The draft genome of strain <i>c</i>Cpun from biting midges confirms insect <i>Cardinium</i> are not a monophyletic group and reveals a novel gene family expansion in a symbiont

Siozios, Stefanos ORCID: 0000-0002-1104-7061, Pilgrim, Jack ORCID: 0000-0002-2941-1482, Darby, Alistair C ORCID: 0000-0002-3786-6209, Baylis, Matthew ORCID: 0000-0003-0335-187X and Hurst, Gregory DD ORCID: 0000-0002-7163-7784
(2019) The draft genome of strain <i>c</i>Cpun from biting midges confirms insect <i>Cardinium</i> are not a monophyletic group and reveals a novel gene family expansion in a symbiont. PEERJ, 7 (2). e6448-.

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<h4>Background</h4>It is estimated that 13% of arthropod species carry the heritable symbiont <i>Cardinium hertigii</i>. 16S rRNA and gyrB sequence divides this species into at least four groups (A-D), with the A group infecting a range of arthropods, the B group infecting nematode worms, the C group infecting <i>Culicoides</i> biting midges, and the D group associated with the marine copepod <i>Nitocra spinipes</i>. To date, genome sequence has only been available for strains from groups A and B, impeding general understanding of the evolutionary history of the radiation. We present a draft genome sequence for a C group <i>Cardinium</i>, motivated both by the paucity of genomic information outside of the A and B group, and the importance of <i>Culicoides</i> biting midge hosts as arbovirus vectors.<h4>Methods</h4>We reconstructed the genome of <i>c</i>Cpun, a <i>Cardinium</i> strain from group C that naturally infects <i>Culicoides punctatus</i>, through Illumina sequencing of infected host specimens.<h4>Results</h4>The draft genome presented has high completeness, with BUSCO scores comparable to closed group A <i>Cardinium</i> genomes. Phylogenomic analysis based on concatenated single copy core proteins do not support <i>Cardinium</i> from arthropod hosts as a monophyletic group, with nematode <i>Cardinium</i> strains nested within the two groups infecting arthropod hosts. Analysis of the genome of <i>c</i>Cpun revealed expansion of a variety of gene families classically considered important in symbiosis (e.g., ankyrin domain containing genes), and one set-characterized by DUF1703 domains-not previously associated with symbiotic lifestyle. This protein group encodes putative secreted nucleases, and the <i>c</i>Cpun genome carried at least 25 widely divergent paralogs, 24 of which shared a common ancestor in the C group. The genome revealed no evidence in support of B vitamin provisioning to its haematophagous host, and indeed suggests <i>Cardinium</i> may be a net importer of biotin.<h4>Discussion</h4>These data indicate strains of <i>Cardinium</i> within nematodes cluster within <i>Cardinium</i> strains found in insects. The draft genome of <i>c</i>Cpun further produces new hypotheses as to the interaction of the symbiont with the midge host, in particular the biological role of DUF1703 nuclease proteins that are predicted as being secreted by <i>c</i>Cpun. In contrast, the coding content of this genome provides no support for a role for the symbiont in provisioning the host with B vitamins.

Item Type: Article
Uncontrolled Keywords: Cardinium hertigii, Culicoides biting midges, Genome sequence, Phylogenomic analysis, Gene family expansion, Heritable symbionts
Depositing User: Symplectic Admin
Date Deposited: 04 Mar 2019 16:15
Last Modified: 14 Oct 2023 09:07
DOI: 10.7717/peerj.6448
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