Symbiont-Induced Phagosome Changes Rather than Extracellular Discrimination Contribute to the Formation of Social Amoeba Farming Symbiosis

Abstract

ABSTRACT Symbiont recognition is essential in many symbiotic relationships, especially for horizontally transferred symbionts. Therefore, how to find the right partner is a crucial challenge in these symbiotic relationships. Previous studies have demonstrated that both animals and plants have evolved various mechanisms to recognize their symbionts. However, studies about the mechanistic basis of establishing protist-bacterium symbioses are scarce. This study investigated this question using a social amoeba Dictyostelium discoideum and their Burkholderia symbionts. We found no evidence that D. discoideum hosts could distinguish different Burkholderia extracellularly in chemotaxis assays. Instead, symbiont-induced phagosome biogenesis contributed to the formation of social amoeba symbiosis, and D. discoideum hosts have a higher phagosome pH when carrying symbiotic Burkholderia than nonsymbiotic Burkholderia. In conclusion, the establishment of social amoeba symbiosis is not linked with extracellular discrimination but related to symbiont-induced phagosome biogenesis, which provides new insights into the mechanisms of endosymbiosis formation between protists and their symbionts. IMPORTANCE Protists are single-celled, extremely diverse eukaryotic microbes. Like animals and plants, they live with bacterial symbionts and have complex relationships. In protist-bacterium symbiosis, while some symbionts are strictly vertically transmitted, others need to reestablish and acquire symbionts from the environment frequently. However, the mechanistic basis of establishing protist-bacterium symbioses is mostly unclear. This study uses a novel amoeba-symbiont system to show that the establishment of this symbiosis is not linked with extracellular discrimination. Instead, symbiont-induced phagosome biogenesis contributes to the formation of social amoeba-bacterium symbiosis. This study increases our understanding of the mechanistic basis of establishing protist-bacterium symbioses.

Keywords

• symbiosis
• chemotaxis
• phagosome
• discrimination
• Dictyostelium discoideum
• Burkholderia