Antarctic penguins as reservoirs of diversity for avian avulaviruses

Michelle Wille, Malet Aban, Jing Wang, Nicole Moore, Songhua Shan, John Marshall, Daniel González-Acuña, Dhanasekaran Vijaykrishna, Jeff Butler, Jianning Wang, Richard J. Hall, David T. Williams, Aeron C. Hurt

Research output: Contribution to journalArticleResearchpeer-review

Abstract

Wild birds harbor a huge diversity of avian avulaviruses (formerly avian paramyxoviruses). Antarctic penguin species have been screened for avian avulaviruses since the 1980s and, as such, are known hosts of these viruses. In this study, we screened three penguin species from the South Shetland Islands and the Antarctic Peninsula for avian avulaviruses. We show that Adelie penguins (Pygoscelis adeliae) are hosts for four different avian avulavirus species, the recently described avian avulaviruses 17 to 19 and avian avulavirus 10-like, never before isolated in Antarctica. A total of 24 viruses were isolated and sequenced; avian avulavirus 17 was the most common, and phylogenetic analysis demonstrated patterns of occurrence, with different genetic clusters corresponding to penguin age and location. Following infection in specific-pathogen-free (SPF) chickens, all four avian avulavirus species were shed from the oral cavity for up to 7 days postinfection. There was limited shedding from the cloaca in a proportion of infected chickens, and all but one bird seroconverted by day 21. No clinical signs were observed. Taken together, we propose that penguin species, including Antarctic penguins, may be the central reservoir for a diversity of avian avulavirus species and that these viruses have the potential to infect other avian hosts. IMPORTANCE Approximately 99% of all viruses are still to be described, and in our changing world, any one of these unknown viruses could potentially expand their host range and cause epidemic disease in wildlife, agricultural animals, or humans. Avian avulavirus 1 causes outbreaks in wild birds and poultry and is thus well described. However, for many avulavirus species, only a single specimen has been described, and their viral ecology and epidemiology are unknown. Through the detection of avian avulaviruses in penguins from Antarctica, we have been able to expand upon our understanding of three avian avulavirus species (avian avulaviruses 17 to 19) and report a potentially novel avulavirus species. Importantly, we show that penguins appear to play a key role in the epidemiology of avian avulaviruses, and we encourage additional sampling of this avian group.

Original languageEnglish
Article numbere0027119
Number of pages12
JournalJournal of Virology
Volume93
Issue number11
DOIs
Publication statusPublished - Jun 2019

Keywords

  • Adelie penguin
  • Antarctica
  • Avian avulavirus
  • Avian paramyxovirus
  • Disease ecology
  • Penguin
  • Sphenisciformes

Cite this

Wille, M., Aban, M., Wang, J., Moore, N., Shan, S., Marshall, J., ... Hurt, A. C. (2019). Antarctic penguins as reservoirs of diversity for avian avulaviruses. Journal of Virology, 93(11), [e0027119]. https://doi.org/10.1128/JVI.00271-19
Wille, Michelle ; Aban, Malet ; Wang, Jing ; Moore, Nicole ; Shan, Songhua ; Marshall, John ; González-Acuña, Daniel ; Vijaykrishna, Dhanasekaran ; Butler, Jeff ; Wang, Jianning ; Hall, Richard J. ; Williams, David T. ; Hurt, Aeron C. / Antarctic penguins as reservoirs of diversity for avian avulaviruses. In: Journal of Virology. 2019 ; Vol. 93, No. 11.
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abstract = "Wild birds harbor a huge diversity of avian avulaviruses (formerly avian paramyxoviruses). Antarctic penguin species have been screened for avian avulaviruses since the 1980s and, as such, are known hosts of these viruses. In this study, we screened three penguin species from the South Shetland Islands and the Antarctic Peninsula for avian avulaviruses. We show that Adelie penguins (Pygoscelis adeliae) are hosts for four different avian avulavirus species, the recently described avian avulaviruses 17 to 19 and avian avulavirus 10-like, never before isolated in Antarctica. A total of 24 viruses were isolated and sequenced; avian avulavirus 17 was the most common, and phylogenetic analysis demonstrated patterns of occurrence, with different genetic clusters corresponding to penguin age and location. Following infection in specific-pathogen-free (SPF) chickens, all four avian avulavirus species were shed from the oral cavity for up to 7 days postinfection. There was limited shedding from the cloaca in a proportion of infected chickens, and all but one bird seroconverted by day 21. No clinical signs were observed. Taken together, we propose that penguin species, including Antarctic penguins, may be the central reservoir for a diversity of avian avulavirus species and that these viruses have the potential to infect other avian hosts. IMPORTANCE Approximately 99{\%} of all viruses are still to be described, and in our changing world, any one of these unknown viruses could potentially expand their host range and cause epidemic disease in wildlife, agricultural animals, or humans. Avian avulavirus 1 causes outbreaks in wild birds and poultry and is thus well described. However, for many avulavirus species, only a single specimen has been described, and their viral ecology and epidemiology are unknown. Through the detection of avian avulaviruses in penguins from Antarctica, we have been able to expand upon our understanding of three avian avulavirus species (avian avulaviruses 17 to 19) and report a potentially novel avulavirus species. Importantly, we show that penguins appear to play a key role in the epidemiology of avian avulaviruses, and we encourage additional sampling of this avian group.",
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Wille, M, Aban, M, Wang, J, Moore, N, Shan, S, Marshall, J, González-Acuña, D, Vijaykrishna, D, Butler, J, Wang, J, Hall, RJ, Williams, DT & Hurt, AC 2019, 'Antarctic penguins as reservoirs of diversity for avian avulaviruses' Journal of Virology, vol. 93, no. 11, e0027119. https://doi.org/10.1128/JVI.00271-19

Antarctic penguins as reservoirs of diversity for avian avulaviruses. / Wille, Michelle; Aban, Malet; Wang, Jing; Moore, Nicole; Shan, Songhua; Marshall, John; González-Acuña, Daniel; Vijaykrishna, Dhanasekaran; Butler, Jeff; Wang, Jianning; Hall, Richard J.; Williams, David T.; Hurt, Aeron C.

In: Journal of Virology, Vol. 93, No. 11, e0027119, 06.2019.

Research output: Contribution to journalArticleResearchpeer-review

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T1 - Antarctic penguins as reservoirs of diversity for avian avulaviruses

AU - Wille, Michelle

AU - Aban, Malet

AU - Wang, Jing

AU - Moore, Nicole

AU - Shan, Songhua

AU - Marshall, John

AU - González-Acuña, Daniel

AU - Vijaykrishna, Dhanasekaran

AU - Butler, Jeff

AU - Wang, Jianning

AU - Hall, Richard J.

AU - Williams, David T.

AU - Hurt, Aeron C.

PY - 2019/6

Y1 - 2019/6

N2 - Wild birds harbor a huge diversity of avian avulaviruses (formerly avian paramyxoviruses). Antarctic penguin species have been screened for avian avulaviruses since the 1980s and, as such, are known hosts of these viruses. In this study, we screened three penguin species from the South Shetland Islands and the Antarctic Peninsula for avian avulaviruses. We show that Adelie penguins (Pygoscelis adeliae) are hosts for four different avian avulavirus species, the recently described avian avulaviruses 17 to 19 and avian avulavirus 10-like, never before isolated in Antarctica. A total of 24 viruses were isolated and sequenced; avian avulavirus 17 was the most common, and phylogenetic analysis demonstrated patterns of occurrence, with different genetic clusters corresponding to penguin age and location. Following infection in specific-pathogen-free (SPF) chickens, all four avian avulavirus species were shed from the oral cavity for up to 7 days postinfection. There was limited shedding from the cloaca in a proportion of infected chickens, and all but one bird seroconverted by day 21. No clinical signs were observed. Taken together, we propose that penguin species, including Antarctic penguins, may be the central reservoir for a diversity of avian avulavirus species and that these viruses have the potential to infect other avian hosts. IMPORTANCE Approximately 99% of all viruses are still to be described, and in our changing world, any one of these unknown viruses could potentially expand their host range and cause epidemic disease in wildlife, agricultural animals, or humans. Avian avulavirus 1 causes outbreaks in wild birds and poultry and is thus well described. However, for many avulavirus species, only a single specimen has been described, and their viral ecology and epidemiology are unknown. Through the detection of avian avulaviruses in penguins from Antarctica, we have been able to expand upon our understanding of three avian avulavirus species (avian avulaviruses 17 to 19) and report a potentially novel avulavirus species. Importantly, we show that penguins appear to play a key role in the epidemiology of avian avulaviruses, and we encourage additional sampling of this avian group.

AB - Wild birds harbor a huge diversity of avian avulaviruses (formerly avian paramyxoviruses). Antarctic penguin species have been screened for avian avulaviruses since the 1980s and, as such, are known hosts of these viruses. In this study, we screened three penguin species from the South Shetland Islands and the Antarctic Peninsula for avian avulaviruses. We show that Adelie penguins (Pygoscelis adeliae) are hosts for four different avian avulavirus species, the recently described avian avulaviruses 17 to 19 and avian avulavirus 10-like, never before isolated in Antarctica. A total of 24 viruses were isolated and sequenced; avian avulavirus 17 was the most common, and phylogenetic analysis demonstrated patterns of occurrence, with different genetic clusters corresponding to penguin age and location. Following infection in specific-pathogen-free (SPF) chickens, all four avian avulavirus species were shed from the oral cavity for up to 7 days postinfection. There was limited shedding from the cloaca in a proportion of infected chickens, and all but one bird seroconverted by day 21. No clinical signs were observed. Taken together, we propose that penguin species, including Antarctic penguins, may be the central reservoir for a diversity of avian avulavirus species and that these viruses have the potential to infect other avian hosts. IMPORTANCE Approximately 99% of all viruses are still to be described, and in our changing world, any one of these unknown viruses could potentially expand their host range and cause epidemic disease in wildlife, agricultural animals, or humans. Avian avulavirus 1 causes outbreaks in wild birds and poultry and is thus well described. However, for many avulavirus species, only a single specimen has been described, and their viral ecology and epidemiology are unknown. Through the detection of avian avulaviruses in penguins from Antarctica, we have been able to expand upon our understanding of three avian avulavirus species (avian avulaviruses 17 to 19) and report a potentially novel avulavirus species. Importantly, we show that penguins appear to play a key role in the epidemiology of avian avulaviruses, and we encourage additional sampling of this avian group.

KW - Adelie penguin

KW - Antarctica

KW - Avian avulavirus

KW - Avian paramyxovirus

KW - Disease ecology

KW - Penguin

KW - Sphenisciformes

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JO - Journal of Virology

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Wille M, Aban M, Wang J, Moore N, Shan S, Marshall J et al. Antarctic penguins as reservoirs of diversity for avian avulaviruses. Journal of Virology. 2019 Jun;93(11). e0027119. https://doi.org/10.1128/JVI.00271-19