Integrative Biology of Marine Models Laboratory, Sorbonne Université, CNRS, Station Biologique de Roscoff, Roscoff, France.
Génomique Métabolique, Institut François Jacob, CEA, CNRS, Université Evry, Université Paris-Saclay, Genoscope, Evry, 91057, France.
BMC Genomics. 2024 Oct 10;25(1):950. doi: 10.1186/s12864-024-10811-3.
Brown algae belong to the Stramenopiles phylum and are phylogenetically distant from plants and other multicellular organisms. This independent evolutionary history has shaped brown algae with numerous metabolic characteristics specific to this group, including the synthesis of peculiar polysaccharides contained in their extracellular matrix (ECM). Alginates and fucose-containing sulphated polysaccharides (FCSPs), the latter including fucans, are the main components of ECMs. However, the metabolic pathways of these polysaccharides remain poorly described due to a lack of genomic data.
An extensive genomic dataset has been recently released for brown algae and their close sister species, for which we previously performed an expert annotation of key genes involved in ECM-carbohydrate metabolisms. Here we provide a deeper analysis of this set of genes using comparative genomics, phylogenetics analyses, and protein modelling. Two key gene families involved in both the synthesis and degradation of alginate were suggested to have been acquired by the common ancestor of brown algae and their closest sister species Schizocladia ischiensis. Our analysis indicates that this assumption can be extended to additional metabolic steps, and thus to the whole alginate metabolic pathway. The pathway for the biosynthesis of fucans still remains biochemically unresolved and we also investigate putative fucosyltransferase genes that may harbour a fucan synthase activity in brown algae.
Our analysis is the first extensive survey of carbohydrate-related enzymes in brown algae, and provides a valuable resource for future research into the glycome and ECM of brown algae. The expansion of specific families related to alginate metabolism may have represented an important prerequisite for the evolution of developmental complexity in brown algae. Our analysis questions the possible occurrence of FCSPs outside brown algae, notably within their closest sister taxon and in other Stramenopiles such as diatoms. Filling this knowledge gap in the future will help determine the origin and evolutionary history of fucan synthesis in eukaryotes.
褐藻属于有孔虫门，在系统发育上与植物和其他多细胞生物相距甚远。这种独立的进化历史使褐藻具有许多特定于该类群的代谢特征，包括其细胞外基质 (ECM) 中所含的特殊多糖的合成。褐藻酸和含岩藻糖的硫酸化多糖 (FCSPs)，后者包括岩藻聚糖，是 ECM 的主要成分。然而，由于缺乏基因组数据，这些多糖的代谢途径仍描述不足。
最近为褐藻及其近亲物种发布了广泛的基因组数据集，我们之前对参与 ECM 碳水化合物代谢的关键基因进行了专家注释。在这里，我们使用比较基因组学、系统发育分析和蛋白质建模对这组基因进行了更深入的分析。两个涉及褐藻酸合成和降解的关键基因家族被认为是褐藻及其近亲物种 Schizocladia ischiensis 的共同祖先获得的。我们的分析表明，这种假设可以扩展到其他代谢步骤，从而扩展到整个褐藻酸代谢途径。岩藻聚糖生物合成途径在生化上仍未解决，我们还研究了褐藻中可能具有岩藻聚糖合酶活性的假定岩藻糖基转移酶基因。
我们的分析是对褐藻中碳水化合物相关酶的首次广泛调查，为未来研究褐藻的聚糖和 ECM 提供了有价值的资源。与褐藻酸代谢相关的特定家族的扩张可能代表了褐藻发育复杂性进化的重要前提。我们的分析对 FCSPs 可能不在褐藻中出现提出了质疑，尤其是在它们最亲近的分类群中和其他有孔虫门生物（如硅藻）中。未来填补这一知识空白将有助于确定真核生物中岩藻聚糖合成的起源和进化历史。
