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Phylogenetic analysis of cell-cycle regulatory proteins within the Symbiodiniaceae

Gorman, Lucy M. and Wilkinson, Shaun P. and Kitchen, Sheila A. and Oakley, Clinton A. and Grossman, Arthur R. and Weis, Virginia M. and Davy, Simon K. (2020) Phylogenetic analysis of cell-cycle regulatory proteins within the Symbiodiniaceae. Scientific Reports, 10 . Art. No. 20473. ISSN 2045-2322. PMCID PMC7686383. https://resolver.caltech.edu/CaltechAUTHORS:20201125-100253645

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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.


Item Type:Article
Related URLs:
URLURL TypeDescription
https://doi.org/10.1038/s41598-020-76621-1DOIArticle
https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7686383PubMed CentralArticle
ORCID:
AuthorORCID
Wilkinson, Shaun P.0000-0002-7332-7931
Kitchen, Sheila A.0000-0003-4402-8139
Oakley, Clinton A.0000-0002-4673-0645
Grossman, Arthur R.0000-0002-3747-5881
Weis, Virginia M.0000-0002-1826-2848
Davy, Simon K.0000-0003-3584-5356
Additional Information:© The Author(s) 2020. This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. Received 11 April 2020; Accepted 28 October 2020; Published 24 November 2020. This research was supported by the Marsden Fund of the Royal Society Te Apārangi of New Zealand (Grant Number VUW1601), awarded to S.K.D., A.R.G., V.M.W. and C.A.O. and an associated PhD scholarship to L.M.G. Additional support was provided via strategic research funds from the School of Biological Sciences at Victoria University of Wellington to S.K.D. Author Contributions: The study was conceptualised by L.M.G., C.A.O., A.R.G., V.M.W., and S.K.D. L.M.G. wrote the manuscript, collected and analysed the sequence and phylogenetic data, and constructed all figures (apart from figure 3) and all tables. S.P.W. helped L.M.G. with data collection and analysis. S.A.K. conducted and analysed the expression analysis, constructed figure 3, helped revise the manuscript, and advised on methods, data analysis and visualisation, C.A.O., V.M.W., S.K.D., A.R.G. helped edit and refine the manuscript. All authors reviewed the manuscript before submission. The authors declare no competing interests.
Funders:
Funding AgencyGrant Number
Marsden FundUNSPECIFIED
Royal Society Te ApārangiVUW1601
Victoria University of WellingtonUNSPECIFIED
Subject Keywords:Evolutionary biology; Marine biology
PubMed Central ID:PMC7686383
Record Number:CaltechAUTHORS:20201125-100253645
Persistent URL:https://resolver.caltech.edu/CaltechAUTHORS:20201125-100253645
Official Citation:Gorman, L.M., Wilkinson, S.P., Kitchen, S.A. et al. Phylogenetic analysis of cell-cycle regulatory proteins within the Symbiodiniaceae. Sci Rep 10, 20473 (2020). https://doi.org/10.1038/s41598-020-76621-1
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:106824
Collection:CaltechAUTHORS
Deposited By: Tony Diaz
Deposited On:25 Nov 2020 18:19
Last Modified:02 Dec 2020 17:10

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