Single cell transcriptomics of of Abedinium reveals a new early-branching dinoflagellate lineage

AbstractDinoflagellates possess many unique cellular characteristics with unresolved evolutionary histories including nuclei with greatly expanded genomes and chromatin packaged using histone-like proteins and dinoflagellate-viral nucleoproteins instead of histones, highly reduced mitochondrial genomes with extensive RNA editing, a mix of photosynthetic and cryptic secondary plastids, and tertiary plastids. Resolving the evolutionary origin of these traits requires understanding their ancestral states and early intermediates. Several deep-branching dinoflagellate lineages are good candidates for such reconstruction, however they tend to be delicate and environmentally sparse, so such analyses are not always simple. Here, we employ transcriptome sequencing from manually-isolated and microscopically documented cells to resolve the placement of two cells of one such genus, Abedinium, collected by ROV in deep waters off the coast of Monterey Bay. One cell corresponds to the only described species, A. dasypus, while the second cell is distinct and formally described as Abedinium folium, sp. nov. Abedinium has classically been assigned to the deep-branching dinoflagellates subgroup Noctilucea, which is weakly supported by phylogenetic analyses of the single characterized gene from any member of the genus, small subunit ribosomal RNA (SSU rRNA). However, a phylogenetic analysis based on 221 proteins from the transcriptome places Abedinium in a distinct lineage, separate from and basal to the Noctilucea and the rest of the core dinoflagellates. The transcriptome also contains evidence of a cryptic plastid functioning in the biosynthesis of isoprenoids, iron-sulfur clusters, and heme, a mitochondrial genome with all three expected protein-coding genes (cob, cox1, and cox3), and the presence of some but not all dinoflagellate-specific chromatin packaging proteins.

摘要：甲藻（Dinoflagellates）具备诸多独特的细胞特征，其演化历史迄今尚未厘清，其中包括基因组大幅扩张的细胞核、以类组蛋白与甲藻病毒核蛋白（dinoflagellate-viral nucleoproteins）而非组蛋白包装的染色质、伴随广泛RNA编辑的高度简化线粒体基因组、兼具光合与隐蔽次生质体的混合营养体系，以及三级质体。要解析这些性状的演化起源，需明确其祖先状态与早期过渡形式。若干深分支甲藻谱系是开展此类演化重建研究的优良候选类群，但这类生物通常较为脆弱且环境分布稀缺，因此相关分析往往并非易事。
本研究通过对经手动分离并经显微镜记录的细胞进行转录组测序，旨在明确在蒙特雷湾（Monterey Bay）近岸深海通过遥控水下机器人（Remotely Operated Vehicle，ROV）采集的Abedinium属两个细胞的系统发育定位。其中一个细胞对应该属唯一已描述物种A. dasypus，另一个细胞则为新种，正式命名为Abedinium folium, sp. nov.。
Abedinium传统上被归入深分支甲藻的夜光藻亚群（Noctilucea），但基于该属任意成员已表征的单个基因——小亚基核糖体RNA（small subunit ribosomal RNA，SSU rRNA）——的系统发育分析，其支持度较弱。然而，基于转录组221个蛋白质的系统发育分析显示，Abedinium隶属于一个独立谱系，与夜光藻亚群及核心甲藻其余类群相互分离，且位于二者的基部分支。
该转录组还带有如下证据：一个参与类异戊二烯、铁硫簇与血红素生物合成的隐蔽质体；一套包含全部三种预期蛋白编码基因（cob、cox1与cox3）的线粒体基因组；以及部分而非全部甲藻特异性染色质包装蛋白。