The swan genome and transcriptome, it is not all black and white.


Journal

Genome biology
ISSN: 1474-760X
Titre abrégé: Genome Biol
Pays: England
ID NLM: 100960660

Informations de publication

Date de publication:
23 Jan 2023
Historique:
received: 27 05 2022
accepted: 12 12 2022
entrez: 22 1 2023
pubmed: 23 1 2023
medline: 25 1 2023
Statut: epublish

Résumé

The Australian black swan (Cygnus atratus) is an iconic species with contrasting plumage to that of the closely related northern hemisphere white swans. The relative geographic isolation of the black swan may have resulted in a limited immune repertoire and increased susceptibility to infectious diseases, notably infectious diseases from which Australia has been largely shielded. Unlike mallard ducks and the mute swan (Cygnus olor), the black swan is extremely sensitive to highly pathogenic avian influenza. Understanding this susceptibility has been impaired by the absence of any available swan genome and transcriptome information. Here, we generate the first chromosome-length black and mute swan genomes annotated with transcriptome data, all using long-read based pipelines generated for vertebrate species. We use these genomes and transcriptomes to show that unlike other wild waterfowl, black swans lack an expanded immune gene repertoire, lack a key viral pattern-recognition receptor in endothelial cells and mount a poorly controlled inflammatory response to highly pathogenic avian influenza. We also implicate genetic differences in SLC45A2 gene in the iconic plumage of the black swan. Together, these data suggest that the immune system of the black swan is such that should any avian viral infection become established in its native habitat, the black swan would be in a significant peril.

Sections du résumé

BACKGROUND BACKGROUND
The Australian black swan (Cygnus atratus) is an iconic species with contrasting plumage to that of the closely related northern hemisphere white swans. The relative geographic isolation of the black swan may have resulted in a limited immune repertoire and increased susceptibility to infectious diseases, notably infectious diseases from which Australia has been largely shielded. Unlike mallard ducks and the mute swan (Cygnus olor), the black swan is extremely sensitive to highly pathogenic avian influenza. Understanding this susceptibility has been impaired by the absence of any available swan genome and transcriptome information.
RESULTS RESULTS
Here, we generate the first chromosome-length black and mute swan genomes annotated with transcriptome data, all using long-read based pipelines generated for vertebrate species. We use these genomes and transcriptomes to show that unlike other wild waterfowl, black swans lack an expanded immune gene repertoire, lack a key viral pattern-recognition receptor in endothelial cells and mount a poorly controlled inflammatory response to highly pathogenic avian influenza. We also implicate genetic differences in SLC45A2 gene in the iconic plumage of the black swan.
CONCLUSION CONCLUSIONS
Together, these data suggest that the immune system of the black swan is such that should any avian viral infection become established in its native habitat, the black swan would be in a significant peril.

Identifiants

pubmed: 36683094
doi: 10.1186/s13059-022-02838-0
pii: 10.1186/s13059-022-02838-0
pmc: PMC9867998
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

13

Subventions

Organisme : NHGRI NIH HHS
ID : UM1 HG009375
Pays : United States
Organisme : Wellcome Trust
ID : 108749/Z/15/Z, 222155/Z/20/Z
Pays : United Kingdom

Informations de copyright

© 2023. The Author(s).

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Auteurs

Anjana C Karawita (AC)

School of Chemistry and Molecular Biosciences, The University of Queensland, St Lucia, QLD, 4072, Australia.
Commonwealth Scientific and Industrial Research Organisation, Australian Centre for Disease Preparedness, 5 Portarlington Road, Geelong, VIC, 3220, Australia.

Yuanyuan Cheng (Y)

School of Life and Environmental Sciences, The University of Sydney, Sydney, NSW, 2006, Australia.

Keng Yih Chew (KY)

School of Chemistry and Molecular Biosciences, The University of Queensland, St Lucia, QLD, 4072, Australia.

Arjun Challagulla (A)

Commonwealth Scientific and Industrial Research Organisation, Australian Centre for Disease Preparedness, 5 Portarlington Road, Geelong, VIC, 3220, Australia.

Robert Kraus (R)

Department of Migration, Max Planck Institute of Animal Behavior, Radolfzell, 78315, Germany.
Department of Biology, University of Konstanz, Konstanz, 78457, Germany.

Ralf C Mueller (RC)

Department of Migration, Max Planck Institute of Animal Behavior, Radolfzell, 78315, Germany.
Department of Biology, University of Konstanz, Konstanz, 78457, Germany.

Marcus Z W Tong (MZW)

School of Chemistry and Molecular Biosciences, The University of Queensland, St Lucia, QLD, 4072, Australia.

Katina D Hulme (KD)

School of Chemistry and Molecular Biosciences, The University of Queensland, St Lucia, QLD, 4072, Australia.

Helle Bielefeldt-Ohmann (H)

School of Chemistry and Molecular Biosciences, The University of Queensland, St Lucia, QLD, 4072, Australia.

Lauren E Steele (LE)

School of Chemistry and Molecular Biosciences, The University of Queensland, St Lucia, QLD, 4072, Australia.

Melanie Wu (M)

School of Chemistry and Molecular Biosciences, The University of Queensland, St Lucia, QLD, 4072, Australia.

Julian Sng (J)

School of Chemistry and Molecular Biosciences, The University of Queensland, St Lucia, QLD, 4072, Australia.

Ellesandra Noye (E)

School of Chemistry and Molecular Biosciences, The University of Queensland, St Lucia, QLD, 4072, Australia.

Timothy J Bruxner (TJ)

Institute for Molecular Bioscience, The University of Queensland, St Lucia, QLD, 4072, Australia.

Gough G Au (GG)

Commonwealth Scientific and Industrial Research Organisation, Australian Centre for Disease Preparedness, 5 Portarlington Road, Geelong, VIC, 3220, Australia.

Suzanne Lowther (S)

Commonwealth Scientific and Industrial Research Organisation, Australian Centre for Disease Preparedness, 5 Portarlington Road, Geelong, VIC, 3220, Australia.

Julie Blommaert (J)

Department of Organismal Biology - Systematic Biology, Evolutionary Biology Centre, Uppsala University, Science for Life Laboratory, Uppsala, 752 36, Sweden.
The New Zealand Institute for Plant & Food Research Ltd, Nelson, 7010, New Zealand.

Alexander Suh (A)

Department of Organismal Biology - Systematic Biology, Evolutionary Biology Centre, Uppsala University, Science for Life Laboratory, Uppsala, 752 36, Sweden.
School of Biological Sciences, University of East Anglia, Norwich Research Park, Norwich, NR4 7TU, UK.

Alexander J McCauley (AJ)

Commonwealth Scientific and Industrial Research Organisation, Australian Centre for Disease Preparedness, 5 Portarlington Road, Geelong, VIC, 3220, Australia.

Parwinder Kaur (P)

School of Agriculture and Environment, The University of Western Australia, Perth, WA, 6009, Australia.

Olga Dudchenko (O)

The Centre for Genome Architecture, Department of Molecular and Human Genetics, Baylor College of Medicine, Houston, TX, 77030, USA.
Centre for Theoretical Biological Physics and Department of Computer Science, Rice University, Houston, TX, 77030, USA.

Erez Aiden (E)

School of Agriculture and Environment, The University of Western Australia, Perth, WA, 6009, Australia.
The Centre for Genome Architecture, Department of Molecular and Human Genetics, Baylor College of Medicine, Houston, TX, 77030, USA.
Centre for Theoretical Biological Physics and Department of Computer Science, Rice University, Houston, TX, 77030, USA.
Broad Institute of MIT and Harvard, Cambridge, MA, 02139, USA.
Shanghai Institute for Advanced Immunochemical Studies, ShanghaiTech, Pudong, 201210, China.

Olivier Fedrigo (O)

The Vertebrate Genome Laboratory, The Rockefeller University, NY, 10065, USA.

Giulio Formenti (G)

The Vertebrate Genome Laboratory, The Rockefeller University, NY, 10065, USA.

Jacquelyn Mountcastle (J)

The Vertebrate Genome Laboratory, The Rockefeller University, NY, 10065, USA.

William Chow (W)

Tree of Life, Welcome Sanger Institute, Cambridge, CB10 1SA, UK.

Fergal J Martin (FJ)

European Molecular Biology Laboratory, European Bioinformatics Institute, Wellcome Genome Campus, Hinxton, Cambridge, CB10 1SD, UK.

Denye N Ogeh (DN)

European Molecular Biology Laboratory, European Bioinformatics Institute, Wellcome Genome Campus, Hinxton, Cambridge, CB10 1SD, UK.

Françoise Thiaud-Nissen (F)

National Centre for Biotechnology Information, National Library of Medicine, National Institutes of Health, Bethesda, MD, USA.

Kerstin Howe (K)

Tree of Life, Welcome Sanger Institute, Cambridge, CB10 1SA, UK.

Alan Tracey (A)

Tree of Life, Welcome Sanger Institute, Cambridge, CB10 1SA, UK.

Jacqueline Smith (J)

The Roslin Institute and Royal (Dick) School of Veterinary Studies, University of Edinburgh, Easter Bush Campus, Midlothian, EH25 9RG, UK.

Richard I Kuo (RI)

The Roslin Institute and Royal (Dick) School of Veterinary Studies, University of Edinburgh, Easter Bush Campus, Midlothian, EH25 9RG, UK.

Marilyn B Renfree (MB)

School of Biosciences, The University of Melbourne, Melbourne, VIC, 3052, Australia.

Takashi Kimura (T)

Faculty of Veterinary Medicine, Hokkaido University, Sapporo, Hokkaido, 060-0818, Japan.

Yoshihiro Sakoda (Y)

Faculty of Veterinary Medicine, Hokkaido University, Sapporo, Hokkaido, 060-0818, Japan.

Mathew McDougall (M)

New Zealand Fish & Game - Eastern Region, Rotorua, 3046, New Zealand.

Hamish G Spencer (HG)

Department of Zoology, University of Otago, Dunedin, 9054, New Zealand.

Michael Pyne (M)

Currumbin Wildlife Sanctuary, Currumbin, QLD, 4223, Australia.

Conny Tolf (C)

Centre for Ecology and Evolution in Microbial Model Systems (EEMiS), Linnaeus University, Kalmar, SE-391 82, Sweden.

Jonas Waldenström (J)

Centre for Ecology and Evolution in Microbial Model Systems (EEMiS), Linnaeus University, Kalmar, SE-391 82, Sweden.

Erich D Jarvis (ED)

The Vertebrate Genome Laboratory, The Rockefeller University, NY, 10065, USA.

Michelle L Baker (ML)

Commonwealth Scientific and Industrial Research Organisation, Australian Centre for Disease Preparedness, 5 Portarlington Road, Geelong, VIC, 3220, Australia.

David W Burt (DW)

School of Chemistry and Molecular Biosciences, The University of Queensland, St Lucia, QLD, 4072, Australia.

Kirsty R Short (KR)

School of Chemistry and Molecular Biosciences, The University of Queensland, St Lucia, QLD, 4072, Australia. k.short@uq.edu.au.

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