Metabolic exchange is one of the foundations of symbiotic associations between organisms and is a driving force in evolution. In the ocean, photosymbiosis between heterotrophic hosts and microalgae is powered by photosynthesis and relies on the transfer of organic carbon to the host (e.g. sugars). Yet, the identity of transferred carbohydrates as well as the molecular mechanisms that drive this exchange remain largely unknown, especially in unicellular photosymbioses that are widespread in the open ocean. Combining genomics, single-holobiont transcriptomics, and environmental metatranscriptomics, we revealed the transportome of the marine microalga Phaeocystis in symbiosis within acantharia, with a focus on sugar transporters. At the genomic level, the sugar transportome of Phaeocystis is comparable to non-symbiotic haptophytes. By contrast, we found significant remodeling of the expression of the transportome in symbiotic microalgae compared to the free-living stage. More particularly, 36% of sugar transporter genes were differentially expressed. Several of them, such as GLUTs, TPTs, and aquaporins, with glucose, triose-phosphate sugars, and glycerol as potential substrates, were upregulated at the holobiont and community level. We also showed that algal sugar transporter genes exhibit distinct temporal expression patterns during the day. This reprogrammed transportome indicates that symbiosis has a major impact on sugar fluxes within and outside the algal cell, and highlights the complexity and the dynamics of metabolic exchanges between partners. This study improves our understanding of the molecular players of the metabolic connectivity underlying the ecological success of planktonic photosymbiosis and paves the way for more studies on transporters across photosymbiotic models.

中文翻译：

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浮游生物宿主内共生微藻的运输组重塑


代谢交换是生物之间共生关系的基础之一，是进化的驱动力。在海洋中，异养宿主和微藻之间的光共生由光合作用提供动力，并依赖于有机碳（例如糖）向宿主的转移。然而，转移碳水化合物的身份以及驱动这种交换的分子机制在很大程度上仍然未知，尤其是在开阔海洋中广泛存在的单细胞光共生中。结合基因组学、单全息转录组学和环境元转录组学，我们揭示了海洋微藻 Phaeocystis 在棘皮内共生的运输组，重点是糖转运蛋白。在基因组水平上，Phaeocystis 的糖转运组与非共生触生体相当。相比之下，我们发现与自由生活阶段相比，共生微藻中运输组的表达发生了显着的重塑。更具体地说，36% 的糖转运蛋白基因是差异表达的。其中几种，如 GLUTs、TPT 和水通道蛋白，以葡萄糖、磷酸丙糖和甘油为潜在底物，在全息和群落水平上调。我们还表明，藻糖转运蛋白基因在白天表现出不同的时间表达模式。这种重编程的运输组表明共生对藻细胞内外的糖通量有重大影响，并突出了伙伴之间代谢交换的复杂性和动态。 这项研究提高了我们对浮游生物光共生生态成功背后的代谢连接的分子参与者的理解，并为跨光共生模型对转运蛋白的更多研究铺平了道路。