Phylogenetic analysis of cell-cycle regulatory proteins within the Symbiodiniaceae

Abstract In oligotrophic waters, cnidarian hosts rely on symbiosis with their photosynthetic dinoflagellate partners (family Symbiodiniaceae) to obtain the nutrients they need to grow, reproduce and survive. For this symbiosis to persist, the host must regulate the growth and proliferation of its sy...

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Autores principales:	Lucy M. Gorman, Shaun P. Wilkinson, Sheila A. Kitchen, Clinton A. Oakley, Arthur R. Grossman, Virginia M. Weis, Simon K. Davy
Formato:	article
Lenguaje:	EN
Publicado:	Nature Portfolio 2020
Materias:	Medicine R Science Q
Acceso en línea:	https://doaj.org/article/aa0b4312c85547bc828b55fda294d785
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spelling	oai:doaj.org-article:aa0b4312c85547bc828b55fda294d7852021-12-02T15:10:31ZPhylogenetic analysis of cell-cycle regulatory proteins within the Symbiodiniaceae10.1038/s41598-020-76621-12045-2322https://doaj.org/article/aa0b4312c85547bc828b55fda294d7852020-11-01T00:00:00Zhttps://doi.org/10.1038/s41598-020-76621-1https://doaj.org/toc/2045-2322Abstract In oligotrophic waters, cnidarian hosts rely on symbiosis with their photosynthetic dinoflagellate partners (family Symbiodiniaceae) to obtain the nutrients they need to grow, reproduce and survive. For this symbiosis to persist, the host must regulate the growth and proliferation of its symbionts. One of the proposed regulatory mechanisms is arrest of the symbiont cell cycle in the G1 phase, though the cellular mechanisms involved remain unknown. Cell-cycle progression in eukaryotes is controlled by the conserved family of cyclin-dependent kinases (CDKs) and their partner cyclins. We identified CDKs and cyclins in different Symbiodiniaceae species and examined their relationship to homologs in other eukaryotes. Cyclin proteins related to eumetazoan cell-cycle-related cyclins A, B, D, G/I and Y, and transcriptional cyclin L, were identified in the Symbiodiniaceae, alongside several alveolate-specific cyclin A/B proteins, and proteins related to protist P/U-type cyclins and apicomplexan cyclins. The largest expansion of Symbiodiniaceae cyclins was in the P/U-type cyclin groups. Proteins related to eumetazoan cell-cycle-related CDKs (CDK1) were identified as well as transcription-related CDKs. The largest expansion of CDK groups was, however, in alveolate-specific groups which comprised 11 distinct CDK groups (CDKA-J) with CDKB being the most widely distributed CDK protein. As a result of its phylogenetic position, conservation across Symbiodiniaceae species, and the presence of the canonical CDK motif, CDKB emerged as a likely candidate for a Saccharomyces cerevisiae Cdc28/Pho85-like homolog in Symbiodiniaceae. Similar to cyclins, two CDK-groups found in Symbiodiniaceae species were solely associated with apicomplexan taxa. A comparison of Breviolum minutum CDK and cyclin gene expression between free-living and symbiotic states showed that several alveolate-specific CDKs and two P/U-type cyclins exhibited altered expression in hospite, suggesting that symbiosis influences the cell cycle of symbionts on a molecular level. These results highlight the divergence of Symbiodiniaceae cell-cycle proteins across species. These results have important implications for host control of the symbiont cell cycle in novel cnidarian–dinoflagellate symbioses.Lucy M. GormanShaun P. WilkinsonSheila A. KitchenClinton A. OakleyArthur R. GrossmanVirginia M. WeisSimon K. DavyNature PortfolioarticleMedicineRScienceQENScientific Reports, Vol 10, Iss 1, Pp 1-13 (2020)
institution	DOAJ
collection	DOAJ
language	EN
topic	Medicine R Science Q
spellingShingle	Medicine R Science Q Lucy M. Gorman Shaun P. Wilkinson Sheila A. Kitchen Clinton A. Oakley Arthur R. Grossman Virginia M. Weis Simon K. Davy Phylogenetic analysis of cell-cycle regulatory proteins within the Symbiodiniaceae
description	Abstract In oligotrophic waters, cnidarian hosts rely on symbiosis with their photosynthetic dinoflagellate partners (family Symbiodiniaceae) to obtain the nutrients they need to grow, reproduce and survive. For this symbiosis to persist, the host must regulate the growth and proliferation of its symbionts. One of the proposed regulatory mechanisms is arrest of the symbiont cell cycle in the G1 phase, though the cellular mechanisms involved remain unknown. Cell-cycle progression in eukaryotes is controlled by the conserved family of cyclin-dependent kinases (CDKs) and their partner cyclins. We identified CDKs and cyclins in different Symbiodiniaceae species and examined their relationship to homologs in other eukaryotes. Cyclin proteins related to eumetazoan cell-cycle-related cyclins A, B, D, G/I and Y, and transcriptional cyclin L, were identified in the Symbiodiniaceae, alongside several alveolate-specific cyclin A/B proteins, and proteins related to protist P/U-type cyclins and apicomplexan cyclins. The largest expansion of Symbiodiniaceae cyclins was in the P/U-type cyclin groups. Proteins related to eumetazoan cell-cycle-related CDKs (CDK1) were identified as well as transcription-related CDKs. The largest expansion of CDK groups was, however, in alveolate-specific groups which comprised 11 distinct CDK groups (CDKA-J) with CDKB being the most widely distributed CDK protein. As a result of its phylogenetic position, conservation across Symbiodiniaceae species, and the presence of the canonical CDK motif, CDKB emerged as a likely candidate for a Saccharomyces cerevisiae Cdc28/Pho85-like homolog in Symbiodiniaceae. Similar to cyclins, two CDK-groups found in Symbiodiniaceae species were solely associated with apicomplexan taxa. A comparison of Breviolum minutum CDK and cyclin gene expression between free-living and symbiotic states showed that several alveolate-specific CDKs and two P/U-type cyclins exhibited altered expression in hospite, suggesting that symbiosis influences the cell cycle of symbionts on a molecular level. These results highlight the divergence of Symbiodiniaceae cell-cycle proteins across species. These results have important implications for host control of the symbiont cell cycle in novel cnidarian–dinoflagellate symbioses.
format	article
author	Lucy M. Gorman Shaun P. Wilkinson Sheila A. Kitchen Clinton A. Oakley Arthur R. Grossman Virginia M. Weis Simon K. Davy
author_facet	Lucy M. Gorman Shaun P. Wilkinson Sheila A. Kitchen Clinton A. Oakley Arthur R. Grossman Virginia M. Weis Simon K. Davy
author_sort	Lucy M. Gorman
title	Phylogenetic analysis of cell-cycle regulatory proteins within the Symbiodiniaceae
title_short	Phylogenetic analysis of cell-cycle regulatory proteins within the Symbiodiniaceae
title_full	Phylogenetic analysis of cell-cycle regulatory proteins within the Symbiodiniaceae
title_fullStr	Phylogenetic analysis of cell-cycle regulatory proteins within the Symbiodiniaceae
title_full_unstemmed	Phylogenetic analysis of cell-cycle regulatory proteins within the Symbiodiniaceae
title_sort	phylogenetic analysis of cell-cycle regulatory proteins within the symbiodiniaceae
publisher	Nature Portfolio
publishDate	2020
url	https://doaj.org/article/aa0b4312c85547bc828b55fda294d785
work_keys_str_mv	AT lucymgorman phylogeneticanalysisofcellcycleregulatoryproteinswithinthesymbiodiniaceae AT shaunpwilkinson phylogeneticanalysisofcellcycleregulatoryproteinswithinthesymbiodiniaceae AT sheilaakitchen phylogeneticanalysisofcellcycleregulatoryproteinswithinthesymbiodiniaceae AT clintonaoakley phylogeneticanalysisofcellcycleregulatoryproteinswithinthesymbiodiniaceae AT arthurrgrossman phylogeneticanalysisofcellcycleregulatoryproteinswithinthesymbiodiniaceae AT virginiamweis phylogeneticanalysisofcellcycleregulatoryproteinswithinthesymbiodiniaceae AT simonkdavy phylogeneticanalysisofcellcycleregulatoryproteinswithinthesymbiodiniaceae
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Phylogenetic analysis of cell-cycle regulatory proteins within the Symbiodiniaceae

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