Brachiopod and mollusc biomineralisation is a conserved process that was lost in the phoronid–bryozoan stem lineage
Abstract Background Brachiopods and molluscs are lophotrochozoans with hard external shells which are often believed to have evolved convergently. While palaeontological data indicate that both groups are descended from biomineralising Cambrian ancestors, the closest relatives of brachiopods, phoron...
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| Format: | Article |
| Language: | English |
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BMC
2022-09-01
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| Series: | EvoDevo |
| Online Access: | https://doi.org/10.1186/s13227-022-00202-8 |
| _version_ | 1811208776066269184 |
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| author | Joel Vikberg Wernström Ludwik Gąsiorowski Andreas Hejnol |
| author_facet | Joel Vikberg Wernström Ludwik Gąsiorowski Andreas Hejnol |
| author_sort | Joel Vikberg Wernström |
| collection | DOAJ |
| description | Abstract Background Brachiopods and molluscs are lophotrochozoans with hard external shells which are often believed to have evolved convergently. While palaeontological data indicate that both groups are descended from biomineralising Cambrian ancestors, the closest relatives of brachiopods, phoronids and bryozoans, are mineralised to a much lower extent and are comparatively poorly represented in the Palaeozoic fossil record. Although brachiopod and mollusc shells are structurally analogous, genomic and proteomic evidence indicates that their formation involves a complement of conserved, orthologous genes. Here, we study a set of genes comprised of 3 homeodomain transcription factors, one signalling molecule and 6 structural proteins which are implicated in mollusc and brachiopod shell formation, search for their orthologs in transcriptomes or genomes of brachiopods, phoronids and bryozoans, and present expression patterns of 8 of the genes in postmetamorphic juveniles of the rhynchonelliform brachiopod T. transversa. Results Transcriptome and genome searches for the 10 target genes in the brachiopods Terebratalia transversa, Lingula anatina, Novocrania anomala, the bryozoans Bugula neritina and Membranipora membranacea, and the phoronids Phoronis australis and Phoronopsis harmeri resulted in the recovery of orthologs of the majority of the genes in all taxa. While the full complement of genes was present in all brachiopods with a single exception in L. anatina, a bloc of four genes could consistently not be retrieved from bryozoans and phoronids. The genes engrailed, distal-less, ferritin, perlucin, sp1 and sp2 were shown to be expressed in the biomineralising mantle margin of T. transversa juveniles. Conclusions The gene expression patterns we recovered indicate that while mineralised shells in brachiopods and molluscs are structurally analogous, their formation builds on a homologous process that involves a conserved complement of orthologous genes. Losses of some of the genes related to biomineralisation in bryozoans and phoronids indicate that loss of the capacity to form mineralised structures occurred already in the phoronid–bryozoan stem group and supports the idea that mineralised skeletons evolved secondarily in some of the bryozoan subclades. |
| first_indexed | 2024-04-12T04:27:22Z |
| format | Article |
| id | doaj.art-f5df98da625b433bbc8a55d507adf5bf |
| institution | Directory Open Access Journal |
| issn | 2041-9139 |
| language | English |
| last_indexed | 2024-04-12T04:27:22Z |
| publishDate | 2022-09-01 |
| publisher | BMC |
| record_format | Article |
| series | EvoDevo |
| spelling | doaj.art-f5df98da625b433bbc8a55d507adf5bf2022-12-22T03:48:02ZengBMCEvoDevo2041-91392022-09-0113111110.1186/s13227-022-00202-8Brachiopod and mollusc biomineralisation is a conserved process that was lost in the phoronid–bryozoan stem lineageJoel Vikberg Wernström0Ludwik Gąsiorowski1Andreas Hejnol2The Arctic University Museum of Norway, UiT–The Arctic University of NorwayDepartment of Biological Sciences, University of BergenDepartment of Biological Sciences, University of BergenAbstract Background Brachiopods and molluscs are lophotrochozoans with hard external shells which are often believed to have evolved convergently. While palaeontological data indicate that both groups are descended from biomineralising Cambrian ancestors, the closest relatives of brachiopods, phoronids and bryozoans, are mineralised to a much lower extent and are comparatively poorly represented in the Palaeozoic fossil record. Although brachiopod and mollusc shells are structurally analogous, genomic and proteomic evidence indicates that their formation involves a complement of conserved, orthologous genes. Here, we study a set of genes comprised of 3 homeodomain transcription factors, one signalling molecule and 6 structural proteins which are implicated in mollusc and brachiopod shell formation, search for their orthologs in transcriptomes or genomes of brachiopods, phoronids and bryozoans, and present expression patterns of 8 of the genes in postmetamorphic juveniles of the rhynchonelliform brachiopod T. transversa. Results Transcriptome and genome searches for the 10 target genes in the brachiopods Terebratalia transversa, Lingula anatina, Novocrania anomala, the bryozoans Bugula neritina and Membranipora membranacea, and the phoronids Phoronis australis and Phoronopsis harmeri resulted in the recovery of orthologs of the majority of the genes in all taxa. While the full complement of genes was present in all brachiopods with a single exception in L. anatina, a bloc of four genes could consistently not be retrieved from bryozoans and phoronids. The genes engrailed, distal-less, ferritin, perlucin, sp1 and sp2 were shown to be expressed in the biomineralising mantle margin of T. transversa juveniles. Conclusions The gene expression patterns we recovered indicate that while mineralised shells in brachiopods and molluscs are structurally analogous, their formation builds on a homologous process that involves a conserved complement of orthologous genes. Losses of some of the genes related to biomineralisation in bryozoans and phoronids indicate that loss of the capacity to form mineralised structures occurred already in the phoronid–bryozoan stem group and supports the idea that mineralised skeletons evolved secondarily in some of the bryozoan subclades.https://doi.org/10.1186/s13227-022-00202-8 |
| spellingShingle | Joel Vikberg Wernström Ludwik Gąsiorowski Andreas Hejnol Brachiopod and mollusc biomineralisation is a conserved process that was lost in the phoronid–bryozoan stem lineage EvoDevo |
| title | Brachiopod and mollusc biomineralisation is a conserved process that was lost in the phoronid–bryozoan stem lineage |
| title_full | Brachiopod and mollusc biomineralisation is a conserved process that was lost in the phoronid–bryozoan stem lineage |
| title_fullStr | Brachiopod and mollusc biomineralisation is a conserved process that was lost in the phoronid–bryozoan stem lineage |
| title_full_unstemmed | Brachiopod and mollusc biomineralisation is a conserved process that was lost in the phoronid–bryozoan stem lineage |
| title_short | Brachiopod and mollusc biomineralisation is a conserved process that was lost in the phoronid–bryozoan stem lineage |
| title_sort | brachiopod and mollusc biomineralisation is a conserved process that was lost in the phoronid bryozoan stem lineage |
| url | https://doi.org/10.1186/s13227-022-00202-8 |
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