Context dependence in the symbiosis betweenDictyostelium discoideumandParaburkholderia

Abstract

Symbiotic interactions change with environmental context. Measuring these context‐dependent effects in hosts and symbionts is critical to determining the nature of symbiotic interactions. We investigated context dependence in the symbiosis between social amoeba hosts and their inedible Paraburkholderia bacterial symbionts, where the context is the abundance of host food bacteria. Paraburkholderia have been shown to harm hosts dispersed to food‐rich environments, but aid hosts dispersed to food‐poor environments by allowing hosts to carry food bacteria. Through measuring symbiont density and host spore production, we show that this food context matters in three other ways. First, it matters for symbionts, who suffer a greater cost from competition with food bacteria in the food‐rich context. Second, it matters for host‐symbiont conflict, changing how symbiont density negatively impacts host spore production. Third, data‐based simulations show that symbiosis often provides a long‐term fitness advantage for hosts after rounds of growth and dispersal in variable food contexts, especially when conditions are harsh with little food. These results show how food context can have many consequences for the Dictyostelium‐Paraburkholderia symbiosis and that both sides can frequently benefit.

Reduced and Nonreduced Genomes in Paraburkholderia Symbionts of Social Amoebas

“…The association between D. discoideum and its Paraburkholderia symbionts appears to be facultative, and these symbionts are able to simultaneously maintain a free-living and host-associated lifestyle ( 8 , 9 ). With Paraburkholderia the fitness outcomes to host and symbiont appear to be context dependent ( 12 ), as with most facultative host-microbe symbioses ( 6 ). D. discoideum amoeba hosts generally suffer negative fitness consequences of association.…”

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

“…discoideum and Paraburkholderia appears to involve elements of conflict and cooperation that are affected in multiple ways by food bacteria. show host clone replicates that were measured on two separate dates (see Figure 1A in Scott et al 2022). Points in B are independent, so we do not show clone identity.…”

“…P. hayleyella and P. bonniae also have reduced genomes relative to P. agricolaris and most other Paraburkholderia (Brock et al, 2020;Noh et al, 2022), which indicates that P. hayleyella and P. bonniea have been associated closely with their hosts during a long evolutionary history (McCutcheon & Moran, 2012). Fitness of D. discoideum hosts and Paraburkholderia symbionts is affected by interactions with a third set of organisms, the various food bacteria in the environment that are eaten by host amoebae (Brock et al, 2011;DiSalvo et al, 2015;Scott et al, 2022). Paraburkholderia symbionts are largely inedible by hosts, and are carried undigested inside the sorus along with additional edible bacteria (Brock et al, 2011;DiSalvo et al, 2015;Khojandi et al, 2019).…”

“…Paraburkholderia symbionts are largely inedible by hosts, and are carried undigested inside the sorus along with additional edible bacteria (Brock et al ., 2011; DiSalvo et al ., 2015; Khojandi et al ., 2019). When hosts disperse to food-poor environments where food bacteria are rare, hosts benefit from Paraburkholderia infection because hosts are able to carry food bacteria to seed new populations (Brock et al ., 2011; DiSalvo et al ., 2015; Scott et al ., 2022). When infected hosts disperse to food-rich environments, hosts pay a cost of producing fewer spores relative to uninfected D. discoideum (Brock et al ., 2011; DiSalvo et al ., 2015).…”

“…When infected hosts disperse to food-rich environments, hosts pay a cost of producing fewer spores relative to uninfected D. discoideum (Brock et al ., 2011; DiSalvo et al ., 2015). Presence of more Paraburkholderia is also associated with lower host spore production, but this effect depends on whether food bacteria are present (Scott et al ., 2022). Thus, host fitness depends on the abundance of food bacteria in the environment prior to fruiting body formation.…”