Third-party effects in theDictyostelium-Paraburkholderiasymbiosis: food bacteria that are eaten, carried, or left behind

AbstractSymbiotic 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.