Abstract
Bat-borne viruses may affect public health and the global economy. These mammals have a wide geographical distribution and unique biological, physiological, and immunogenic characteristics, allowing the dissemination of many known and unknown viruses. Enteric viruses, such as adeno (AdV) and rotaviruses, are recognized as the main causative agents of disease and outbreaks. In the present study, the presence of viruses from Adenoviridae and Reoviridae families was evaluated in molossid, phyllostomid, and vespertilionid bats captured in Rio Grande do Sul, Southern Brazil, between September 2021 and July 2022. Sixty bat rectal swabs were analyzed by PCR. Eight (13.3%) samples were positive for adenovirus and classified as human mastadenovirus C (HAdV-C) (three samples) and HAdV-E (five samples) by sequencing followed by phylogenetic analysis. All samples were negative in rotavirus specific RT-PCR. This is the first study to describe the presence of HAdV in samples of Glossophaga soricina, Eptesicus brasiliensis, and Histiotus velatus. Furthermore, the presence of HAdV-E in bats was reported, which is unusual and may suggest that other HAdV genotypes, in addition to HAdV-C, may also be harbored by wild animals. The data generated in the present study reinforces the importance of eco-surveillance of viral agents related to diseases in humans and wild animals. In addition, it is essential to identify possible new hosts or reservoirs that increase the risk of spillover and dissemination of infectious pathogens, helping to prevent and control zoonotic diseases.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data Availability
The virus sequences obtained in the present study were deposited in GenBank under accession numbers OQ689002–OQ689009.
References
Ai, L., Zhu, C., Zhang, W., He, T., Ke, Y., Wu, J., Yin, W., Zou, X., Ding, C., Luo, Y., Wang, C., Qian, H., & Tan, W. (2022). Genomic characteristics and pathogenicity of a new bat adenoviruses strains that was isolated in at sites along the southeastern coasts of the P. R. of China from 2015 to 2019. Virus Research, 308, 198653. https://doi.org/10.1016/j.virusres.2021.198653
Asano, K. M., Gregori, F., Hora, A. S., Scheffer, K. C., Fahl, W. O., Iamamoto, K., Mori, E., Silva, F. D., Taniwaki, S. A., & Brandão, P. E. (2016). Group A rotavirus in Brazilian bats: Description of novel T15 and H15 genotypes. Archives of Virology, 161, 3225–3230. https://doi.org/10.1007/s00705-016-3010-9
Banerjee, A., Baker, M. L., Kulcsar, K., Misra, V., Plowright, R., & Mossman, K. (2020). Novel insights into immune systems of bats. Frontiers in Immunology. https://doi.org/10.3389/fimmu.2020.00026
Banerjee, A., Kulcsar, K., Misra, V., Frieman, M., & Mossman, K. (2019). Bats and coronaviruses. Viruses, 11, 7–9. https://doi.org/10.3390/v11010041
Bosch, A., Guix, S., Sano, D., & Pintó, R. M. (2008). New tools for the study and direct surveillance of viral pathogens in water. Current Opinion in Biotechnology, 19, 295–301. https://doi.org/10.1016/j.copbio.2008.04.006
Chiappetta, C. M., Cibulski, S. P., Lima, F. E. S., Varela, A. P. M., Amorim, D. B., Tavares, M., & Roehe, P. M. (2017). Molecular detection of circovirus and adenovirus in feces of fur seals (Arctocephalus spp.). EcoHealth, 14, 69–77. https://doi.org/10.1007/s10393-016-1195-8
da Silva, L. C., Almeida, R. G., da Silva, P. H., Oprea, M., Mendes, P., Brito, D., & Bernardi Vieira, T. (2021). Temporal changes in the potential geographic distribution of Histiotus velatus (Chiroptera, Vespertilionidae), the “decade effect.” Ecology and Evolution, 11(23), 16972–16980. https://doi.org/10.1002/ece3.8333
Demoliner, M., Gularte, J. S., Girardi, V., Eisen, A. K., de Souza, F. G., Staggemeier, R., Henzel, A., & Spilki, F. R. (2021). Microbial source tracking in small farms: Use of different methods for adenovirus detection. Water, Air, and Soil Pollution, 232, 63. https://doi.org/10.1007/s11270-021-05011-8
Egert-Berg, K., Handel, M., Goldshtein, A., Eitan, O., Borissov, I., & Yovel, Y. (2021). Fruit bats adjust their foraging strategies to urban environments to diversify their diet. BMC Biology, 19, 123. https://doi.org/10.1186/s12915-021-01060-x
Ellwanger, J. H., Fearnside, P. M., Ziliotto, M., Valverde-Villegas, J. M., Veiga, A. B. G. D., Vieira, G. F., Bach, E., Cardoso, J. C., Müller, N. F. D., Lopes, G., Caesar, L., Kulmann-Leal, B., Kaminski, V. L., Silveira, E. S., Spilki, F. R., Weber, M. N., Almeida, S. E. M., Hora, V. P. D., & Chies, J. A. B. (2022). Synthesizing the connections between environmental disturbances and zoonotic spillover. Anais da Academia Brasileira de Ciências, 94, e20211530. https://doi.org/10.1590/0001-3765202220211530
Finoketti, F., dos Santos, R. N., Campos, A. A. S., Zani, A. L. D. S., Barboza, C. M., Fernandes, M. E. S., de Souza, T. C. P., dos Santos, D. D., Bortolanza, G. W., Filho, H. O., Roehe, P. M., Franco, A. C., & de CarvalhoRuthnerBatista, H. B. (2019). Detection of adenovirus, papillomavirus and parvovirus in Brazilian bats of the species Artibeus lituratus and Sturnira lilium. Archives of Virology, 164, 1015–1025. https://doi.org/10.1007/s00705-018-04129-1
Gartner, L. E., Demoliner, M., Girardi, V., de Oliveira, K. G., de Souza, F. G., & Henzel, A. (2022). Detection of Protoparvovirus in wastewater and human adenovirus in a green leafy vegetable in an environmental education center in southern Brazil. Water Policy, 24(12), 1827–1841. https://doi.org/10.2166/wp.2022.062
Gularte, J. S., de Oliveira, Hansen R., Demoliner, M., Fiutowski, J., Eisen, A. K., Heldt, F. H., Rodrigues de Almeida, P., Müller de Quevedo, D., Rubahn, H. G., & Rosado Spilki, F. (2021). Functionalized surfaces as a tool for virus sensing: A demonstration of human mastadenovirus detection in environmental waters. Chemosensors, 9, 19. https://doi.org/10.3390/chemosensors9020019
Hackenbrack, N., Rogers, M. B., Ashley, R. E., Keel, M. K., Kubiski, S. V., Bryan, J. A., Ghedin, E., Holmes, E. C., Hafenstein, S. L., & Allison, A. B. (2017). Evolution and cryo-electron microscopy capsid structure of a North American bat adenovirus and its relationship to other mastadenoviruses. Journal of Virology, 91, e0150416. https://doi.org/10.1128/jvi.01504-16
Iglesias-Caballero, M., Juste, J., Vázquez-Morón, S., Falcon, A., Aznar-Lopez, C., Ibáñez, C., Pozo, F., Ruiz, G., Berciano, J. M., Garin, I., Aihartza, J., Echevarría, J. E., & Casas, I. (2018). New adenovirus groups in western palaearctic bats. Viruses, 10, 443. https://doi.org/10.3390/v10080443
Irving, A. T., Ahn, M., Goh, G., Anderson, D. E., & Wang, L. F. (2021). Lessons from the host defences of bats, a unique viral reservoir. Nature. https://doi.org/10.1038/s41586-020-03128-0
Katoh, K., & Standley, D. M. (2013). MAFFT multiple sequence alignment software version 7: Improvements in performance and usability. Molecular Biology and Evolution, 30, 772–780. https://doi.org/10.1093/molbev/mst010
Kim, H. K., Yoon, S. W., Kim, D. J., Koo, B. S., Noh, J. Y., Kim, J. H., Choi, Y. G., Na, W., Chang, K. T., Song, D., & Jeong, D. G. (2016). Detection of severe acute respiratory syndrome-like, middle east respiratory syndrome-like bat coronaviruses and group h rotavirus in faeces of Korean Bats. Transboundary and emerging diseases, 63(4), 365–372. https://doi.org/10.1111/tbed.12515
Kittigul, L., Ekchaloemkiet, S., Utrarachkij, F., Siripanichgon, K., Sujirarat, D., Pungchitton, S., & Boonthum, A. (2005). An efficient virus concentration method and RT-nested PCR for detection of rotaviruses in environmental water samples. Journal of Virological Methods, 124, 117–122. https://doi.org/10.1016/j.jviromet.2004.11.013
Kosulin, K., Geiger, E., Vécsei, A., Huber, W. D., Rauch, M., Brenner, E., Wrba, F., Hammer, K., Innerhofer, A., Pötschger, U., Lawitschka, A., Matthes-Leodolter, S., Fritsch, G., & Lion, T. (2016). Persistence and reactivation of human adenoviruses in the gastrointestinal tract. Clinical Microbiology and Infection, 22, 381.e1-381.e8. https://doi.org/10.1016/j.cmi.2015.12.013
Kuzmin, I. V., Mayer, A. E., Niezgoda, M., Markotter, W., Agwanda, B., Breiman, R. F., & Rupprecht, C. E. (2010). Shimoni bat virus, a new representative of the Lyssavirus genus. Virus Research, 149, 197–210. https://doi.org/10.1016/j.virusres.2010.01.018
Letko, M., Seifert, S. N., Olival, K. J., Plowright, R. K., & Munster, V. J. (2020). Bat-borne virus diversity, spillover and emergence. Nature Reviews Microbiology. https://doi.org/10.1038/s41579-020-0394-z
Li, Y., Ge, X., Zhang, H., Zhou, P., Zhu, Y., Zhang, Y., Yuan, J., Wang, L. F., & Shi, Z. (2010). Host range, prevalence, and genetic diversity of adenoviruses in bats. Journal of Virology, 84, 3889–3897. https://doi.org/10.1128/jvi.02497-09
Lima, F. E. D. S., Cibulski, S. P., Elesbao, F., Carnieli Junior, P., Batista, H. B. D. C. R., Roehe, P. M., & Franco, A. C. (2013). First detection of adenovirus in the vampire bat (Desmodus rotundus) in Brazil. Virus Genes, 47, 378–381. https://doi.org/10.1007/s11262-013-0947-6
Luis, A. D., Hayman, D. T., O’Shea, T. J., Cryan, P. M., Gilbert, A. T., Pulliam, J. R., Mills, J. N., Timonin, M. E., Willis, C. K., Cunningham, A. A., Fooks, A. R., Rupprecht, C. E., Wood, J. L., & Webb, C. T. (2013). A comparison of bats and rodents as reservoirs of zoonotic viruses: Are bats special? Proceedings of the Royal Society B: Biological Sciences, 280, 20122753. https://doi.org/10.1098/rspb.2012.2753
Menezes, P. Q., Silva, T. T., Simas, F. B., Brauner, R. K., Bandarra, P., Demoliner, M., Eisen, A. K. A., Rodrigues, P., Spilki, F. R., Fischer, G., & Hübner, S. O. (2020). Molecular detection of human adenovirus and rotavirus in feces of white-eared opossums. EcoHealth, 17, 326–332. https://doi.org/10.1007/s10393-020-01497-6
Monteiro, G. S., Fleck, J. D., Kluge, M., Rech, N. K., Soliman, M. C., Staggemeier, R., Rodrigues, M. T., Barros, M. P., Heinzelmann, L. S., & Spilki, F. R. (2015). Adenoviruses of canine and human origins in stool samples from free-living pampas foxes (Lycalopex gymnocercus) and crab-eating foxes (Cerdocyon thous) in São Francisco de Paula, Rio dos Sinos basin. Brazilian Journal of Biology, 75, S11–S16. https://doi.org/10.1590/1519-6984.0313
Nakamura, N., Kobayashi, S., Minagawa, H., Matsushita, T., Sugiura, W., & Iwatani, Y. (2016). Molecular epidemiology of enteric viruses in patients with acute gastroenteritis in Aichi prefecture, Japan, 2008/09-2013/14. Journal of Medical Virology, 88, 1180–1186. https://doi.org/10.1002/jmv.24445
Oleaga, A., Balseiro, A., Espí, A., & Royo, L. J. (2022). Wolf (Canis lupus) as canine adenovirus type 1 (CAdV-1) sentinel for the endangered cantabrian brown bear (Ursus arctos arctos). Transboundary and Emerging Diseases, 69, 516–523. https://doi.org/10.1111/tbed.14010
Oliveira, F. W., Santin, M., Schindler, Z., Hennayra Corá, D., Thiel, N., Siebel, A. M., & Galiano, D. (2020). Oxidative state of the frugivorous bat Sturnira lilium (Chiroptera: Phyllostomidae) in agricultural and urban areas of southern Brazil. Environmental Science and Pollution Research, 27, 30868–30874. https://doi.org/10.1007/s11356-020-09552-z/Published
Parashar, U. D., Gibson, C. J., Bresee, J. S., & Glass, R. I. (2006). Rotavirus and severe childhood diarrhea. Emerging Infectious Diseases, 12, 304–306.
Prado, T., & Miagostovich, M. P. (2014). Environmental virology and sanitation in Brazil: A narrative review. Cadernos De Saúde Publica, 30, 1367–1378. https://doi.org/10.1590/0102-311X00109213
Radke, J. R., & Cook, J. L. (2018). Human adenovirus infections: Update and consideration of mechanisms of viral persistence. Current Opinion in Infectious Diseases. https://doi.org/10.1097/QCO.0000000000000451
Raut, C. G., Yadav, P. D., Towner, J. S., Amman, B. R., Erickson, B. R., Cannon, D. L., Sivaram, A., Basu, A., Nichol, S. T., Mishra, A. C., & Mourya, D. T. (2012). Isolation of a novel adenovirus from Rousettus leschenaultii bats from India. Intervirology, 55, 488–490. https://doi.org/10.1159/000337026
Sita, A., Birlem, G. E., de Almeida, P. R., Stein, J. F., Mallmann, L., Demoliner, M., da Silva, M. S., Gularte, J. S., Hansen, A. W., Fleck, J. D., Spilki, F. R., Higino, S. S. S., de Azevedo, S. S., da Rocha, D. T., & Weber, M. N. (2022). Detection of human Mastadenovirus C in wild guinea pigs (Cavia aperea aperea) feces. Brazilian Journal of Microbiology, 53, 2101–2105. https://doi.org/10.1007/s42770-022-00829-
Soares, V. M., dos Santos, E. A. R., Tadielo, L. E., Cerqueira-Cézar, C. K., da CruzEncideSampaio, A. N., Eisen, A. K. A., de Oliveira, K. G., Padilha, M. B., de Moraes Guerra, M. E., Gasparetto, R., Brum, M. C. S., Traesel, C. K., Henzel, A., Spilki, F. R., & Pereira, J. G. (2022). Detection of adenovirus, rotavirus, and hepatitis E virus in meat cuts marketed in Uruguaiana, Rio Grande do Sul Brazil. One Health, 14, 100377. https://doi.org/10.1016/j.onehlt.2022.100377
Tamura, K., Stecher, G., & Kumar, S. (2021). MEGA11: Molecular evolutionary genetics analysis version 11. Molecular Biology and Evolution, 38(7), 3022–3027. https://doi.org/10.1093/molbev/msab120
Vecchia, A. D., Fleck, J. D., Comerlato, J., Kluge, M., Bergamaschi, B., da Silva, J. V., da Luz, R. B., Teixeira, T. F., Garbinatto, G. N., Oliveira, D. V., Zanin, J. G., van der Sand, S., Frazzon, A. P., Franco, A. C., Roehe, P. M., & Spilki, F. R. (2012). First description of Adenovirus, Enterovirus, Rotavirus and Torque teno virus in water samples collected from the Arroio Diluvio, Porto Alegre, Brazil. Brazilian Journal of Biology, 72, 323–329.
Waruhiu, C., Ommeh, S., Obanda, V., Agwanda, B., Gakuya, F., Ge, X. Y., Yang, X. L., Wu, L. J., Zohaib, A., Hu, B., & Shi, Z. L. (2017). Molecular detection of viruses in Kenyan bats and discovery of novel astroviruses, caliciviruses and rotaviruses. Virologica Sinica, 32, 101–114. https://doi.org/10.1007/s12250-016-3930-2
Acknowledgements
The authors thank all the members of the laboratory for helping with the experiment.
Funding
This study was funded by Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) - 50/2022 INCT Vigilância Genômica de Vírus e Saúde Única, Fundação de Amparo à Pesquisa do Estado do Rio Grande do Sul (FAPERGS) - 23/2551-0000143-8, Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) - Finance Code 001, and PROPPEX/FEEVALE.
Author information
Authors and Affiliations
Contributions
Conceptualization, PRA, AAW, CR, JDF, FRS and MNW; methodology, MD, JSG, FRS and MNW; sample collection, AS, GEB, KP, DSS, PRA, AAW and DTR; sample processing, AS, GEB, DSS, GMP, LM, JFS, MD and JSG; software, AS and MNW; writing—original draft preparation, AS, KP, AWH, FRS, MNW; writing—review and editing, AS, JDF, FRS, DTR and MNW; project administration, MNW; funding acquisition, FRS and MNW. All authors have read and agreed to the published version of the manuscript.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Sita, A., Birlem, G.E., de Souza da Silva, D. et al. Evaluation of Mastadenovirus and Rotavirus Presence in Phyllostomid, Vespertilionid, and Molossid Bats Captured in Rio Grande do Sul, Southern Brazil. Food Environ Virol (2024). https://doi.org/10.1007/s12560-023-09575-y
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s12560-023-09575-y