The draft genome of strain cCpun from biting midges confirms insect Cardinium are not a monophyletic group and reveals a novel gene family expansion in a symbiont
Background It is estimated that 13% of arthropod species carry the heritable symbiont Cardinium hertigii. 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 Cul...
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PeerJ Inc.
2019-02-01
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| Online Access: | https://peerj.com/articles/6448.pdf |
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| author | Stefanos Siozios Jack Pilgrim Alistair C. Darby Matthew Baylis Gregory D.D. Hurst |
| author_facet | Stefanos Siozios Jack Pilgrim Alistair C. Darby Matthew Baylis Gregory D.D. Hurst |
| author_sort | Stefanos Siozios |
| collection | DOAJ |
| description | Background It is estimated that 13% of arthropod species carry the heritable symbiont Cardinium hertigii. 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 Culicoides biting midges, and the D group associated with the marine copepod Nitocra spinipes. 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 Cardinium, motivated both by the paucity of genomic information outside of the A and B group, and the importance of Culicoides biting midge hosts as arbovirus vectors. Methods We reconstructed the genome of cCpun, a Cardinium strain from group C that naturally infects Culicoides punctatus, through Illumina sequencing of infected host specimens. Results The draft genome presented has high completeness, with BUSCO scores comparable to closed group A Cardinium genomes. Phylogenomic analysis based on concatenated single copy core proteins do not support Cardinium from arthropod hosts as a monophyletic group, with nematode Cardinium strains nested within the two groups infecting arthropod hosts. Analysis of the genome of cCpun 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 cCpun 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 Cardinium may be a net importer of biotin. Discussion These data indicate strains of Cardinium within nematodes cluster within Cardinium strains found in insects. The draft genome of cCpun 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 cCpun. In contrast, the coding content of this genome provides no support for a role for the symbiont in provisioning the host with B vitamins. |
| first_indexed | 2024-03-09T06:22:09Z |
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| id | doaj.art-c457869fdc3643e59a378349c5539b4c |
| institution | Directory Open Access Journal |
| issn | 2167-8359 |
| language | English |
| last_indexed | 2024-03-09T06:22:09Z |
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| spelling | doaj.art-c457869fdc3643e59a378349c5539b4c2023-12-03T11:35:09ZengPeerJ Inc.PeerJ2167-83592019-02-017e644810.7717/peerj.6448The draft genome of strain cCpun from biting midges confirms insect Cardinium are not a monophyletic group and reveals a novel gene family expansion in a symbiontStefanos Siozios0Jack Pilgrim1Alistair C. Darby2Matthew Baylis3Gregory D.D. Hurst4Institute of Integrative Biology, Faculty of Health and Life Sciences, University of Liverpool, Liverpool, UKInstitute of Infection and Global Health, Faculty of Health and Life Sciences, University of Liverpool, Liverpool, UKInstitute of Integrative Biology, Faculty of Health and Life Sciences, University of Liverpool, Liverpool, UKInstitute of Infection and Global Health, Faculty of Health and Life Sciences, University of Liverpool, Liverpool, UKInstitute of Integrative Biology, Faculty of Health and Life Sciences, University of Liverpool, Liverpool, UKBackground It is estimated that 13% of arthropod species carry the heritable symbiont Cardinium hertigii. 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 Culicoides biting midges, and the D group associated with the marine copepod Nitocra spinipes. 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 Cardinium, motivated both by the paucity of genomic information outside of the A and B group, and the importance of Culicoides biting midge hosts as arbovirus vectors. Methods We reconstructed the genome of cCpun, a Cardinium strain from group C that naturally infects Culicoides punctatus, through Illumina sequencing of infected host specimens. Results The draft genome presented has high completeness, with BUSCO scores comparable to closed group A Cardinium genomes. Phylogenomic analysis based on concatenated single copy core proteins do not support Cardinium from arthropod hosts as a monophyletic group, with nematode Cardinium strains nested within the two groups infecting arthropod hosts. Analysis of the genome of cCpun 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 cCpun 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 Cardinium may be a net importer of biotin. Discussion These data indicate strains of Cardinium within nematodes cluster within Cardinium strains found in insects. The draft genome of cCpun 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 cCpun. In contrast, the coding content of this genome provides no support for a role for the symbiont in provisioning the host with B vitamins.https://peerj.com/articles/6448.pdfCardinium hertigiiCulicoides biting midgesGenome sequencePhylogenomic analysisGene family expansionHeritable symbionts |
| spellingShingle | Stefanos Siozios Jack Pilgrim Alistair C. Darby Matthew Baylis Gregory D.D. Hurst The draft genome of strain cCpun from biting midges confirms insect Cardinium are not a monophyletic group and reveals a novel gene family expansion in a symbiont PeerJ Cardinium hertigii Culicoides biting midges Genome sequence Phylogenomic analysis Gene family expansion Heritable symbionts |
| title | The draft genome of strain cCpun from biting midges confirms insect Cardinium are not a monophyletic group and reveals a novel gene family expansion in a symbiont |
| title_full | The draft genome of strain cCpun from biting midges confirms insect Cardinium are not a monophyletic group and reveals a novel gene family expansion in a symbiont |
| title_fullStr | The draft genome of strain cCpun from biting midges confirms insect Cardinium are not a monophyletic group and reveals a novel gene family expansion in a symbiont |
| title_full_unstemmed | The draft genome of strain cCpun from biting midges confirms insect Cardinium are not a monophyletic group and reveals a novel gene family expansion in a symbiont |
| title_short | The draft genome of strain cCpun from biting midges confirms insect Cardinium are not a monophyletic group and reveals a novel gene family expansion in a symbiont |
| title_sort | draft genome of strain ccpun from biting midges confirms insect cardinium are not a monophyletic group and reveals a novel gene family expansion in a symbiont |
| topic | Cardinium hertigii Culicoides biting midges Genome sequence Phylogenomic analysis Gene family expansion Heritable symbionts |
| url | https://peerj.com/articles/6448.pdf |
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