Mechanisms of association with amoeba hosts are shared by Paraburkholderia symbionts amid differential responses based on evolutionary history

Abstract

Dictyostelium discoideum is a soil dwelling amoeba that feeds on bacteria but can also host bacterial symbionts. Roughly one third of D. discoideum isolated from the wild were found to associate with facultative Paraburkholderia bacterial symbionts but the molecular mechanisms that enable symbiotic association are unknown. We explore gene expression during the initial association of novel hosts and three Paraburkholderia symbiont species using dual RNA-sequencing. We hypothesized that the magnitude and genomic distribution of differentially expressed genes may reflect the different evolutionary histories of reduced-genome symbionts P. bonniea or P. hayleyella vs. nonreduced-genome P. agricolaris. Hosts differentially expressed a smaller proportion of their genome in response to P. bonniea or P. hayleyella than to P. agricolaris. In addition, when the same host genes were differentially expressed in response to symbiotic association, the magnitude of the response was larger in response to P. agricolaris. Analysis of phagocytosis-related genes indicated that premature accumulation of post-lysosomal markers may enable Paraburkholderia survival. From the symbiont perspective, Paraburkholderia symbionts changed expression of similar proportions of their genomes when associated with D. discoideum. Upregulated host-association genes were overrepresented on the secondary chromid for P. agricolaris but evenly distributed across the chromosome and chromid for P. bonniea and P. hayleyella. Notably, all symbionts upregulated the shared type III and type VI secretion systems that we previously identified as candidate symbiosis genes. These results emphasize common elements of host-symbiont crosstalk between D. discoideum and three Paraburkholderia symbiont species, as well as distinctions due to different evolutionary histories.