School of Biological Sciences, Victoria University of Wellington, Wellington, 6140, New Zealand.
Division of Biology and Biological Engineering, California Institute of Technology, Pasadena, CA, 91125, USA.
Sci Rep. 2020 Nov 24;10(1):20473. doi: 10.1038/s41598-020-76621-1.
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 G 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.
在贫营养水域中，刺胞动物宿主依赖与其光合作用的甲藻伙伴（Symbiodiniaceae 科）共生来获取生长、繁殖和生存所需的营养。为了使这种共生关系持续下去，宿主必须调节其共生体的生长和增殖。一种拟议的调节机制是将共生体的细胞周期阻滞在 G1 期，尽管涉及的细胞机制仍不清楚。真核生物的细胞周期进程受保守的细胞周期蛋白依赖性激酶（CDK）家族及其伴侣细胞周期蛋白控制。我们鉴定了不同 Symbiodiniaceae 物种中的 CDK 和细胞周期蛋白，并研究了它们与其他真核生物同源物的关系。在 Symbiodiniaceae 中发现了与真后生动物细胞周期相关的细胞周期蛋白 A、B、D、G/I 和 Y 以及转录细胞周期蛋白 L 相关的细胞周期蛋白，以及几种纤毛动物特异性细胞周期蛋白 A/B 蛋白，以及与原生动物 P/U 型细胞周期蛋白和顶复门细胞周期蛋白相关的蛋白。Symbiodiniaceae 细胞周期蛋白最大的扩张是在 P/U 型细胞周期蛋白组中。鉴定出与真后生动物细胞周期相关的 CDK（CDK1）相关蛋白以及转录相关的 CDK。然而，CDK 组最大的扩张是在纤毛动物特异性组中，其中包含 11 个不同的 CDK 组（CDKA-J），CDKB 是分布最广泛的 CDK 蛋白。由于其系统发育位置、Symbiodiniaceae 物种中的保守性以及典型 CDK 基序的存在，CDKB 成为 Symbiodiniaceae 中 Saccharomyces cerevisiae Cdc28/Pho85 样同源物的候选者。与细胞周期蛋白类似，在 Symbiodiniaceae 物种中发现的两个 CDK 组仅与顶复门分类群相关。比较自由生活和共生状态下 Breviolum minutum CDK 和细胞周期蛋白基因的表达表明，几种纤毛动物特异性 CDK 和两个 P/U 型细胞周期蛋白在宿主中表现出改变的表达，表明共生在分子水平上影响共生体的细胞周期。这些结果突出了 Symbiodiniaceae 细胞周期蛋白在物种间的差异。这些结果对宿主控制新型刺胞动物-甲藻共生体的共生体细胞周期具有重要意义。
