Discovery of all three types in cartilaginous fishes enables phylogenetic resolution of the origins and evolution of interferons

Anthony K. Redmond (Corresponding Author), Jun Zou, Christopher J. Secombes, Daniel J. MacQueen, Helen Dooley (Corresponding Author)

Research output: Contribution to journalArticle

1 Citation (Scopus)

Abstract

Interferons orchestrate host antiviral responses in jawed vertebrates. They are categorized into three classes; IFN1 and IFN3 are the primary antiviral cytokine lineages, while IFN2 responds to a broader variety of pathogens. The evolutionary relationships within and between these three classes have proven difficult to resolve. Here, we reassess interferon evolution, considering key phylogenetic pitfalls including taxon sampling, alignment quality, model adequacy, and outgroup choice. We reveal that cartilaginous fishes, and hence the jawed vertebrate ancestor, possess(ed) orthologs of all three interferon classes. We show that IFN3 groups sister to IFN1, resolve the origins of the human IFN3 lineages, and find that intronless IFN3s emerged at least three times. IFN2 genes are highly conserved, except for IFN-γ-rel, which we confirm resulted from a teleost-specific duplication. Our analyses show that IFN1 phylogeny is highly sensitive to phylogenetic error. By accounting for this, we describe a new backbone IFN1 phylogeny, that implies several IFN1 genes existed in the jawed vertebrate ancestor. One of these is represented by the intronless IFN1s of tetrapods, including mammalian-like repertoires of reptile IFN1s and a subset of amphibian IFN1s, in addition to newly-identified intron-containing shark IFN1 genes. IFN-f, previously only found in teleosts, likely represents another ancestral jawed vertebrate IFN1 family member, suggesting the current classification of fish IFN1s into two groups based on the number of cysteines may need revision. The providence of the remaining fish IFN1s and the coelacanth IFN1s proved difficult to resolve, but they may also be ancestral jawed vertebrate IFN1 lineages. Finally, a large group of amphibian-specific IFN1s falls sister to all other IFN1s and was likely also present in the jawed vertebrate ancestor. Our results verify that intronless IFN1s have evolved multiple times in amphibians and indicate that no one-to-one orthology exists between mammal and reptile IFN1s. Our data also imply that diversification of the multiple IFN1s present in the jawed vertebrate ancestor has occurred through a rapid birth-death process, consistent with functional maintenance over a 450-million-year host-pathogen arms race. In summary, this study reveals a new model of interferon evolution important to our understanding of jawed vertebrate antiviral immunity.
Original languageEnglish
Article number1558
Number of pages16
JournalFrontiers in Immunology
Volume10
Early online date12 Jul 2019
DOIs
Publication statusPublished - Jul 2019

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Interferons
Vertebrates
Fishes
Amphibians
Antiviral Agents
Reptiles
Phylogeny
Siblings
Genes
Sharks
Introns
Cysteine
Mammals
Immunity
Maintenance
Parturition
Cytokines

Keywords

  • interferon
  • evolution
  • shark
  • phylogenetics
  • Jawed vertebrates (gnathostomes)
  • antiviral immunity
  • retrotransposition
  • cytokine
  • Cytokine
  • Shark
  • Retrotransposition
  • Antiviral immunity
  • Jawed vertebrate
  • Phylogenetics
  • Evolution
  • Interferon
  • IFN-GAMMA
  • DEATH EVOLUTION
  • CONTAINING TYPE-I
  • jawed vertebrate
  • MIXTURE-MODELS
  • CRYSTAL-STRUCTURE
  • INBORN-ERRORS
  • LAMBDA
  • SEQUENCE ALIGNMENT
  • GENE FAMILY
  • REVEALS

ASJC Scopus subject areas

  • Immunology and Allergy
  • Immunology

Cite this

Discovery of all three types in cartilaginous fishes enables phylogenetic resolution of the origins and evolution of interferons. / Redmond, Anthony K. (Corresponding Author); Zou, Jun; Secombes, Christopher J.; MacQueen, Daniel J.; Dooley, Helen (Corresponding Author).

In: Frontiers in Immunology, Vol. 10, 1558, 07.2019.

Research output: Contribution to journalArticle

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N1 - Data Availability All datasets generated and analyzed for the study are included in the manuscript and the Supplementary Files. Acknowledgments PhyloBayes analyses were performed using the University of Aberdeen's Maxwell high performance computing cluster. AR was supported by a University of Aberdeen Center for Genome-Enabled Biology and Medicine Ph.D. studentship. DM received support from BBSRC Institutional Strategic Programme funding (grant number: BBS/E/D/20002172). Silhouettes in Figure 7 were obtained from http://phylopic.org; all of which are public domain except for the anole lizard silhouette, which was created by Ghedo and T. Michael Keesey (license: https://creativecommons.org/licenses/by-sa/3.0/).

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N2 - Interferons orchestrate host antiviral responses in jawed vertebrates. They are categorized into three classes; IFN1 and IFN3 are the primary antiviral cytokine lineages, while IFN2 responds to a broader variety of pathogens. The evolutionary relationships within and between these three classes have proven difficult to resolve. Here, we reassess interferon evolution, considering key phylogenetic pitfalls including taxon sampling, alignment quality, model adequacy, and outgroup choice. We reveal that cartilaginous fishes, and hence the jawed vertebrate ancestor, possess(ed) orthologs of all three interferon classes. We show that IFN3 groups sister to IFN1, resolve the origins of the human IFN3 lineages, and find that intronless IFN3s emerged at least three times. IFN2 genes are highly conserved, except for IFN-γ-rel, which we confirm resulted from a teleost-specific duplication. Our analyses show that IFN1 phylogeny is highly sensitive to phylogenetic error. By accounting for this, we describe a new backbone IFN1 phylogeny, that implies several IFN1 genes existed in the jawed vertebrate ancestor. One of these is represented by the intronless IFN1s of tetrapods, including mammalian-like repertoires of reptile IFN1s and a subset of amphibian IFN1s, in addition to newly-identified intron-containing shark IFN1 genes. IFN-f, previously only found in teleosts, likely represents another ancestral jawed vertebrate IFN1 family member, suggesting the current classification of fish IFN1s into two groups based on the number of cysteines may need revision. The providence of the remaining fish IFN1s and the coelacanth IFN1s proved difficult to resolve, but they may also be ancestral jawed vertebrate IFN1 lineages. Finally, a large group of amphibian-specific IFN1s falls sister to all other IFN1s and was likely also present in the jawed vertebrate ancestor. Our results verify that intronless IFN1s have evolved multiple times in amphibians and indicate that no one-to-one orthology exists between mammal and reptile IFN1s. Our data also imply that diversification of the multiple IFN1s present in the jawed vertebrate ancestor has occurred through a rapid birth-death process, consistent with functional maintenance over a 450-million-year host-pathogen arms race. In summary, this study reveals a new model of interferon evolution important to our understanding of jawed vertebrate antiviral immunity.

AB - Interferons orchestrate host antiviral responses in jawed vertebrates. They are categorized into three classes; IFN1 and IFN3 are the primary antiviral cytokine lineages, while IFN2 responds to a broader variety of pathogens. The evolutionary relationships within and between these three classes have proven difficult to resolve. Here, we reassess interferon evolution, considering key phylogenetic pitfalls including taxon sampling, alignment quality, model adequacy, and outgroup choice. We reveal that cartilaginous fishes, and hence the jawed vertebrate ancestor, possess(ed) orthologs of all three interferon classes. We show that IFN3 groups sister to IFN1, resolve the origins of the human IFN3 lineages, and find that intronless IFN3s emerged at least three times. IFN2 genes are highly conserved, except for IFN-γ-rel, which we confirm resulted from a teleost-specific duplication. Our analyses show that IFN1 phylogeny is highly sensitive to phylogenetic error. By accounting for this, we describe a new backbone IFN1 phylogeny, that implies several IFN1 genes existed in the jawed vertebrate ancestor. One of these is represented by the intronless IFN1s of tetrapods, including mammalian-like repertoires of reptile IFN1s and a subset of amphibian IFN1s, in addition to newly-identified intron-containing shark IFN1 genes. IFN-f, previously only found in teleosts, likely represents another ancestral jawed vertebrate IFN1 family member, suggesting the current classification of fish IFN1s into two groups based on the number of cysteines may need revision. The providence of the remaining fish IFN1s and the coelacanth IFN1s proved difficult to resolve, but they may also be ancestral jawed vertebrate IFN1 lineages. Finally, a large group of amphibian-specific IFN1s falls sister to all other IFN1s and was likely also present in the jawed vertebrate ancestor. Our results verify that intronless IFN1s have evolved multiple times in amphibians and indicate that no one-to-one orthology exists between mammal and reptile IFN1s. Our data also imply that diversification of the multiple IFN1s present in the jawed vertebrate ancestor has occurred through a rapid birth-death process, consistent with functional maintenance over a 450-million-year host-pathogen arms race. In summary, this study reveals a new model of interferon evolution important to our understanding of jawed vertebrate antiviral immunity.

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KW - evolution

KW - shark

KW - phylogenetics

KW - Jawed vertebrates (gnathostomes)

KW - antiviral immunity

KW - retrotransposition

KW - cytokine

KW - Cytokine

KW - Shark

KW - Retrotransposition

KW - Antiviral immunity

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KW - Phylogenetics

KW - Evolution

KW - Interferon

KW - IFN-GAMMA

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KW - MIXTURE-MODELS

KW - CRYSTAL-STRUCTURE

KW - INBORN-ERRORS

KW - LAMBDA

KW - SEQUENCE ALIGNMENT

KW - GENE FAMILY

KW - REVEALS

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