SPP 1596:  Ecology and Species Barriers in Emerging Viral Diseases

• Subject Area: Medicine ; Agriculture, Forestry and Veterinary Medicine ; Biology
• Term: from 2013 to 2021
• Project identifier: Deutsche Forschungsgemeinschaft (DFG) - Project number 198576642

• Final Report Year: 2022

Final Report Abstract

Ziel des Schwerpunktprogramms 1596 war eine Stärkung der Kooperation zwischen den Fachdisziplinen Zoologie/Ökologie und Virologie zur besseren Erschließung des modernen Arbeitsfeldes „Disease ecology / Pandemic preparedness research“ in Deutschland. Die insgesamt 20 Projekte waren in der Regel als Tandem zwischen den Disziplinen oder als Kombination von unterschiedlichen Spezialisierungen innerhalb des Fachs Virologie angelegt. Durch die Projekte wurde eine große Zahl von Gruppen in die Lage versetzt, neue Analysemöglichkeiten zu nutzen und Fragen zu adressieren, die teilweise weit außerhalb ihres bisherigen Arbeitsspektrums lagen. Kernergebnisse liegen in der Erfassung und funktionellen Untersuchung größerer ökologischer Effekte wie Amplifikations- und Dilutionseffekt auf Viren in natürlichen Reservoiren in Mittelamerika, der verbesserten geogenetischen Erfassung des Nagerreservoirs von Hantaviren in Deutschland, einem verbesserten Verständnis der Barrierewirkung des Interferonsystems gegen RNA-Viren aus Säugern und Arthropoden, sowie einer Serie von genetisch-funktionellen Analysen zur Evolutionsgeschichte mehrerer humanpathogenetisch relevanter Krankheitserreger. Das Programm unterstützte den Aufbau neuer Technikressourcen in einer Vielzahl von Arbeitsgruppen und beförderte die Entwicklung der Karriere mehrerer Nachwuchswissenschaftler/innen. Insgesamt fünf Teilnehmerinnen des Programms wurden auf ordentliche Professuren berufen. Aus dem Kreis der Teilnehmenden sind drei BMBF-geförderte Forschungsverbünde und zwei Nachwuchsgruppen hervorgegangen.

Publications

• Bats carry pathogenic hepadnaviruses antigenically related to hepatitis B virus and capable of infecting human hepatocytes. Proc Natl Acad Sci U S A. 2013 Oct 1;110(40):16151-6
  Drexler JF, Geipel A, König A, Corman VM, van Riel D, Leijten LM, Bremer CM, Rasche A, Cottontail VM, Maganga GD, Schlegel M, Müller MA, Adam A, Klose SM, Carneiro AJ, Stöcker A, Franke CR, Gloza-Rausch F, Geyer J, Annan A, Adu-Sarkodie Y, Oppong S, Binger T, Vallo P, Tschapka M, Ulrich RG, Gerlich WH, Leroy E, Kuiken T, Glebe D, Drosten C
  (See online at https://doi.org/10.1073/pnas.1308049110)
• Middle East respiratory syndrome coronavirus accessory protein 4a is a type I interferon antagonist. J Virol. 2013;87(22):12489-95
  Niemeyer D, Zillinger T, Muth D, Zielecki F, Horvath G, Suliman T, et al.
  (See online at https://doi.org/10.1128/jvi.01845-13)
• A unique nodavirus with novel features: mosinovirus expresses two subgenomic RNAs, a capsid gene of unknown origin, and a suppressor of the antiviral RNA interference pathway. J Virol. 2014;88(22):13447-59
  Schuster S, Zirkel F, Kurth A, van Cleef KW, Drosten C, van Rij RP, et al.
  (See online at https://doi.org/10.1128/jvi.02144-14)
• Mosquito and Drosophila entomobirnaviruses suppress dsRNA- and siRNA-induced RNAi. Nucleic Acids Res. 2014;42(13):8732-44
  van Cleef KW, van Mierlo JT, Miesen P, Overheul GJ, Fros JJ, Schuster S, et al.
  (See online at https://doi.org/10.1093/nar/gku528)
• Evolutionary and phenotypic analysis of live virus isolates suggests arthropod origin of a pathogenic RNA virus family. Proc Natl Acad Sci U S A. 2015;112(24):7536-41
  Marklewitz M, Zirkel F, Kurth A, Drosten C, Junglen S
  (See online at https://doi.org/10.1073/pnas.1502036112)
• Investigating the zoonotic origin of the West African Ebola epidemic. EMBO Mol Med. 2015;7(1):17-23
  Mari Saez A, Weiss S, Nowak K, Lapeyre V, Zimmermann F, Dux A, et al.
  (See online at https://doi.org/10.15252/emmm.201404792)
• Out of the Reservoir: Phenotypic and Genotypic Characterization of a Novel Cowpox Virus Isolated from a Common Vole. J Virol. 2015 Nov;89(21):10959-69
  Hoffmann D, Franke A, Jenckel M, Tamošiūnaitė A, Schluckebier J, Granzow H, Hoffmann B, Fischer S, Ulrich RG, Höper D, Goller K, Osterrieder N, Beer M
  (See online at https://doi.org/10.1128/jvi.01195-15)
• Presence of Middle East respiratory syndrome coronavirus antibodies in Saudi Arabia: a nationwide, cross-sectional, serological study. The Lancet Infectious Diseases. 2015;15(5):559-64
  Müller MA, Meyer B, Corman VM, Al-Masri M, Turkestani A, Ritz D, et al.
  (See online at https://doi.org/10.1016/s1473-3099(15)70090-3)
• Differential transcriptional responses to Ebola and Marburg virus infection in bat and human cells. Sci Rep. 2016 Oct 7;6:34589
  Hölzer M, Krähling V, Amman F, Barth E, Bernhart SH, Carmelo VA, Collatz M, Doose G, Eggenhofer F, Ewald J, Fallmann J, Feldhahn LM, Fricke M, Gebauer J, Gruber AJ, Hufsky F, Indrischek H, Kanton S, Linde J, Mostajo N, Ochsenreiter R, Riege K, Rivarola-Duarte L, Sahyoun AH, Saunders SJ, Seemann SE, Tanzer A, Vogel B, Wehner S, Wolfinger MT, Backofen R, Gorodkin J, Grosse I, Hofacker I, Hoffmann S, Kaleta C, Stadler PF, Becker S, Marz M
  (See online at https://doi.org/10.1038/srep34589)
• Differential transcriptional responses to Ebola and Marburg virus infection in bat and human cells. Sci Rep. 2016;6:34589
  Holzer M, Krahling V, Amman F, Barth E, Bernhart SH, Carmelo VA, et al.
  (See online at https://doi.org/10.1038/srep34589)
• Insectivorous bats carry host specific astroviruses and coronaviruses across different regions in Germany. Infect Genet Evol. 2016;37:108-16
  Fischer K, Zeus V, Kwasnitschka L, Kerth G, Haase M, Groschup MH, et al.
  (See online at https://doi.org/10.1016/j.meegid.2015.11.010)
• Link of a ubiquitous human coronavirus to dromedary camels. Proc Natl Acad Sci U S A. 2016 Aug 30;113(35):9864-9
  Corman VM, Eckerle I, Memish ZA, Liljander AM, Dijkman R, Jonsdottir H, Juma Ngeiywa KJ, Kamau E, Younan M, Al Masri M, Assiri A, Gluecks I, Musa BE, Meyer B, Müller MA, Hilali M, Bornstein S, Wernery U, Thiel V, Jores J, Drexler JF, Drosten C
  (See online at https://doi.org/10.1073/pnas.1604472113)
• Bat Astroviruses: Towards Understanding the Transmission Dynamics of a Neglected Virus Family. Viruses. 2017;9(2)
  Fischer K, Pinho Dos Reis V, Balkema-Buschmann A
  (See online at https://doi.org/10.3390/v9020034)
• Evolution and Antiviral Specificities of Interferon-Induced Mx Proteins of Bats against Ebola, Influenza, and Other RNA Viruses. J Virol. 2017;91(15)
  Fuchs J, Holzer M, Schilling M, Patzina C, Schoen A, Hoenen T, et al.
  (See online at https://doi.org/10.1128/jvi.00361-17)
• Habitat disturbance results in chronic stress and impaired health status in forest-dwelling paleotropical bats. Conserv Physiol. 2017;5(1):cox020
  Seltmann A, Czirjak GA, Courtiol A, Bernard H, Struebig MJ, Voigt CC
  (See online at https://doi.org/10.1093/conphys/cox020)
• Host-Associated Absence of Human Puumala Virus Infections in Northern and Eastern Germany. Emerg Infect Dis. 2017;23(1):83-6
  Drewes S, Ali HS, Saxenhofer M, Rosenfeld UM, Binder F, Cuypers F, et al.
  (See online at https://doi.org/10.3201/eid2301.160224)
• Seasonal Fluctuations of Astrovirus, But Not Coronavirus Shedding in Bats Inhabiting Human-Modified Tropical Forests. Ecohealth. 2017;14(2):272-84
  Seltmann A, Corman VM, Rasche A, Drosten C, Czirjak GA, Bernard H, et al.
  (See online at https://doi.org/10.1007/s10393-017-1245-x)
• A novel hepatitis B virus species discovered in capuchin monkeys sheds new light on the evolution of primate hepadnaviruses. J Hepatol. 2018 Jun;68(6):1114-1122
  de Carvalho Dominguez Souza BF, König A, Rasche A, de Oliveira Carneiro I, Stephan N, Corman VM, Roppert PL, Goldmann N, Kepper R, Müller SF, Völker C, de Souza AJS, Gomes-Gouvêa MS, Moreira-Soto A, Stöcker A, Nassal M, Franke CR, Rebello Pinho JR, Soares MDCP, Geyer J, Lemey P, Drosten C, Netto EM, Glebe D, Drexler JF
  (See online at https://doi.org/10.1016/j.jhep.2018.01.029)
• Emerging Viruses in Bees: From Molecules to Ecology. Adv Virus Res. 2018;101:251-91
  McMahon DP, Wilfert L, Paxton RJ, Brown MJF
  (See online at https://doi.org/10.1016/bs.aivir.2018.02.008)
• Entry, Replication, Immune Evasion, and Neurotoxicity of Synthetically Engineered Bat-Borne Mumps Virus. Cell Rep. 2018;25(2):312-20 e7
  Kruger N, Sauder C, Huttl S, Papies J, Voigt K, Herrler G, et al.
  (See online at https://doi.org/10.1016/j.celrep.2018.09.018)
• (2019). Secondary contact between diverged host lineages entails ecological speciation in a European hantavirus. PLOS Biology 17: e3000142
  Saxenhofer, M., Schmidt, S., Ulrich, R.G., Heckel, G.
  (See online at https://doi.org/10.1371/journal.pbio.3000142)
• Adenovirus infection is associated with altered gut microbial communities in a non-human primate. Sci Rep. 2019;9(1):13410
  Wasimuddin, Corman VM, Ganzhorn JU, Rakotondranary J, Ratovonamana YR, Drosten C, et al.
  (See online at https://doi.org/10.1038/s41598-019-49829-z)
• Challenges of next-generation sequencing in conservation management: Insights from long-term monitoring of corridor effects on the genetic diversity of mouse lemurs in a fragmented landscape. Evol Appl. 2019;12(3):425-42
  Montero BK, Refaly E, Ramanamanjato JB, Randriatafika F, Rakotondranary SJ, Wilhelm K, et al.
  (See online at https://doi.org/10.1111/eva.12723)
• Fusogenicity of the Ghana Virus (Henipavirus: Ghanaian bat henipavirus) Fusion Protein is Controlled by the Cytoplasmic Domain of the Attachment Glycoprotein. Viruses. 2019;11(9)
  Voigt K, Hoffmann M, Drexler JF, Muller MA, Drosten C, Herrler G, et al.
  (See online at https://doi.org/10.3390/v11090800)
• Highly diversified shrew hepatitis B viruses corroborate ancient origins and divergent infection patterns of mammalian hepadnaviruses. Proc Natl Acad Sci U S A. 2019 Aug 20;116(34):17007-17012
  Rasche A, Lehmann F, König A, Goldmann N, Corman VM, Moreira-Soto A, Geipel A, van Riel D, Vakulenko YA, Sander AL, Niekamp H, Kepper R, Schlegel M, Akoua-Koffi C, Souza BFCD, Sahr F, Olayemi A, Schulze V, Petraityte-Burneikiene R, Kazaks A, Lowjaga KAAT, Geyer J, Kuiken T, Drosten C, Lukashev AN, Fichet-Calvet E, Ulrich RG, Glebe D, Drexler JF
  (See online at https://doi.org/10.1073/pnas.1908072116)
• Highly diversified shrew hepatitis B viruses corroborate ancient origins and divergent infection patterns of mammalian hepadnaviruses. Proc Natl Acad Sci U S A. 2019 Aug 20;116(34):17007-17012
  Rasche A, Lehmann F, König A, Goldmann N, Corman VM, Moreira-Soto A, Geipel A, van Riel D, Vakulenko YA, Sander AL, Niekamp H, Kepper R, Schlegel M, Akoua-Koffi C, Souza BFCD, Sahr F, Olayemi A, Schulze V, Petraityte-Burneikiene R, Kazaks A, Lowjaga KAAT, Geyer J, Kuiken T, Drosten C, Lukashev AN, Fichet-Calvet E, Ulrich RG, Glebe D, Drexler JF
  (See online at https://doi.org/10.1073/pnas.1908072116)
• Re-assessing the diversity of negative strand RNA viruses in insects. PLoS Pathog. 2019 Dec 12;15(12):e1008224
  Käfer S, Paraskevopoulou S, Zirkel F, Wieseke N, Donath A, Petersen M, Jones TC, Liu S, Zhou X, Middendorf M, Junglen S, Misof B, Drosten C
  (See online at https://doi.org/10.1371/journal.ppat.1008224)
• Virus- and Interferon Alpha-Induced Transcriptomes of Cells from the Microbat Myotis daubentonii. iScience. 2019;19:647-61
  Holzer M, Schoen A, Wulle J, Muller MA, Drosten C, Marz M, Weber, F
  (See online at https://doi.org/10.1016/j.isci.2019.08.016)
• (2020) Pathogen-associated selection on innate immunity genes (TLR4, TLR7) in a neotropical rodent in landscapes differing in anthropogenic disturbance. Heredity, 125, 184-199
  Heni AC, Schmid J, Rasche A, Corman VM, Drosten C, Sommer S
  (See online at https://doi.org/10.1038/s41437-020-0331-y)
• Density dependence and persistence of Morogoro arenavirus transmission in a fluctuating population of its reservoir host. J Anim Ecol. 2020;89(2):506-18
  Marien J, Borremans B, Verhaeren C, Kirkpatrick L, Gryseels S, Gouy de Bellocq J, et al.
  (See online at https://doi.org/10.1111/1365-2656.13107)
• Experimental infection of bumblebees with honeybee-associated viruses: no direct fitness costs but potential future threats to novel wild bee hosts. R Soc Open Sci. 2020;7(7):200480
  Tehel A, Streicher T, Tragust S, Paxton RJ
  (See online at https://doi.org/10.1098/rsos.200480)
• Mammalian deltavirus without hepadnavirus coinfection in the neotropical rodent Proechimys semispinosus. Proc Natl Acad Sci U S A. 2020 Jul 28;117(30):17977-17983
  Paraskevopoulou S, Pirzer F, Goldmann N, Schmid J, Corman VM, Gottula LT, Schroeder S, Rasche A, Muth D, Drexler JF, Heni AC, Eibner GJ, Page RA, Jones TC, Müller MA, Sommer S, Glebe D, Drosten C
  (See online at https://doi.org/10.1073/pnas.2006750117)
• Tick populations from endemic and nonendemic areas in Germany show differential susceptibility to TBEV. Sci Rep. 2020;10(1):15478
  Liebig K, Boelke M, Grund D, Schicht S, Springer A, Strube C, et al.
  (See online at https://doi.org/10.1038/s41598-020-71920-z)
• Tick-transmitted thogotovirus gains high virulence by a single MxA escape mutation in the viral nucleoprotein. PLoS Pathog. 2020; 16(11):e1009038
  Fuchs J, Oschwald A, Graf L, Kochs G
  (See online at https://doi.org/10.1371/journal.ppat.1009038)
• What a Difference a Gene Makes: Identification of Virulence Factors of Cowpox Virus. J Virol. 2020;94(2)
  Tamosiunaite A, Weber S, Schippers T, Franke A, Xu Z, Jenckel M, et al.
  (See online at https://doi.org/10.1128/jvi.01625-19)
• Characterization and Vector Competence Studies of Chikungunya Virus Lacking Repetitive Motifs in the 3' Untranslated Region of the Genome. Viruses. 2021;13(3)
  Karliuk Y, Vom Hemdt A, Wieseler J, Pfeffer M, Kummerer BM
  (See online at https://doi.org/10.3390/v13030403)
• Experimental Morogoro Virus Infection in Its Natural Host, Mastomys natalensis. Viruses. 2021;13(5)
  Hoffmann C, Wurr S, Pallasch E, Bockholt S, Rieger T, Gunther S, et al.
  (See online at https://doi.org/10.3390/v13050851)
• The Stable Matching Problem in TBEV Enzootic Circulation: How Important Is the Perfect Tick-Virus Match? Microorganisms. 2021;9(1)
  Liebig K, Boelke M, Grund D, Schicht S, Bestehorn-Willmann M, Chitimia-Dobler L, et al.
  (See online at https://doi.org/10.3390/microorganisms9010196)