.org/10.1186/s12864-020-06943-x
  62. Mote, R.S., Carpenter, J.M., Dockman, R.L., Steinberger, A.J., Suen, G., Norberg, T., Harn, D.A., Wagner, J.J., Filipov, N.M., 2020a. Assessing the Beneficial Effects of the Immunomodulatory Glycan LNFPIII on Gut Microbiota and Health in a Mouse Model of Gulf War Illness. Int J Environ Res Public Health 17. https://doi.org/10.3390/ijerph17197081
  63. Kontur, W.S., Olmsted, C.N., Yusko, L.M., Niles, A.V., Walters, K.A., Beebe, E.T., Vander Meulen, K.A., Karlen, S.D., Gall, D.L., Noguera, D.R., Donohue, T.J., 2019. A heterodimeric glutathione S-transferase that stereospecifically breaks lignin’s β(R)-aryl ether bond reveals the diversity of bacterial β-etherases. J Biol Chem 294, 1877–1890. https://doi.org/10.1074/jbc.RA118.006548
  64. Li, H., Young, S.E., Poulsen, M., Currie, C.R., 2020. Symbiont-Mediated Digestion of Plant Biomass in Fungus-Farming Insects. Annu Rev Entomol. https://doi.org/10.1146/annurev-ento-040920-061140