Bees are major pollinators involved in the maintenance of all terrestrial ecosystems. Biotic and abiotic factors placing these insects at risk is a research priority for ecological and agricultural sustainability. Parasites are one of the key players of this global decline and the study of their mechanisms of action is essential to control honeybee colony losses. Trypanosomatid parasites and particularly the Lotmaria passim are widely spread in honeybees, however their lifestyle is poorly understood. In this work, we show how these parasites are able to differentiate into a new parasitic lifestyle: the trypanosomatid biofilms. Using different microscopic techniques, we demonstrated that the secretion of Extracellular Polymeric Substances by free-swimming unicellular promastigote forms is a prerequisite for the generation and adherence of multicellular biofilms to solid surfaces in vitro and in vivo. Moreover, compared to human-infective trypanosomatid parasites our study shows how trypanosomatid parasites of honeybees increases their resistance and thus resilience to drastic changes in environmental conditions such as ultralow temperatures and hypoosmotic shock, which would explain their success thriving within or outside their hosts. These results set up the basis for the understanding of the success of this group of parasites in nature and to unveil the impact of such pathogens in honeybees, a keystones species in most terrestrial ecosystems.

蜜蜂是参与维持所有陆地生态系统的主要传粉者。使这些昆虫面临危险的生物和非生物因素是生态和农业可持续性的研究重点。寄生虫是导致全球蜜蜂数量下降的关键因素之一，研究其作用机制对于控制蜂群损失至关重要。锥虫寄生虫，特别是Lotmaria passim在蜜蜂中广泛传播，但人们对它们的生活方式知之甚少。在这项工作中，我们展示了这些寄生虫如何分化成一种新的寄生生活方式：锥虫生物膜。使用不同的显微技术，我们证明自由游动的单细胞前鞭毛体形式分泌的细胞外聚合物物质是体外和体内多细胞生物膜生成和粘附到固体表面的先决条件。此外，与人类感染性锥虫寄生虫相比，我们的研究表明，蜜蜂的锥虫寄生虫如何增强其抵抗力，从而增强对超低温和低渗休克等环境条件剧烈变化的恢复能力，这可以解释它们在宿主体内或宿主体外成功繁衍生息的原因。这些结果为了解自然界中这组寄生虫的成功奠定了基础，并揭示了此类病原体对蜜蜂（大多数陆地生态系统的关键物种）的影响。