Joerg Graf

Professor, Gratis Appointment

Molecular and Cell Biology / Microbiology

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Education: Ph.D. University of Southern California, Postdoctoral study, University of Berne, Switzerland

Research Interests: While all animals are colonized by bacteria, we know very little about molecular interactions between these bacteria and their host animal unless the bacteria cause disease. The main goal of our research is to enhance the general understanding of how bacteria and animals interact. As a model for digestive-tract associations, we investigate the digestive-tract symbiosis of the medicinal leech, Hirudo medicinalis . In the largest compartment of the leech digestive tract, only two species of bacteria are found, Aeromonas veronii and a novel Rikenella species. Historically, the study of digestive-tract symbioses has been hindered by the presence of complex microbial communities but the unusual simplicity of the leech symbiosis provides an opportunity to investigate the interaction on a molecular level. While A. veronii functions as a cooperative symbiont inside the leech, this species is also a human pathogen when injected into vertebrate tissue during leech feeding, causing wound infections and, when ingested, diarrhea. The switching between symbiotic and pathogenic lifestyles suggests the ability of A. veronii to regulate its physiology according to its host and provides an opportunity to learn about the evolution of bacteria-animal associations. We use molecular tools to tease apart the interaction and epifluorescent microscopy for visualization of the symbionts. Additional research interests include the use of 16S rRNA gene sequences for the identification of bacteria, the molecular investigation of other symbiotic or pathogenic bacteria, and the discovery of novel antimicrobial compounds.

Selected Publications:

Casale A, Maldonado CA, Taropawala O, O’Sullivan B, Graf J. Draft Genome Sequence of Plesiomonas shigelloides MD22D9, Isolated from the Digestive Tract of Macrobdella decora. Microbiol Resour Announc. 2022 Dec 14:e0093922. doi: 10.1128/mra.00939-22. Epub ahead of print. PMID: 36515507.

Michael E. Stephens, Jacquelynn Benjamino, Joerg Graf, Daniel J. Gage (2022). Simultaneous Single-Cell Genome and Transcriptome Sequencing of Termite Hindgut Protists Reveals Metabolic and Evolutionary Traits of Their Endosymbionts. mSphere: https://doi.org/10.1128/msphere.00021-22

Presley, SJ, J Graf, AF Hassan, AR Sjodin,  and MR Willig. 2021. Effects of host species identity and diet on biodiversity of oral and rectal microbiomes of Puerto Rican bats. Curr. Microbio. 78:3526-40. https://doi.org/10.1007/s00284-021-02607-5

Testerman, T., S. Reichley, S. King, J. Graf. 2021. Draft Genome of Aeromonas popoffii ID682, isolated from a natural water source in Idaho. Microbiology Resource Announcements 10 (29) https://journals.asm.org/doi/full/10.1128/MRA.00445-21

Testerman, T., S. Reichley, S. King, J. Graf. 2021. Draft Genome of Janthinobacterium lividum ID1246, isolated from a rainbow trout hatchery biofilm. Microbiology Resource Announcements 10 (28) https://doi.org/10.1128/MRA.00444-21

EA McClure, EA, MC Nelson, A Lin, J Graf. Macrobdella decora: Old World Leech Gut Microbial Community Structure Conserved in a New World Leech. Appl. Env. Microbiol. 87:e02082-20. https://doi.org/10.1128/AEM.02082-20 

Graf, J., N. Ledala, M.J. Caimano, E. Jackson, D. Gratalo, D. Fasulo, M.D. Driscoll, S. Coleman, A. Matson. 2021. High-Resolution Differentiation of Enteric Bacteria in Premature Infant Fecal Microbiomes Using a Novel rRNA Amplicon. mBio 12:e03656-20. https://doi.org/10.1128/mBio.03656-20

Klub, L., Gosselin, S., Fullmer, M., Graf, J. Gogarten, J.P. and M. Bansal. 2021. Systematic Detection of Large-Scale Multi-Gene Horizontal Transfer in Prokaryotes. Mol. Biol. Evol. in press. https://doi.org/10.1093/molbev/msab043

Graf, J., M.C. Nelson, and S.M. Colston. 2020. Closed Genome Sequence of Aeromonas veronii Strain Hm21, an Isolate from the Medicinal Leech Hirudo verbana. Microbiology Resource Announcements 9 (42). https://doi.org/10.1128/MRA.00922-20

Kravetz, A.M., T. Testerman, B. Galuppo, J. Graf, B. Pierpont, S. Siebel, R. Feinn, N. Santoro. 2020. Effect of Gut Microbiota and PNPLA3 rs738409 Variant on Nonalcoholic Fatty Liver Disease (NAFLD) in Obese Youth. J. Clin Endocrinol Metabol. 105:dgaa382 https://doi.org/10.1210/clinem/dgaa382

Talagrand-Reboul, E., SM Colston, J Graf, B Lamy, E Jumas-Bilak. 2020. Comparative and Evolutionary Genomics of Isolates Provide Insight into the Pathoadaptation of Aeromonas. Genome biology and evolution 12: 535-552. https://doi.org/10.1093/gbe/evaa055

Lee, Juneyoung, John d’Aigle, Louise Atadja, Victoria Quaicoe, Pedram Honarpisheh, Bhanu P Ganesh, Ahmad Hassan, Joerg Graf, Joseph F Petrosino, Nagireddy Putluri, Liang Zhu, David J Durgan, Robert M Bryan, Jr, Louise D McCullough, Venugopal Reddy Venna. 2020. Gut Microbiota-Derived Short-Chain Fatty Acids Promote Post-Stroke Recovery in Aged Mice. Circulation Research.127:453. https://doi.org/10.1161/CIRCRESAHA.119.316448

Beka, L., MS Fullmer, SM Colston, MC Nelson, E Talagrand-Reboul, P Walker, B Ford, IS Whitaker, B. Lamy, JP Gogarten, J Graf. 2018. Low-Level Antimicrobials in the Medicinal Leech Select for Resistant Pathogens That Spread to Patients. mBio http://mbio.asm.org/content/9/4/e01328-18

Adami,AJ, SJ Bracken, LA Guernsey, E Rafti, KR Maas, J Graf, AP Matson, RS Thrall and CM Schramm. 2018. Early-life antibiotics attenuate regulatory T cell generation and increase the severity of murine house dust mite-induced asthma. Pediatric research https://www.nature.com/articles/s41390-018-0031-y

Benjamino, J., S., Lincoln, R. Srivastava, and J. Graf. 2018. Low-abundant bacteria drive compositional changes in the gut microbiota after dietary alteration. Microbiome 6: 86. https://doi.org/10.1186/s40168-018-0469-5.

Spychala, M.S., V.R. Venna, M. Jandzinski, S.J. Doran, D.J. Durgan, B.P. Ganesh, N.J. Ajami, N. Putluri, J. Graf, R.M. Bryan, L.D. McCullough. 2018. Age‐related changes in the gut microbiota influence systemic inflammation and stroke outcome. Ann. Neurol https://doi.org/10.1002/ana.25250

Colston, S.M., A. Navarro, A.J. Martinez-Murcia, and J. Graf. 2018. Draft Genome Sequence of Aeromonas cavernicola sp. nov. DSM 24474T, Isolated from a Cavern Brook in the Moravia Region of the Czech Republic. Genome announcements 6: e00227-18. doi.org/10.1128/genomeA.00227-18.

Colston, S.M., A. Navarro, A.J. Martinez-Murcia, and J. Graf. 2018. Draft Genome Sequence of Aeromonas lusitana sp. nov. Strain DSM 24905T, Isolated from a Hot Spring in Vila-Real, PortugalGenome announcements 6: e00226-18. doi.org/10.1128/genomeA.00226-18.

Benjamino J, Graf J. 2016. Characterization of the Core and Caste-Specific Microbiota in the Termite, Reticulitermes flavipes. Front Microbiol 7:171 (PMC4756164).

Crapser J, Ritzel R, Verma R, Venna VR, Liu F, Chauhan A, Koellhoffer E, Patel A, Ricker A, Maas K, Graf J, McCullough LD. 2016. Ischemic stroke induces gut permeability and enhances bacterial translocation leading to sepsis in aged mice. Aging (Albany NY) 8(5):1049-63 (PMC4931853).

Cong X, Xu W, Janton S, Henderson WA, Matson A, McGrath JM, Maas K, Graf J. 2016. Gut Microbiome Developmental Patterns in Early Life of Preterm Infants: Impacts of Feeding and Gender. PLoS ONE 11(4):e0152751 (PMC4844123).

Nelson, M.C., T. Welch and J. Graf. 2015. Complete genome sequence of Yersinia ruckeri str. CSF007-82, etiologic agent of red mouth disease in salmonid fish. Genome Announcements. doi: 10.1128/genomeA.01491-14

Ott, B., L. Beka, J. Graf, and R.V.M. Rio. 2015. Draft genome sequence of Pedobacter sp. strain Hv1, an isolate from medicinal leech mucosal castings. Genome Announc. 3:e01469-15.

Li, Y.F, J. Shi, M. C. Nelson, P.H. Chen, J. Graf, Y. Li, Z. Yu. 2016. Impact of different ratios of feedstock to liquid anaerobic digestion effluent on the performance and microbiome of solid-state anaerobic digesters digesting corn stover. Bioresource Technol. 200, 744-752.

Mosser, T., E. Talagrand-Reboul, S. M. Colston, J. Graf, MJ Figueras, E. Jumas-Bilak, B. Lamy. 2015. Co-infections with multiple Aeromonas spp. enhance their virulence in the Caenorhabditis elegans model. Frontiers in Microbiol. DOI: 10.3389/fmicb.2015.01218

Li,Y.F., C. Abraham, M.C. Nelson, P.H. Chen, J. Graf, Z. Yu. 2015. Effect of organic loading on the microbiota in a temperature-phased anaerobic digestion (TPAD) system co-digesting dairy manure and waste whey. Appl. Microbiol. Biotechnol. 99: 8777-8792.

Maltz, M. B. LeVarge and J. Graf. 2015. Identification of Iron and Heme Utilization Genes in Aeromonas and their Role in the Colonization of the Leech Digestive Tract. Front. Microbiol. doi:10.3389/fmicb.2015.00763

Cong, X., W. Henderson, J. Graf, and J. McGrath. 2015. Brain-Gut-Microbiota Signaling System in Regulation of Early Life Experience. Adv. Neonatal Care. doi: 10.1097/ANC.0000000000000191.

Nelson, M. C. and J. Graf. 2015. Complete genome sequence of the novel leech symbiont Mucinivorans hirudinis M3T. Genome Announcements. doi: 10.1128/genomeA.01530-14.

Nelson, M. C., L. Bomar, M. Maltz and J. Graf. 2015. Mucinivorans hirudinis gen. nov., sp. nov., an anaerobic, mucin-degrading bacterium isolated from the digestive tract of the Hungarian medicinal leech, Hirudo verbana. Int. J. Syst. Evol. Microbiol. 65:990-5. doi: 10.1099/ijs.0.000052.

Nelson, M.C., T. Welch and J. Graf. 2015. Complete genome sequence of Yersinia ruckeri str. CSF007-82, etiologic agent of red mouth disease in salmonid fish. Genome Announcements. doi: 10.1128/genomeA.01491-14.

Colston#, S., M. Fullmer#, L. Beka, B. Lamy, J. P. Gogarten*, J. Graf*. 2014. Evaluation of Bioinformatic Genome Comparisons for Taxonomic and Phylogenic Assignments using Aeromonas as a Test Case. #Co-first authors, *Co-corresponding authors. mBio doi:10.1128/mBio.02136-14

Li, Y.-F., M.C. Nelson, P.-H. Chen, J. Graf, Y. Li, and Z. Yu. 2014. Comparison of the microbial communities in solid-state anaerobic digesters (SS-ADs) operated at mesophilic and thermophilic temperatures. Appl. Microbiol. Biotechnol. DOI 10.1007/s00253-014-6036-5.

Maltz, M.A., L. Bomar, P. Lapierre, H.G. Morrison, E.A. McClure, M.L. Sogin and J. Graf. 2014. Metagenomic Analysis of the Medicinal Leech Gut Microbiota. Front. Microbiol. doi: 10.3389/fmicb.2014.00151

Yu, R. B. F. Smets, P. Gan, A. A. MacKay, and J. Graf. 2014. Seasonal and Spatial Variations in Microbial Activity at Various Phylogenetic Resolutions at a Groundwater Surface Water Interface: Critical Role of Flooding in Microbial Activity Determination. Can. J. Microbiol. 60(5): 277-286, 10.1139/cjm-2014-0048

Nelson, M.C.,, H.G. Morrison, J. Benjamino, S.L. Grim, J. Graf. 2014. Analysis, Optimization and Verification of Illumina-Generated 16S rRNA Gene Amplicon Surveys. PLOS One 9(4): e94249. doi:10.1371/journal.pone.0094249.

Whitaker, I., M. Maltz, M.E. Siddall, and J. Graf. 2014. Characterization of the digestive tract microbiota of Hirudo orientalis (medicinal leech) and antibiotic resistance profile. Plast. Recon. Surgery 133, p 408e–418e. DOI: 10.1097/01.prs.0000438461.06217.bb

Bomar, L., M. Maltz, S. Colston and J. Graf. 2011. Directed culturing of microorganisms using metatranscriptomics. mBio 2:e00012-11. doi:10.1128/mBio.00012-11.

Silver, A.C., D. Williams, J. Faucher*, A.J. Horneman, J.P. Gogarten, and J. Graf. 2011. Complex evolutionary history of the Aeromonas veronii group revealed by host interaction and DNA sequence data. PLOS One. PLOS One. 6: e16751.

Whitaker, I.S., I.C. Josty, S. Hawkins, E. Azzopardi, N. Naghmeh, J. Graf, L Damaris, W.C. Lineawaver and M. Kon. 2011. Medicinalleeches and the microsurgeon: a four-year study, clinical series and risk benefit review. Microsurgery J. 31:281-287.

Maltz, M. and J. Graf. 2011. The Type II Secretion System is Essential for Erythrocyte Lysis and Gut Colonization of the Leech Digestive-Tract Symbiont Aeromonas veronii. Appl. Environ. Microbiol. 77:597-603.

Rio, R.V.M., M. Maltz, B. McCormick, A. Reiss and J. Graf. 2009. Symbiont Succession during the Embryonic Development of the European Medicinal Leech, Hirudo verbana. Appl. Environ. Microbiol. 75:6890-6895

Kikuchi, Y. L. Bomar and J. Graf. 2009. Stratified bacterial community in the bladder of the medicinal leech, Hirudo verbana. Environ. Microbiol. in press.

Rio, R.V.M., M. Maltz, B. McCormick, A. Reiss and J. Graf. 2009. Symbiont Succession during the Embryonic Development of the European Medicinal Leech, Hirudo verbana. Appl. Environ. Microbiol. in press.

Laufer, A., M. Siddall and J. Graf. 2008. Characterization of the Digestive-Tract Microbiota of Hirudo orientalis, a European Medicinal Leech. Appl. Environ. Microbiol. 74:6151-6154.

Silver, A.C., Y. Kikuchi, A. A. Fadl, J. Sha, A. Chopra and J. Graf. 2007. Interaction between innate immune cells and a bacterial type-three secretion system in mutualistic and pathogenic associations. Proc. Natl. Acad. Sci.USA. 104:9481-9486.

Rio, R.V.M., M. Anderegg and J. Graf. 2007. Characterization of a catalase gene from Aeromonas veronii, the digestive-tract symbiont of the medicinal leech. Microbiology. 153:1897-1906.

Kikuchi, Y. and J. Graf. 2007. Spatial and temporal population dynamics of a naturally occurring two-species microbial community inside the Medicinal Leech. Appl. Environ. Microbiol. 73:1984-1991. (cover article)

Worthen, P. L., C. J. Gode and J. Graf. 2006. Culture-independent characterization of the digestive-tract microbiota of the medicinal leech, a tripartide symbiosis. Appl. Environ. Microbiol. 72:4775-4781.

Graf, J. 2005. Molecular requirements for the colonization of Hirudo medicinalis by Aeromonas veronii . In: Overmann, J. (ed) Molecular mechanisms of symbiosis. Series: Progress in Molecular and Subcellular Biology. Springer-Verlag, Berlin.

Braschler, T., S. Merino, J. Tomas, and J. Graf . 2003. Complement resistance is essential for the colonization of the digestive tract of Hirudo medicinalis by Aeromonas strains. Appl. Envrionment. Microbiol. 69:4268-4271.

Graf, J. 2002. The effect of the symbionts on the physiology of Hirudo medicinalis , the medicinal leech. Inv. Reproductive Develop Biol. 41:269-275.

Iten, A., S. Graf, M. Egger, M. Tauber and J. Graf. 2001. Helicobacter sp. flexispira bacteremia in an immunocompetent young adult. J. Clin. Microbiol. 39:1716-1720.

Graf, J. 2000. Symbiosis of Aeromonas and Hirudo medicinalis, the medicinal leech. ASM News 66:147-153.

Graf, J. and E. G. Ruby. 2000. Novel glnD phenotypes in Vibrio fischeri, nitrogen metabolism, iron uptake and symbiosis are effected. Mol. Microbiol. 37:168-179.

Morandi, A., O. Zhaxyba yeva, P. Gogarten and J. Graf . 2005. Evolutionary and Diagnostic Implications of Intragenomic Heterogeneity in the 16S rRNA Gene in Aeromonas Strains. J. Bacteriol. 187: 6561-6564.