Analyze Diet
Frontiers in veterinary science2024; 11; 1429654; doi: 10.3389/fvets.2024.1429654

Genomic revelations: investigating rotavirus a presence in wild ruminants and its zoonotic potential.

Abstract: Rotaviruses A (RVA) are a major cause of acute viral gastroenteritis in humans worldwide and are responsible for about two million hospitalizations per year. They can also infect other mammals such as pigs, calves, goats, lambs, and horses, in which they are also considered a major cause of viral diarrhea. While RVA is well studied in humans and domestic animals, its occurrence in wild ruminants is not well known. The RVA genome is a double-stranded RNA consisting of 11 segments, and genotyping is based on the VP7 (G) and VP4 (P) segments. Currently, there are 42G genotypes and 58P genotypes. RVA has a high mutation rate, and some combinations of G and P genotypes can infect different animal species, leading to speculation about the potential for zoonotic transmission. Unassigned: A total of 432 fecal samples were collected from roe deer, red deer, chamois, mouflon and Alpine ibex in Slovenia between 2017 and 2021. To investigate the presence of RVA in wild ruminants, real-time RT-PCR was used. Positive samples were subjected to next generation sequencing (NGS) using RIP-seq method. Unassigned: In total, 7 samples were RVA positive. Complete genomes were determined and phylogenetically analyzed for all 7 RVAs. Four different genotype constellations were present in 7 positive RVA animals: G8-P[14]-I2- R2-C2-M2-A3-N2-T6-E2-H3, G6-P [14]-I2-R2-C2-M2-A11-N2-T6-E2-H3, G10-P [15]-I2-R2-C2-M2-A3-N2-T6-E2-H3 and G10-P [15]-I2-R2-C2-M2-A11- N2-T6-E2-H3. Genotypes G6P[14] and G10P[15] were found in both roe deer and red deer, representing the first confirmed occurrence of RVA in red deer. In addition, genotype G8P[14] was found in chamois, representing the first known case of positive RVA in this species. Some of these genotypes have also been found in humans, indicating the potential for zoonotic transmission.
Publication Date: 2024-08-15 PubMed ID: 39211480PubMed Central: PMC11358691DOI: 10.3389/fvets.2024.1429654Google Scholar: Lookup
The Equine Research Bank provides access to a large database of publicly available scientific literature. Inclusion in the Research Bank does not imply endorsement of study methods or findings by Mad Barn.
  • Journal Article

Summary

This research summary has been generated with artificial intelligence and may contain errors and omissions. Refer to the original study to confirm details provided. Submit correction.

This research delves into the occurrence of Rotaviruses A (RVA) in wild ruminants and their potential for zoonotic transmission, based on genetic analysis conducted on fecal samples collected from various deer species in Slovenia.

Research Context and Purpose

  • The authors of this research are concerned with Rotaviruses A (RVA) – a common cause for acute viral gastroenteritis in humans and other mammals like pigs, horses, goats, and calves. This research focuses on understanding the occurrence of RVA in wild ruminants, a group of mammals not extensively studied for RVA infection.
  • The research purpose is also directed towards understanding the zoonotic potential of RVA, i.e., its capability to transmit from animals to humans.

Research Methodology

  • The research involves the collection of 432 fecal samples from different wild ruminants – roe deer, red deer, chamois, mouflon, and Alpine ibex – in Slovenia between 2017 and 2021.
  • The technique employed to detect the presence of RVA in these samples was real-time RT-PCR. The positive samples identified were further subjected to next-generation sequencing (NGS) using the RIP-seq method for more detailed genomic analysis.

Findings and Conclusions

  • A total of 7 RVA positive samples were identified, and full genomes of these RVAs were determined and analysed.
  • The positive RVAs were found to have four different genotype constellations – G8-P[14]-I2- R2-C2-M2-A3-N2-T6-E2-H3, G6-P [14]-I2-R2-C2-M2-A11-N2-T6-E2-H3, G10-P [15]-I2-R2-C2-M2-A3-N2-T6-E2-H3 and G10-P [15]-I2-R2-C2-M2-A11- N2-T6-E2-H3.
  • Additionally, the genotypes G6P[14] and G10P[15] were identified in both roe deer and red deer, indicating the first known occurrence of RVA in red deer. Genotype G8P[14] was observed in chamois, marking another first-time detection of RVA in a species.
  • The crucial concluding point is that these genotypes have also been found in humans, insinuating that they could potentially transmit from these wild ruminants to humans.

Cite This Article

APA
Šenica P, Žele Vengušt D, Vengušt G, Kuhar U. (2024). Genomic revelations: investigating rotavirus a presence in wild ruminants and its zoonotic potential. Front Vet Sci, 11, 1429654. https://doi.org/10.3389/fvets.2024.1429654

Publication

ISSN: 2297-1769
NlmUniqueID: 101666658
Country: Switzerland
Language: English
Volume: 11
Pages: 1429654
PII: 1429654

Researcher Affiliations

Šenica, Petra
  • Veterinary Faculty, Institute of Microbiology and Parasitology, University of Ljubljana, Ljubljana, Slovenia.
Žele Vengušt, Diana
  • Veterinary Faculty, Institute of Pathology, Wild Animals, Fish and Bees, University of Ljubljana, Ljubljana, Slovenia.
Vengušt, Gorazd
  • Veterinary Faculty, Institute of Pathology, Wild Animals, Fish and Bees, University of Ljubljana, Ljubljana, Slovenia.
Kuhar, Urška
  • Veterinary Faculty, Institute of Microbiology and Parasitology, University of Ljubljana, Ljubljana, Slovenia.

Conflict of Interest Statement

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

References

This article includes 52 references
  1. Kumar D, Shepherd FK, Springer NL, Mwangi W, Marthaler DG. Rotavirus infection in swine: genotypic diversity, immune responses, and role of gut microbiome in rotavirus immunity.. Pathogens (2022) 11:1078.
    doi: 10.3390/pathogens11101078pmc: PMC9607047pubmed: 36297136google scholar: lookup
  2. Papp H, László B, Jakab F, Ganesh B, De Grazia S, Matthijnssens J. Review of group A rotavirus strains reported in swine and cattle.. Vet Microbiol (2013) 165:190–9.
  3. Papp H, Malik YS, Farkas SL, Jakab F, Martella V, Bányai K. Rotavirus strains in neglected animal species including lambs, goats and camelids.. Virusdisease (2014) 25:215–22.
    doi: 10.1007/s13337-014-0203-2pmc: PMC4188177pubmed: 25674588google scholar: lookup
  4. Bailey KE, Gilkerson JR, Browning GF. Equine rotaviruses-current understanding and continuing challenges.. Vet Microbiol (2013) 167:135–44.
  5. Dhama K, Chauhan RS, Mahendran M, Malik SVS. Rotavirus diarrhea in bovines and other domestic animals.. Vet Res Commun (2009) 33:1–23.
    doi: 10.1007/s11259-008-9070-xpmc: PMC7088678pubmed: 18622713google scholar: lookup
  6. Dennehy PH. Transmission of rotavirus and other enteric pathogens in the home.. Pediatr Infect Dis J (2000) 19:S103–5.
  7. Wilhelm B, Waddell L, Greig J, Rajić A, Houde A, McEwen SA. A scoping review of the evidence for public health risks of three emerging potentially zoonotic viruses: hepatitis E virus, norovirus, and rotavirus.. Prev Vet Med (2015) 119:61–79.
  8. Matthijnssens J, Ciarlet M, McDonald SM, Attoui H, Bányai K, Brister JR. Uniformity of rotavirus strain nomenclature proposed by the rotavirus classification working group (RCWG).. Arch Virol (2011) 156:1397–413.
    doi: 10.1007/s00705-011-1006-zpmc: PMC3398998pubmed: 21597953google scholar: lookup
  9. Pesavento JB, Crawford SE, Estes MK, Venkataram Prasad BV. Rotavirus proteins: structure and assembly.. Curr Top Microbiol Immunol (2006) 309:189–219.
    doi: 10.1007/3-540-30773-7_7pubmed: 16913048google scholar: lookup
  10. Knipe DM, Howley PM, Cohen JI, Griffin DE, Lamb RA, Martin MA. Fields virology.. Philadelphia, PA: Lippincott Williams & Wilkins; (2013).
  11. RCWG . List of accepted genotypes. Laboratory of Viral Metagenomics (2023). Available at: https://rega.kuleuven.be/cev/viralmetagenomics/virus-classification/rcwg
  12. Bányai K, Papp H, Dandár E, Molnár P, Mihály I, Van Ranst M. Whole genome sequencing and phylogenetic analysis of a zoonotic human G8P[14] rotavirus strain.. Infect Genet Evol (2010) 10:1140–4.
    doi: 10.1016/j.meegid.2010.05.001pubmed: 20471499google scholar: lookup
  13. Malik YS, Bhat S, Dar PS, Sircar S, Dhama K, Singh RK. Evolving rotaviruses, interspecies transmission and Zoonoses.. Open Virol J (2020) 14:1–6.
  14. Chamsai E, Charoenkul K, Udom K, Jairak W, Chaiyawong S, Amonsin A. Genetic characterization and evidence for multiple reassortments of rotavirus a G3P[3] in dogs and cats in Thailand.. Front Vet Sci (2024) 11:1415771.
    doi: 10.3389/fvets.2024.1415771pmc: PMC11157116pubmed: 38855413google scholar: lookup
  15. Matthijnssens J, Ciarlet M, Heiman E, Arijs I, Delbeke T, McDonald SM. Full genome-based classification of rotaviruses reveals a common origin between human Wa-like and porcine rotavirus strains and human DS-1-like and bovine rotavirus strains.. J Virol (2008) 82:3204–19.
    doi: 10.1128/JVI.02257-07pmc: PMC2268446pubmed: 18216098google scholar: lookup
  16. Matthijnssens J, Van Ranst M. Genotype constellation and evolution of group a rotaviruses infecting humans.. Curr Opin Virol (2012) 2:426–33.
    doi: 10.1016/j.coviro.2012.04.007pubmed: 22683209google scholar: lookup
  17. Martella V, Bányai K, Matthijnssens J, Buonavoglia C, Ciarlet M. Zoonotic aspects of rotaviruses.. Vet Microbiol (2010) 140:246–55.
    doi: 10.1016/j.vetmic.2009.08.028pubmed: 19781872google scholar: lookup
  18. Gutiérrez-Aguirre I, Steyer A, Boben J, Gruden K, Poljšak-Prijatelj M, Ravnikar M. Sensitive detection of multiple rotavirus genotypes with a single reverse transcription-real-time quantitative PCR assay.. J Clin Microbiol (2008) 46:2547–54.
    doi: 10.1128/JCM.02428-07pmc: PMC2519481pubmed: 18524966google scholar: lookup
  19. Zhao J, Ohsumi TK, Kung JT, Ogawa Y, Grau DJ, Sarma K. Genome-wide identification of polycomb-associated RNAs by RIP-seq.. Mol Cell (2010) 40:939–53.
  20. Nurk S, Meleshko D, Korobeynikov A, Pevzner PA. MetaSPAdes: a new versatile metagenomic assembler.. Genome Res (2017) 27:824–34.
    doi: 10.1101/gr.213959.116pmc: PMC5411777pubmed: 28298430google scholar: lookup
  21. Buchfink B, Xie C, Huson DH. Fast and sensitive protein alignment using DIAMOND.. Nat Methods (2015) 12:59–60.
    doi: 10.1038/nmeth.3176pubmed: 25402007google scholar: lookup
  22. Huson DH, Beier S, Flade I, Górska A, El-Hadidi M, Mitra S. MEGAN Community edition - interactive exploration and analysis of large-scale microbiome sequencing data.. PLoS Comput Biol (2016) 12:e1004957.
  23. Subspecies Classification Service . BV-BRC (2023). Available at: https://www.bv-brc.org/app/SubspeciesClassification
  24. Katoh K, Standley DM. MAFFT multiple sequence alignment software version 7: improvements in performance and usability.. Mol Biol Evol (2013) 30:772–80.
    doi: 10.1093/molbev/mst010pmc: PMC3603318pubmed: 23329690google scholar: lookup
  25. Tamura K, Stecher G, Kumar S. MEGA11: molecular evolutionary genetics analysis version 11.. Mol Biol Evol (2021) 38:3022–7.
    doi: 10.1093/molbev/msab120pmc: PMC8233496pubmed: 33892491google scholar: lookup
  26. Althof N, Trojnar E, Johne R. Rotaviruses in wild ungulates from Germany, 2019–2022.. Microorganisms (2023) 11:566.
  27. Díaz Alarcón RG, Liotta DJ, Miño S. Zoonotic RVA: state of the art and distribution in the animal world.. Viruses (2022) 14:2554.
    doi: 10.3390/v14112554pmc: PMC9694813pubmed: 36423163google scholar: lookup
  28. Matthijnssens J, Bilcke J, Ciarlet M, Martella V, Bányai K, Rahman M. Rotavirus disease and vaccination: impact on genotype diversity.. Future Microbiol (2009) 4:1303–16.
    doi: 10.2217/fmb.09.96pubmed: 19995190google scholar: lookup
  29. Mullick S, Mukherjee A, Ghosh S, Pazhani GP, Sur D, Manna B. Genomic analysis of human rotavirus strains G6P[14] and G11P[25] isolated from Kolkata in 2009 reveals interspecies transmission and complex reassortment events.. Infect Genet Evol (2013) 14:15–21.
    doi: 10.1016/j.meegid.2012.11.010pubmed: 23219735google scholar: lookup
  30. Delogu R, Ianiro G, Morea A, Chironna M, Fiore L, Ruggeri FM. Molecular characterization of two rare human G8P[14] rotavirus strains, detected in Italy in 2012.. Infect Genet Evol (2016) 44:303–12.
    doi: 10.1016/j.meegid.2016.07.018pubmed: 27449953google scholar: lookup
  31. Alaoui Amine S, Melloul M, El Alaoui MA, Touil N, El Fahime E. Full-length genome analysis of the first human G8P[14] rotavirus strain from Morocco suggests evidence of zoonotic transmission.. Virus Genes (2019) 55:465–78.
    doi: 10.1007/s11262-019-01677-9pubmed: 31197545google scholar: lookup
  32. Gautam R, Mijatovic-Rustempasic S, Roy S, Esona MD, Lopez B, Mencos Y. Full genomic characterization and phylogenetic analysis of a zoonotic human G8P[14] rotavirus strain detected in a sample from Guatemala.. Infect Genet Evol (2015) 33:206–11.
  33. Wu F-T, Báanyai K, Wu HS, Yang DCF, Lin JS, Hsiung CA. Identification of a G8P[14] rotavirus isolate obtained from a Taiwanese child: evidence for a relationship with bovine rotaviruses.. Jpn J Infect Dis (2012) 65:455–7.
    doi: 10.7883/yoken.65.455pmc: PMC8211372pubmed: 22996226google scholar: lookup
  34. Matthijnssens J, Potgieter CA, Ciarlet M, Parreño V, Martella V, Bányai K. Are human P[14] rotavirus strains the result of interspecies transmissions from sheep or other ungulates that belong to the mammalian order Artiodactyla?. J Virol (2009) 83:2917–29.
    doi: 10.1128/JVI.02246-08pmc: PMC2655590pubmed: 19153225google scholar: lookup
  35. Steyer A, Naglič T, Jamnikar-Ciglenečki U, Kuhar U. Detection and whole-genome analysis of a zoonotic G8P[14] rotavirus strain isolated from a child with diarrhea.. Genome Announc (2017) 5:e01053-17.
    doi: 10.1128/genomeA.01053-17pmc: PMC5637500pubmed: 29025940google scholar: lookup
  36. Marton S, Dóró R, Fehér E, Forró B, Ihász K, Varga-Kugler R. Whole genome sequencing of a rare rotavirus from archived stool sample demonstrates independent zoonotic origin of human G8P[14] strains in Hungary.. Virus Res (2017) 227:96–103.
  37. Medici MC, Tummolo F, Bonica MB, Heylen E, Zeller M, Calderaro A. Genetic diversity in three bovine-like human G8P[14] and G10P[14] rotaviruses suggests independent interspecies transmission events.. J Gen Virol (2015) 96:1161–8.
    doi: 10.1099/vir.0.000055pubmed: 25614586google scholar: lookup
  38. Jamnikar-Ciglenecki U, Kuhar U, Steyer A, Kirbis A. Whole genome sequence and a phylogenetic analysis of the G8P[14] group a rotavirus strain from roe deer.. BMC Vet Res (2017) 13:353.
    doi: 10.1186/s12917-017-1280-4pmc: PMC5702219pubmed: 29178883google scholar: lookup
  39. Sawant PM, Digraskar S, Gopalkrishna V. Molecular characterization of unusual G10P[33], G6P[14] genomic constellations of group a rotavirus and evidence of zooanthroponosis in bovines.. Infect Genet Evol (2020) 84:104385.
    doi: 10.1016/j.meegid.2020.104385pubmed: 32522623google scholar: lookup
  40. El Sherif M, Esona MD, Wang Y, Gentsch JR, Jiang B, Glass RI. Detection of the first G6P[14] human rotavirus strain from a child with diarrhea in Egypt.. Infect Genet Evol (2011) 11:1436–42.
    doi: 10.1016/j.meegid.2011.05.012pubmed: 21640199google scholar: lookup
  41. Damanka S, Lartey B, Agbemabiese C, Dennis FE, Adiku T, Nyarko K. Detection of the first G6P[14] human rotavirus strain in an infant with diarrhoea in Ghana.. Virol J (2016) 13:1–7.
    doi: 10.1186/s12985-016-0643-ypmc: PMC5103419pubmed: 27832798google scholar: lookup
  42. Damanka SA, Dennis FE, Lartey BL, Nyarko KM, Agbemabiese CA, Armah GE. Next-generation sequencing of a human-animal reassortant G6P[14] rotavirus a strain from a child hospitalized with diarrhoea.. Arch Virol (2020) 165:1003–5.
    doi: 10.1007/s00705-020-04543-4pubmed: 32037490google scholar: lookup
  43. Bányai K, Martella V, Molnár P, Mihály I, Van Ranst M, Matthijnssens J. Genetic heterogeneity in human G6P[14] rotavirus strains detected in Hungary suggests independent zoonotic origin.. J Infect (2009) 59:213–5.
    doi: 10.1016/j.jinf.2009.06.009pubmed: 19608281google scholar: lookup
  44. Cowley D, Donato CM, Roczo-Farkas S, Kirkwood CD. Novel G10P[14] rotavirus strain, Northern Territory, Australia.. Emerg Infect Dis (2013) 19:1324–7.
    doi: 10.3201/eid1908.121653pmc: PMC3739504pubmed: 23876354google scholar: lookup
  45. Rajendran P, Kang G. Molecular epidemiology of rotavirus in children and animals and characterization of an unusual G10P[15] strain associated with bovine diarrhea in South India.. Vaccine (2014) 32:A89–94.
    doi: 10.1016/j.vaccine.2014.03.026pubmed: 25091687google scholar: lookup
  46. Gazal S, Mir IA, Iqbal A, Taku AK, Kumar B, Bhat MA. Ovine rotaviruses.. Open Vet J (2011) 5:50–4485.
    doi: 10.5455/OVJ.2011.v1.i0.p50pmc: PMC4655755pubmed: 26623281google scholar: lookup
  47. Papp H, Al-Mutairi L, Chehadeh W, Farkas S, Lengyel G, Jakab F. Novel NSP4 genotype in a camel G10P[15] rotavirus strain.. Acta Microbiol Immunol Hung (2012) 59:411–21.
    doi: 10.1556/amicr.59.2012.3.11pubmed: 22982644google scholar: lookup
  48. Chen Y, Zhu W, Sui S, Yin Y, Hu S, Zhang X. Whole genome sequencing of lamb rotavirus and comparative analysis with other mammalian rotaviruses.. Virus Genes (2009) 38:302–10.
    doi: 10.1007/s11262-009-0332-7pubmed: 19214729google scholar: lookup
  49. Armah GE, Hoshino Y, Santos N, Binka F, Damanka S, Adjei R. The global spread of rotavirus G10 strains: detection in Ghanaian children hospitalized with Diarrhoea.. J Infect Dis (2010) 202:S231–8.
    doi: 10.1086/653572pmc: PMC2954461pubmed: 20684709google scholar: lookup
  50. Ghosh S, Alam MM, Ahmed MU, Talukdar RI, Paul SK, Kobayashi N. Complete genome constellation of a caprine group a rotavirus strain reveals common evolution with ruminant and human rotavirus strains.. J Gen Virol (2010) 91:2367–73.
    doi: 10.1099/vir.0.022244-0pubmed: 20505013google scholar: lookup
  51. Masuda T, Nagai M, Yamasato H, Tsuchiaka S, Okazaki S, Katayama Y. Identification of novel bovine group a rotavirus G15P[14] strain from epizootic diarrhea of adult cows by de novo sequencing using a next-generation sequencer.. Vet Microbiol (2014) 171:66–73.
  52. Hou G, Zeng Q, Matthijnssens J, Greenberg HB, Ding S. Rotavirus NSP1 contributes to intestinal viral replication, pathogenesis, and transmission.. mBio (2021) 12:e0320821.
    doi: 10.1128/mBio.03208-21pmc: PMC8669464pubmed: 34903043google scholar: lookup

Citations

This article has been cited 0 times.