Facultative symbiont virulence determines horizontal transmission rate without host specificity in Dictyostelium discoideum social amoebas

Abstract

In facultative symbioses, only a fraction of hosts are associated with symbionts. Specific host and symbiont pairings may be the result of host–symbiont coevolution driven by reciprocal selection or priority effects pertaining to which potential symbiont is associated with a host first. Distinguishing between these possibilities is important for understanding the evolutionary forces that affect facultative symbioses. We used the social amoeba, Dictyostelium discoideum, and its symbiont, Paraburkholderia bonniea, to determine whether ongoing coevolution affects which host–symbiont strain pairs naturally cooccur within a facultative symbiosis. Relative to other Paraburkholderia, including another symbiont of D. discoideum, P. bonniea features a reduced genome size that indicates a significant history of coevolution with its host. We hypothesized that ongoing host–symbiont coevolution would lead to higher fitness for naturally cooccurring (native) host and symbiont pairings compared to novel pairings. We show for the first time that P. bonniea symbionts can horizontally transmit to new amoeba hosts when hosts aggregate together during the social stage of their life cycle. Here we find evidence for a virulence–transmission trade-off without host specificity. Although symbiont strains were significantly variable in virulence and horizontal transmission rate, hosts and symbionts responded similarly to associations in native and novel pairings. We go on to identify candidate virulence factors in the genomes of P. bonniea strains that may contribute to variation in virulence. We conclude that ongoing coevolution is unlikely for D. discoideum and P. bonniea. The system instead appears to represent a stable facultative symbiosis in which naturally cooccurring P. bonniea host and symbiont pairings are the result of priority effects.

Complex third-party effects in theDictyostelium–Paraburkholderiasymbiosis: prey bacteria that are eaten, carried or left behind

“…This correlation could result from higher Paraburkholderia densities interfering with the ability of hosts to eat prey bacteria. Additional support for Paraburkholderia symbiont densities lowering host fitness comes from a recent study on P. bonniae [63].…”

Unpredictable soil conditions can affect the prevalence of a microbial symbiosis

“…The first symbionts to be discovered were three species of facultatively endosymbiotic Paraburkholderia bacteria ( Brock et al, 2011 ; DiSalvo et al, 2015 ). The life histories of these Paraburkholderia bacteria in their natural soil habitats are unknown, but they can be cultured outside of their hosts in the lab ( DiSalvo et al, 2015 ; Brock et al, 2020 ) and one species has been shown to be horizontally transferred in the lab ( Noh et al, 2024 ). Two of these Paraburkholderia species, P. hayleyella and P. bonniea , may have a longer history of host association as shown by their reduced genomes, while P. agricolaris may be a newer symbiont ( Noh et al, 2022 ).…”

“…The source of this fitness cost for hosts is unknown, though there is some evidence that Paraburkholderia itself harms hosts. For example, the density of Paraburkholderia tends to be associated with lower host spore production ( Scott, Queller & Strassmann, 2022a , 2022b ; Noh et al, 2024 ) and Paraburkholderia infection interferes with host immune cells that develop during the multicellular stage ( Scott et al, 2023a ).…”