Skip to main content
Top
Published in: Virology Journal 1/2021

Open Access 01-12-2021 | Coronavirus | Short report

Investigation of astrovirus, coronavirus and paramyxovirus co-infections in bats in the western Indian Ocean

Authors: Axel O. G. Hoarau, Steven M. Goodman, Dana Al Halabi, Beza Ramasindrazana, Erwan Lagadec, Gildas Le Minter, Marie Köster, Andréa Dos Santos, M. Corrie Schoeman, Eduardo S. Gudo, Patrick Mavingui, Camille Lebarbenchon

Published in: Virology Journal | Issue 1/2021

Login to get access

Abstract

Co-infections have a key role in virus transmission in wild reservoir hosts. We investigated the simultaneous presence of astroviruses, coronaviruses, and paramyxoviruses in bats from Madagascar, Mayotte, Mozambique, and Reunion Island. A total of 871 samples from 28 bat species representing 8 families were tested by polymerase chain reactions (PCRs) targeting the RNA-dependent RNA-polymerase genes. Overall, 2.4% of bats tested positive for the presence of at least two viruses, only on Madagascar and in Mozambique. Significant variation in the proportion of co-infections was detected among bat species, and some combinations of co-infection were more common than others. Our findings support that co-infections of the three targeted viruses occur in bats in the western Indian Ocean region, although further studies are needed to assess their epidemiological consequences.
Appendix
Available only for authorised users
Literature
1.
go back to reference Petney TN, Andrews RH. Multiparasite communities in animals and humans: frequency, structure and pathogenic significance. Int J Parasitol. 1998;28:377–93.CrossRef Petney TN, Andrews RH. Multiparasite communities in animals and humans: frequency, structure and pathogenic significance. Int J Parasitol. 1998;28:377–93.CrossRef
2.
go back to reference Cox FEG. Concomitant infections, parasites and immune responses. Parasitology. 2001;122:S23-38.CrossRef Cox FEG. Concomitant infections, parasites and immune responses. Parasitology. 2001;122:S23-38.CrossRef
3.
go back to reference Rigaud T, Perrot-Minnot M-J, Brown MJF. Parasite and host assemblages: embracing the reality will improve our knowledge of parasite transmission and virulence. Proc R Soc B Biol Sci. 2010;277:3693–702.CrossRef Rigaud T, Perrot-Minnot M-J, Brown MJF. Parasite and host assemblages: embracing the reality will improve our knowledge of parasite transmission and virulence. Proc R Soc B Biol Sci. 2010;277:3693–702.CrossRef
4.
go back to reference Vaumourin E, Vourc’h G, Gasqui P, Vayssier-Taussat M. The importance of multiparasitism: examining the consequences of co-infections for human and animal health. Parasites Vectors. 2015;8:545. Vaumourin E, Vourc’h G, Gasqui P, Vayssier-Taussat M. The importance of multiparasitism: examining the consequences of co-infections for human and animal health. Parasites Vectors. 2015;8:545.
5.
go back to reference Hoarau AOG, Mavingui P, Lebarbenchon C. Coinfections in wildlife: focus on a neglected aspect of infectious disease epidemiology. PLOS Pathogens. 2020;16:e1008790. Hoarau AOG, Mavingui P, Lebarbenchon C. Coinfections in wildlife: focus on a neglected aspect of infectious disease epidemiology. PLOS Pathogens. 2020;16:e1008790.
6.
go back to reference Pedersen AB, Fenton A. Emphasizing the ecology in parasite community ecology. Trends Ecol Evol. 2007;22:133–9.CrossRef Pedersen AB, Fenton A. Emphasizing the ecology in parasite community ecology. Trends Ecol Evol. 2007;22:133–9.CrossRef
7.
go back to reference Hellard E, Fouchet D, Vavre F, Pontier D. Parasite–parasite interactions in the wild: How to detect them? Trends Parasitol. 2015;31:640–52.CrossRef Hellard E, Fouchet D, Vavre F, Pontier D. Parasite–parasite interactions in the wild: How to detect them? Trends Parasitol. 2015;31:640–52.CrossRef
8.
go back to reference Peel AJ, Wells K, Giles J, Boyd V, Burroughs A, Edson D, et al. Synchronous shedding of multiple bat paramyxoviruses coincides with peak periods of Hendra virus spillover. Emerg Microbes Infect. 2019;8:1314–23.CrossRef Peel AJ, Wells K, Giles J, Boyd V, Burroughs A, Edson D, et al. Synchronous shedding of multiple bat paramyxoviruses coincides with peak periods of Hendra virus spillover. Emerg Microbes Infect. 2019;8:1314–23.CrossRef
10.
go back to reference Rizzo F, Edenborough KM, Toffoli R, Culasso P, Zoppi S, Dondo A, et al. Coronavirus and paramyxovirus in bats from northwest Italy. BMC Vet Res. 2017;13(1):396.CrossRef Rizzo F, Edenborough KM, Toffoli R, Culasso P, Zoppi S, Dondo A, et al. Coronavirus and paramyxovirus in bats from northwest Italy. BMC Vet Res. 2017;13(1):396.CrossRef
11.
go back to reference Seltmann A, Corman VM, Rasche A, Drosten C, Czirják GÁ, Bernard H, et al. Seasonal fluctuations of astrovirus, but not coronavirus shedding in bats inhabiting human-modified tropical forests. EcoHealth. 2017;14:272–84.CrossRef Seltmann A, Corman VM, Rasche A, Drosten C, Czirják GÁ, Bernard H, et al. Seasonal fluctuations of astrovirus, but not coronavirus shedding in bats inhabiting human-modified tropical forests. EcoHealth. 2017;14:272–84.CrossRef
12.
go back to reference Luis AD, Hayman DTS, O’Shea TJ, Cryan PM, Gilbert AT, Pulliam JRC, et al. A comparison of bats and rodents as reservoirs of zoonotic viruses: Are bats special? Proc R Soc B Biol Sci. 2013;280:20122753.CrossRef Luis AD, Hayman DTS, O’Shea TJ, Cryan PM, Gilbert AT, Pulliam JRC, et al. A comparison of bats and rodents as reservoirs of zoonotic viruses: Are bats special? Proc R Soc B Biol Sci. 2013;280:20122753.CrossRef
13.
go back to reference Anthony SJ, Epstein JH, Murray KA, Navarrete-Macias I, Zambrana-Torrelio CM, Solovyov A, et al. A strategy to estimate unknown viral diversity in mammals. mBio. 2013;4(5):e00598-13. Anthony SJ, Epstein JH, Murray KA, Navarrete-Macias I, Zambrana-Torrelio CM, Solovyov A, et al. A strategy to estimate unknown viral diversity in mammals. mBio. 2013;4(5):e00598-13.
14.
go back to reference Iehlé C, Razafitrimo G, Razainirina J, Andriaholinirina N, Goodman SM, Faure C, et al. Henipavirus and Tioman virus antibodies in pteropodid bats. Madagascar Emerg Infect Dis. 2007;13:159–61.CrossRef Iehlé C, Razafitrimo G, Razainirina J, Andriaholinirina N, Goodman SM, Faure C, et al. Henipavirus and Tioman virus antibodies in pteropodid bats. Madagascar Emerg Infect Dis. 2007;13:159–61.CrossRef
15.
go back to reference Wilkinson DA, Temmam S, Lebarbenchon C, Lagadec E, Chotte J, Guillebaud J, et al. Identification of novel paramyxoviruses in insectivorous bats of the Southwest Indian Ocean. Virus Res. 2012;170:159–63.CrossRef Wilkinson DA, Temmam S, Lebarbenchon C, Lagadec E, Chotte J, Guillebaud J, et al. Identification of novel paramyxoviruses in insectivorous bats of the Southwest Indian Ocean. Virus Res. 2012;170:159–63.CrossRef
16.
go back to reference Wilkinson DA, Melade J, Dietrich M, Ramasindrazana B, Soarimalala V, Lagadec E, et al. Highly diverse Morbillivirus-related paramyxoviruses in wild fauna of the southwestern Indian Ocean islands: evidence of exchange between introduced and endemic small mammals. J Virol. 2014;88:8268–77.CrossRef Wilkinson DA, Melade J, Dietrich M, Ramasindrazana B, Soarimalala V, Lagadec E, et al. Highly diverse Morbillivirus-related paramyxoviruses in wild fauna of the southwestern Indian Ocean islands: evidence of exchange between introduced and endemic small mammals. J Virol. 2014;88:8268–77.CrossRef
17.
go back to reference Dietrich M, Wilkinson DA, Benlali A, Lagadec E, Ramasindrazana B, Dellagi K, et al. Leptospira and paramyxovirus infection dynamics in a bat maternity enlightens pathogen maintenance in wildlife: dual infection dynamics in a bat maternity. Environ Microbiol. 2015;17:4280–9.CrossRef Dietrich M, Wilkinson DA, Benlali A, Lagadec E, Ramasindrazana B, Dellagi K, et al. Leptospira and paramyxovirus infection dynamics in a bat maternity enlightens pathogen maintenance in wildlife: dual infection dynamics in a bat maternity. Environ Microbiol. 2015;17:4280–9.CrossRef
18.
go back to reference Razanajatovo NH, Nomenjanahary LA, Wilkinson DA, Razafimanahaka JH, Goodman SM, Jenkins RK, et al. Detection of new genetic variants of Betacoronaviruses in endemic frugivorous bats of Madagascar. Virol J. 2015;12:42.CrossRef Razanajatovo NH, Nomenjanahary LA, Wilkinson DA, Razafimanahaka JH, Goodman SM, Jenkins RK, et al. Detection of new genetic variants of Betacoronaviruses in endemic frugivorous bats of Madagascar. Virol J. 2015;12:42.CrossRef
19.
go back to reference Mélade J, Wieseke N, Ramasindrazana B, Flores O, Lagadec E, Gomard Y, et al. An eco-epidemiological study of Morbilli-related paramyxovirus infection in Madagascar bats reveals host-switching as the dominant macro-evolutionary mechanism. Sci Rep. 2016;6:23752.CrossRef Mélade J, Wieseke N, Ramasindrazana B, Flores O, Lagadec E, Gomard Y, et al. An eco-epidemiological study of Morbilli-related paramyxovirus infection in Madagascar bats reveals host-switching as the dominant macro-evolutionary mechanism. Sci Rep. 2016;6:23752.CrossRef
20.
go back to reference Lebarbenchon C, Ramasindrazana B, Joffrin L, Bos S, Lagadec E, Le Minter G, et al. Astroviruses in bats, Madagascar. Emerg Microbes Infect. 2017;6:e58. Lebarbenchon C, Ramasindrazana B, Joffrin L, Bos S, Lagadec E, Le Minter G, et al. Astroviruses in bats, Madagascar. Emerg Microbes Infect. 2017;6:e58.
21.
go back to reference Hoarau F, Le Minter G, Joffrin L, Schoeman CM, Lagadec E, Ramasindrazana B, et al. Bat astrovirus in Mozambique. Virol J. 2018;15:104.CrossRef Hoarau F, Le Minter G, Joffrin L, Schoeman CM, Lagadec E, Ramasindrazana B, et al. Bat astrovirus in Mozambique. Virol J. 2018;15:104.CrossRef
22.
go back to reference Brook CE, Ranaivoson HC, Broder CC, Cunningham AA, Héraud J, Peel AJ, et al. Disentangling serology to elucidate henipa‐ and filovirus transmission in Madagascar fruit bats. J Anim Ecol. 2019;88:1001–16. Brook CE, Ranaivoson HC, Broder CC, Cunningham AA, Héraud J, Peel AJ, et al. Disentangling serology to elucidate henipa‐ and filovirus transmission in Madagascar fruit bats. J Anim Ecol. 2019;88:1001–16.
23.
go back to reference Joffrin L, Goodman SM, Wilkinson DA, Ramasindrazana B, Lagadec E, Gomard Y, et al. Bat coronavirus phylogeography in the western Indian Ocean. Sci Rep. 2020;10(1):6873.CrossRef Joffrin L, Goodman SM, Wilkinson DA, Ramasindrazana B, Lagadec E, Gomard Y, et al. Bat coronavirus phylogeography in the western Indian Ocean. Sci Rep. 2020;10(1):6873.CrossRef
24.
go back to reference Chu DKW, Poon LLM, Guan Y, Peiris JSM. Novel Astroviruses in insectivorous bats. J Virol. 2008;82:9107–14.CrossRef Chu DKW, Poon LLM, Guan Y, Peiris JSM. Novel Astroviruses in insectivorous bats. J Virol. 2008;82:9107–14.CrossRef
25.
go back to reference Tong S, Chern S-WW, Li Y, Pallansch MA, Anderson LJ. Sensitive and broadly reactive reverse transcription-PCR assays to detect novel paramyxoviruses. J Clin Microbiol. 2008;46:2652–8.CrossRef Tong S, Chern S-WW, Li Y, Pallansch MA, Anderson LJ. Sensitive and broadly reactive reverse transcription-PCR assays to detect novel paramyxoviruses. J Clin Microbiol. 2008;46:2652–8.CrossRef
26.
go back to reference R Core Team. R: a language and environment for statistical computing. R Foundation for Statistical Computing Vienna, Austria; 2015 R Core Team. R: a language and environment for statistical computing. R Foundation for Statistical Computing Vienna, Austria; 2015
27.
go back to reference Schliep KP. phangorn: phylogenetic analysis in R. Bioinformatics. 2011;27:592–3.CrossRef Schliep KP. phangorn: phylogenetic analysis in R. Bioinformatics. 2011;27:592–3.CrossRef
28.
go back to reference Altschul S. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 1997;25:3389–402.CrossRef Altschul S. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 1997;25:3389–402.CrossRef
29.
go back to reference Zhang Z, Schwartz S, Wagner L, Miller W. A greedy algorithm for aligning DNA sequences. J Comput Biol. 2000;7:203–14.CrossRef Zhang Z, Schwartz S, Wagner L, Miller W. A greedy algorithm for aligning DNA sequences. J Comput Biol. 2000;7:203–14.CrossRef
30.
go back to reference Guindon S, Dufayard J-F, Lefort V, Anisimova M, Hordijk W, Gascuel O. New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 30. Syst Biol. 2010;59:307–21.CrossRef Guindon S, Dufayard J-F, Lefort V, Anisimova M, Hordijk W, Gascuel O. New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 30. Syst Biol. 2010;59:307–21.CrossRef
31.
go back to reference Drexler JF, Corman VM, Müller MA, Maganga GD, Vallo P, Binger T, et al. Bats host major mammalian paramyxoviruses. Nat Commun. 2012;3:796.CrossRef Drexler JF, Corman VM, Müller MA, Maganga GD, Vallo P, Binger T, et al. Bats host major mammalian paramyxoviruses. Nat Commun. 2012;3:796.CrossRef
32.
go back to reference Fischer K, Pinho dos Reis V, Balkema-Buschmann A. Bat astroviruses: towards understanding the transmission dynamics of a neglected virus family. Viruses. 2017;9:34. Fischer K, Pinho dos Reis V, Balkema-Buschmann A. Bat astroviruses: towards understanding the transmission dynamics of a neglected virus family. Viruses. 2017;9:34.
33.
go back to reference Ithete NL, Stoffberg S, Corman VM, Cottontail VM, Richards LR, Schoeman MC, et al. Close relative of human Middle East respiratory syndrome coronavirus in bat. S Afr Emerg Infect Dis. 2013;19:1697–9.CrossRef Ithete NL, Stoffberg S, Corman VM, Cottontail VM, Richards LR, Schoeman MC, et al. Close relative of human Middle East respiratory syndrome coronavirus in bat. S Afr Emerg Infect Dis. 2013;19:1697–9.CrossRef
34.
go back to reference Smith CS, de Jong CE, Meers J, Henning J, Wang L-F, Field HE. Coronavirus infection and diversity in bats in the Australasian region. EcoHealth. 2016;13:72–82.CrossRef Smith CS, de Jong CE, Meers J, Henning J, Wang L-F, Field HE. Coronavirus infection and diversity in bats in the Australasian region. EcoHealth. 2016;13:72–82.CrossRef
35.
go back to reference Willoughby A, Phelps K, PREDICT Consortium, Olival K. A comparative analysis of viral richness and viral sharing in cave-roosting bats. Diversity. 2017;9:35. Willoughby A, Phelps K, PREDICT Consortium, Olival K. A comparative analysis of viral richness and viral sharing in cave-roosting bats. Diversity. 2017;9:35.
36.
go back to reference Altizer S, Dobson A, Hosseini P, Hudson P, Pascual M, Rohani P. Seasonality and the dynamics of infectious diseases. Ecol Lett. 2006;9:467–84.CrossRef Altizer S, Dobson A, Hosseini P, Hudson P, Pascual M, Rohani P. Seasonality and the dynamics of infectious diseases. Ecol Lett. 2006;9:467–84.CrossRef
37.
go back to reference Drexler JF, Corman VM, Wegner T, Tateno AF, Zerbinati RM, Gloza-Rausch F, et al. Amplification of emerging viruses in a bat colony. Emerg Infect Dis. 2011;17:449–56.CrossRef Drexler JF, Corman VM, Wegner T, Tateno AF, Zerbinati RM, Gloza-Rausch F, et al. Amplification of emerging viruses in a bat colony. Emerg Infect Dis. 2011;17:449–56.CrossRef
38.
go back to reference Mühldorfer K, Speck S, Kurth A, Lesnik R, Freuling C, Müller T, et al. Diseases and causes of death in European bats: dynamics in disease susceptibility and infection rates. PLoS ONE. 2011;6:e29773. Mühldorfer K, Speck S, Kurth A, Lesnik R, Freuling C, Müller T, et al. Diseases and causes of death in European bats: dynamics in disease susceptibility and infection rates. PLoS ONE. 2011;6:e29773.
39.
go back to reference George DB, Webb CT, Farnsworth ML, O’Shea TJ, Bowen RA, Smith DL, et al. Host and viral ecology determine bat rabies seasonality and maintenance. Proc Natl Acad Sci. 2011;108:10208–13.CrossRef George DB, Webb CT, Farnsworth ML, O’Shea TJ, Bowen RA, Smith DL, et al. Host and viral ecology determine bat rabies seasonality and maintenance. Proc Natl Acad Sci. 2011;108:10208–13.CrossRef
40.
go back to reference Wacharapluesadee S, Boongird K, Wanghongsa S, Ratanasetyuth N, Supavonwong P, Saengsen D, et al. A longitudinal study of the prevalence of Nipah virus in Pteropus lylei bats in Thailand: evidence for seasonal preference in disease transmission. Vector-Borne Zoonot Dis. 2010;10:183–90.CrossRef Wacharapluesadee S, Boongird K, Wanghongsa S, Ratanasetyuth N, Supavonwong P, Saengsen D, et al. A longitudinal study of the prevalence of Nipah virus in Pteropus lylei bats in Thailand: evidence for seasonal preference in disease transmission. Vector-Borne Zoonot Dis. 2010;10:183–90.CrossRef
41.
go back to reference Joffrin L, Hoarau AOG, Lagadec E, Köster M, Ramanantsalama RV, Mavingui P, et al. Astrovirus in Reunion free-tailed bat (Mormopterus francoismoutoui). Viruses. 2021;13:1524.CrossRef Joffrin L, Hoarau AOG, Lagadec E, Köster M, Ramanantsalama RV, Mavingui P, et al. Astrovirus in Reunion free-tailed bat (Mormopterus francoismoutoui). Viruses. 2021;13:1524.CrossRef
42.
go back to reference Mendenhall IH, Smith GJD, Vijaykrishna D. Ecological drivers of virus evolution: astrovirus as a case study. J Virol. 2015;89:6978–81.CrossRef Mendenhall IH, Smith GJD, Vijaykrishna D. Ecological drivers of virus evolution: astrovirus as a case study. J Virol. 2015;89:6978–81.CrossRef
Metadata
Title
Investigation of astrovirus, coronavirus and paramyxovirus co-infections in bats in the western Indian Ocean
Authors
Axel O. G. Hoarau
Steven M. Goodman
Dana Al Halabi
Beza Ramasindrazana
Erwan Lagadec
Gildas Le Minter
Marie Köster
Andréa Dos Santos
M. Corrie Schoeman
Eduardo S. Gudo
Patrick Mavingui
Camille Lebarbenchon
Publication date
01-12-2021
Publisher
BioMed Central
Published in
Virology Journal / Issue 1/2021
Electronic ISSN: 1743-422X
DOI
https://doi.org/10.1186/s12985-021-01673-2

Other articles of this Issue 1/2021

Virology Journal 1/2021 Go to the issue