Comparative genomics support reduced-genome Paraburkholderia symbionts of Dictyostelium discoideum amoebas are ancestrally adapted professional symbionts

Abstract

The social amoeba Dictyostelium discoideum is a predatory soil protist frequently used for studying host-pathogen interactions. A subset of D. discoideum strains isolated from soil persistently carry symbiotic Paraburkholderia, recently formally described as P. agricolaris, P. bonniea, and P. hayleyella. The three facultative symbiont species of D. discoideum present a unique opportunity to study a naturally occurring symbiosis in a laboratory model protist. In addition, there is a large difference in genome size between P. agricolaris (8.7 million base pairs) vs. P. hayleyella and P. bonniea (4.1 Mbp) and in GC content (62% vs. 59%). We took a comparative genomics approach and compared the three genomes of D. discoideum-symbionts to 12 additional Paraburkholderia genomes to test for genome evolution patterns that frequently accompany host adaptation. Overall, P. agricolaris is difficult to distinguish from other Paraburkholderia based on its genome size and content, but the two reduced genomes of P. bonniea and P. hayleyella display characteristics that support evolution in a host environment. In addition, all three D. discoideum-symbiont genomes have increased secretion system and motility genes that may mediate interactions with their host. Specifically, adjacent BurBor-like type 3 and T6SS-5-like type 6 secretion system operons shared among all three D. discoideum-symbiont genomes may be important for host interaction. Ultimately, our combined evidence supports that the reduced-genome D. discoideum-symbionts have evolved to be professional symbionts ancestrally adapted to their protist hosts.