The specificity of Burkholderia symbionts in the social amoeba farming symbiosis: prevalence, species, genetic and phenotypic diversity

The establishment of symbioses between eukaryotic hosts and bacterial symbionts in nature is a dynamic process. The formation of such relationships depends on the life history of both partners. Bacterial symbionts of amoebae may have unique evolutionary trajectories to the symbiont lifestyle, because bacteria are typically ingested as prey. To persist after being eaten, bacteria must survive phagocytosis. In the social amoeba Dictyostelium discoideum, certain strains of Burkholderia bacteria are able to resist amoebal digestion and maintain a persistent relationship that includes carriage throughout the amoeba’s social cycle that culminates in spore formation. Some Burkholderia strains allow their host to carry other bacteria as food. This carried food is released in new environments in a trait called farming. To better understand the diversity and prevalence of Burkholderia symbionts and the traits they impart to their amoebae hosts, we first screened 700 natural isolates of D. discoideum and found 25% infected with Burkholderia. We next used a multilocus phylogenetic analysis and identified two independent transitions by Burkholderia to the symbiotic lifestyle. Finally, we tested the ability of 38 strains of Burkholderia, from D. discoideum and as well as strains isolated from other sources, for traits relevant to symbiosis in D. discoideum. Only D. discoideum native isolates belonging to the B. agricolaris, B. hayleyella, and B.bonniea species were able to form a persistent symbiotic association with D. discoideum. The Burkholderia Dictyostelium relationship provides a promising arena for further studies of the pathway to symbiosis in a unique system.

自然界中，真核宿主与细菌共生体之间的共生关系构建是一个动态过程。此类共生关系的形成取决于双方的生活史特征。变形虫的细菌共生体在走向共生生活方式的过程中，可能具备独特的演化路径，因为细菌通常是以猎物的形式被宿主摄入的。为了在被吞噬后仍能存活，细菌必须能够抵御吞噬作用（phagocytosis）。在社会性变形虫盘基网柄菌（Dictyostelium discoideum）中，伯克霍尔德氏菌（Burkholderia）的部分菌株可抵御变形虫的消化，并与之建立持久的共生关系：这类共生关系伴随变形虫的整个社交周期，直至孢子形成阶段达到顶点。部分伯克霍尔德氏菌菌株可帮助宿主携带其他细菌作为食物储备，这类被携带的食物会在宿主迁移至新环境时被释放，该特性被称为“农耕”。为了更全面地解析伯克霍尔德氏菌共生体的多样性与流行率，以及它们赋予变形虫宿主的相关特性，本研究首先对700株盘基网柄菌的自然分离株进行了筛选，发现其中25%的菌株携带有伯克霍尔德氏菌。随后，本研究采用多基因座系统发育分析（multilocus phylogenetic analysis），鉴定出伯克霍尔德氏菌向共生生活方式独立演化的两次事件。最后，本研究针对38株伯克霍尔德氏菌菌株（分别分离自盘基网柄菌及其他来源），测试了它们在盘基网柄菌共生相关特性方面的表现。仅源自盘基网柄菌的、隶属于农业伯克霍尔德氏菌（B. agricolaris）、海利伯克霍尔德氏菌（B. hayleyella）以及邦妮伯克霍尔德氏菌（B. bonniea）的本土分离株，能够与盘基网柄菌建立持久的共生关联。伯克霍尔德氏菌与盘基网柄菌的共生关系，为在这一独特系统中探究共生演化路径提供了极具前景的研究平台。