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The evolution of the metazoan Toll receptor family and its expression during protostome development

View ORCID ProfileAndrea Orús-Alcalde, View ORCID ProfileTsai-Ming Lu, View ORCID ProfileAndreas Hejnol
doi: https://doi.org/10.1101/2021.02.01.429095
Andrea Orús-Alcalde
1Sars International Centre for Marine Molecular Biology, University of Bergen, Bergen, Norway
2University of Bergen, Department of Biological Sciences, Bergen, Norway
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  • ORCID record for Andrea Orús-Alcalde
Tsai-Ming Lu
1Sars International Centre for Marine Molecular Biology, University of Bergen, Bergen, Norway
2University of Bergen, Department of Biological Sciences, Bergen, Norway
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Andreas Hejnol
1Sars International Centre for Marine Molecular Biology, University of Bergen, Bergen, Norway
2University of Bergen, Department of Biological Sciences, Bergen, Norway
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  • For correspondence: andreas.hejnol@uib.no
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Abstract

Background Toll-like receptors (TLRs) play a crucial role in immunity and development. They contain leucine-rich repeat domains, one transmembrane domain, and one Toll/IL-1 receptor domain. TLRs have been classified into V-type/scc and P-type/mcc TLRs, based on differences in the leucine-rich repeat domain region. Although TLRs are widespread in animals, detailed phylogenetic studies of this gene family are lacking. Here we aim to uncover TLR evolution by conducting a survey and a phylogenetic analysis in species across Bilateria. To discriminate between their role in development and immunity we furthermore analyzed stage-specific transcriptomes of the ecdysozoans Priapulus caudatus and Hypsibius exemplaris, and the spiralians Crassostrea gigas and Terebratalia transversa.

Results We detected a low number of TLRs in ecdysozoan species, and multiple independent radiations within the Spiralia. V-type/scc and P-type/mcc type-receptors are present in cnidarians, protostomes and deuterostomes, and therefore they emerged early in TLR evolution, followed by a loss in xenacoelomorphs. Our phylogenetic analysis shows that TLRs cluster into three major clades: clade α is present in cnidarians, ecdysozoans, and spiralians; clade β in deuterostomes, ecdysozoans, and spiralians; and clade γ is only found in spiralians. Our stage-specific transcriptome and in situ hybridization analyses show that TLRs are expressed during development in all species analyzed, which indicates a broad role of TLRs during animal development.

Conclusions Our findings suggest that the bilaterian TLRs likely emerged by duplication from a single TLR encoding gene (proto-TLR) present in the last common cnidarian-bilaterian ancestor. This proto-TLR gene duplicated before the split of protostomes and deuterostomes; a second duplication occurred in the lineage to the Trochozoa. While all three clades further radiated in several spiralian lineages, specific TLRs clades have been presumably lost in others. Furthermore, the expression of the majority of these genes during protostome ontogeny suggests their involvement in immunity and development.

Competing Interest Statement

The authors have declared no competing interest.

  • List of abbreviations

    AMPs
    Antimicrobial peptides
    BCIP
    5-bromo-4-chloro-3-indolyl phosphate
    BUSCO
    Benchmarking Universal Single-Copy Orthologs
    IL-1
    Interleukin-I receptor
    LRR
    Leucine-rich repeat
    LRRCT
    Leucine-rich repeat C-terminal domain
    LRRNT
    Leucine-rich repeat N-terminal domain
    Mcc
    multiple cysteine cluster
    NBT
    nitro blue tetrazolium
    NOD
    Nucleotide oligomerization domain
    PBS
    Phosphate-Buffered Saline
    P-type
    Protostome type
    PTw
    PBS with 0.1% Tween® 20
    RSEM
    RNA-Seq by Expectation Maximization
    Scc
    Single cysteine cluster
    TIR
    Toll/IL-1 receptor
    TLR
    Toll-like receptor
    TLR-Cα
    clade α type TLR gene
    TLR-Cβ
    clade β type TLR gene
    TLR-Cγ
    clade γ type TLR gene
    TLR-Cβ/γ
    proto-TLR gene of clades β and γ
    TLR-like
    Toll-like receptor-like
    TM
    Transmembrane
    TMM
    Trimmed mean of M values
    TPM
    Transcripts per million
    V-type
    Vertebrate type
    WMISH
    Whole mount in situ hybridization
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    Posted February 02, 2021.
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    The evolution of the metazoan Toll receptor family and its expression during protostome development
    Andrea Orús-Alcalde, Tsai-Ming Lu, Andreas Hejnol
    bioRxiv 2021.02.01.429095; doi: https://doi.org/10.1101/2021.02.01.429095
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    The evolution of the metazoan Toll receptor family and its expression during protostome development
    Andrea Orús-Alcalde, Tsai-Ming Lu, Andreas Hejnol
    bioRxiv 2021.02.01.429095; doi: https://doi.org/10.1101/2021.02.01.429095

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