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

Abstract

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: 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: 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.

Keywords: Black swan; Genomes; Virology.

Fig. 1

Position of the frame-shift mutation in the mute swan SLC45A2 compared to the black swan genome. The figure was created with whole-genome HAL alignment produced from CACTUS. The alignment was visualized with the University of California, Santa Cruz (UCSC) Genome Assembly in a Box (GBiB). The predicted mute swan gene SLC45A2 was aligned using the BLAT alignment algorithm.

Fig. 2

Gene losses and gains across vertebrate species tree. Data are shown for 17 vertebrate species, three teleost (red), an amphibian (green), six reptilians (including birds) (black, blue, and orange), and five mammals (yellow). The numbers of gene family gains (+) and losses (−) are given to the right of the taxa (p-value < 0.05) compared to the taxon’s last common ancestor. The rate of gene birth and death for clades derived from the most recent common ancestor (MRCA) for Gallianseriformes is 0.0016 (per gene per million years)

Fig. 3

GO enrichment analysis for over-represented GO terms associated with significantly expanded gene families in black swan, mute swan, chicken, and mallard duck

Fig. 4

Principal component analysis (PCA) of infected and uninfected A black swan, B chicken, and C duck endothelial cells. The control and the infected groups showed intergroup clustering, indicating differences in whole transcriptome profiles between the control and the infected group in each species

Fig. 5

Top 30 GO biological process terms that were significantly enriched in infected A black swan, B chicken, and C duck endothelial cells. The bars represent the enrichment score for the corresponding GO biological term with a p-value <0.05