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

Abstract

Symbiotic interactions change depending on the abundance of third parties like predators, prey, or pathogens. Third-party interactions with food bacteria are central to the symbiosis betweenDictyostelium discoideumsocial amoeba hosts and inedibleParaburkholderiabacterial symbionts. Symbiosis withParaburkholderiaallows hostD. discoideumto carry food bacteria through the dispersal stage where host amoebae aggregate and develop into fruiting bodies that disperse spores. Carrying bacteria benefits hosts when food bacteria are scarce but harms hosts when food bacteria are plentiful. The nature of this cost is unknown, but hosts leave bacteria behind when they carry symbionts. If this left-behind bacteria includes uneaten food bacteria, infected hosts may lose potential growth. Thus, decisions about how many food bacteria to eat, to carry, and to leave behind are crucial for understanding both benefits and costs in this symbiosis. We investigated how many food bacteria are uneaten and carried in this symbiosis by measuring fluorescently labeled food bacteria after fruiting body development. We found thatParaburkholderiainfection makes hosts leave both symbionts and uneaten food bacteria but leaving food bacteria uneaten did not explain costs to hosts. Counts of food bacteria in fruiting bodies showed that hosts carry more food bacteria after developing in food-poor environments than in food-rich. This indicates that hosts, and possiblyParaburkholderiasymbionts, actively modify how many food bacteria are carried to ensure hosts have food in the harshest conditions. Decisions about how many third-party bacteria to eat, carry, or leave may thus have important effects on this symbiosis.

Symbiotic bacteria, immune-like sentinel cells, and the response to pathogens in a social amoeba

“…Paraburkholderia infection is known to cause numerous phenotypes in D. discoideum hosts, including conferring the ability to carry food bacteria (DiSalvo et al 2015;Brock, Jones, et al 2016) and a reduction in predation ability (Scott, Queller, and Strassmann 2022b). A prior study showed that D. discoideum clones naturally infected by Paraburkholderia had fewer sentinel cells than naturally uninfected D. discoideum clones (Brock, Callison, et al 2016).…”

“…The interaction between D. discoideum and these Paraburkholderia species has both positive and negative consequences for both participants, and is a rising model system in the study of the evolution of interspecific interactions (Scott, Queller, and Strassmann 2022a;Garcia et al 2019;Brock et al 2011;Brock et al 2013;DiSalvo et al 2015). A heretofore largely unexplored direction, however, is how infection by Paraburkholderia may modulate D. discoideum's interactions with other bacteria.…”

Unpredictable soil conditions can affect the prevalence of a microbial symbiosis

“…Carriage allows host amoebae to seed out populations of prey bacteria that hosts can then eat ( Brock et al, 2011 ). However, the ability to carry comes at the cost of reduced spore production when edible bacteria are common ( DiSalvo et al, 2015 ; Scott, Queller & Strassmann, 2022b ). The source of this fitness cost for hosts is unknown, though there is some evidence that Paraburkholderia itself harms hosts.…”

“…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 ).…”

Symbiotic bacteria, immune-like sentinel cells, and the response to pathogens in a social amoeba

“…Among this latter category are Paraburkholderia agricolaris, P. hayleyella and P. bonniea, which persistently infect D. discoideum cells as intracellular passengers [ 29 ]. Though in many respects Paraburkholderia acts as a pathogen, reducing the apparent fitness of its host, infection by Paraburkholderia imbues D. discoideum with the ability to carry prey bacteria with it throughout the social stages of its life cycle [ 30 – 32 ]. This bacterial carriage can enable D. discoideum to disperse to prey-impoverished environments not available to uninfected D. discoideum.…”