Table_3_Evolutionary Patterns of Thylakoid Architecture in Cyanobacteria.XLSX

While photosynthetic processes have become increasingly understood in cyanobacterial model strains, differences in the spatial distribution of thylakoid membranes among various lineages have been largely unexplored. Cyanobacterial cells exhibit an intriguing diversity in thylakoid arrangements, ranging from simple parietal to radial, coiled, parallel, and special types. Although metabolic background of their variability remains unknown, it has been suggested that thylakoid patterns are stable in certain phylogenetic clades. For decades, thylakoid arrangements have been used in cyanobacterial classification as one of the crucial characters for definition of taxa. The last comprehensive study addressing their evolutionary history in cyanobacteria was published 15 years ago. Since then both DNA sequence and electron microscopy data have grown rapidly. In the current study, we map ultrastructural data of >200 strains onto the SSU rRNA gene tree, and the resulting phylogeny is compared to a phylogenomic tree. Changes in thylakoid architecture in general follow the phylogeny of housekeeping loci. Parietal arrangement is resolved as the original thylakoid organization, evolving into complex arrangement in the most derived group of heterocytous cyanobacteria. Cyanobacteria occupying intermediate phylogenetic positions (greater filamentous, coccoid, and baeocytous types) exhibit fascicular, radial, and parallel arrangements, partly tracing the reconstructed course of phylogenetic branching. Contrary to previous studies, taxonomic value of thylakoid morphology seems very limited. Only special cases such as thylakoid absence or the parallel arrangement could be used as taxonomically informative apomorphies. The phylogenetic trees provide evidence of both paraphyly and reversion from more derived architectures in the simple parietal thylakoid pattern. Repeated convergent evolution is suggested for the radial and fascicular architectures. Moreover, thylakoid arrangement is constrained by cell size, excluding the occurrence of complex architectures in cyanobacteria smaller than 2 μm in width. It may further be dependent on unknown (eco)physiological factors as suggested by recurrence of the radial type in unrelated but morphologically similar cyanobacteria, and occurrence of special features throughout the phylogeny. No straightforward phylogenetic congruences have been found between proteins involved in photosynthesis and thylakoid formation, and the thylakoid patterns. Remarkably, several postulated thylakoid biogenesis factors are partly or completely missing in cyanobacteria, challenging their proposed essential roles.

尽管蓝细菌模式菌株的光合作用过程已得到愈发深入的阐释，但不同类群间类囊体膜的空间分布差异仍未得到充分探究。蓝细菌细胞的类囊体排布呈现出颇具趣味的多样性，从简单的周位排布，延伸至放射状、卷曲状、平行状及特殊类型。尽管这类排布差异的代谢背景仍未明确，但已有研究指出，类囊体模式在特定系统发育进化枝中具有稳定性。数十年来，类囊体排布一直是蓝细菌分类学中界定分类单元的关键特征之一。上一次针对蓝细菌类囊体排布进化历史的综合性研究发表于15年前。自彼时起，DNA序列与电子显微镜数据均实现了快速积累。本研究将超过200株蓝细菌的超微结构数据映射至小亚基核糖体RNA（SSU rRNA）基因树，并将由此构建的系统发育树与系统发育基因组树（phylogenomic tree）进行比对。总体而言，类囊体结构的变化与持家基因座（housekeeping loci）的系统发育轨迹相一致。周位排布被确定为原始的类囊体组织形式，并在最高级的异形胞蓝细菌类群中演化为复杂排布。处于系统发育中间位置的蓝细菌（大型丝状、球状及短囊孢子型类群）呈现出束状、放射状与平行状排布，其部分特征可追溯至已重建的系统发育分支进程。与既往研究结论相悖的是，类囊体形态的分类学价值似乎极为有限。仅类囊体缺失或平行排布等特殊情况，可作为具备分类学信息价值的衍征（apomorphies）使用。系统发育树的结果表明，类囊体排布既存在并系群（paraphyly）现象，也存在从高级结构逆转为简单周位类囊体模式的情况。放射状与束状结构的演化被认为经历了多次趋同进化。此外，类囊体排布受细胞大小限制，因此宽度小于2μm的蓝细菌不会出现复杂的类囊体结构。从非同源但形态相似的蓝细菌中反复出现放射状排布，以及各类群中普遍存在的特殊类囊体特征来看，类囊体排布可能还受未知的（生态）生理因素调控。尚未发现参与光合作用与类囊体形成的蛋白质，与类囊体模式之间存在明确的系统发育一致性。值得注意的是，蓝细菌中部分或完全缺失了若干被假定的类囊体生物发生因子，这对其被提出的必需功能提出了质疑。