A Trojan horse pathogen breaking through partner-choice barriers in the insect gut

Mutualistic symbioses are potentially vulnerable to exploitation, particularly in hosts that acquire symbionts from the environment, where harmful exploiters inhabit. The independent evolution and persistence of intricate partner-choice mechanisms in many symbioses testify the threat by specialized exploiters of mutualisms, although only few have been documented in nature. We report here a lethal “Trojan horse” pathogen, Burkholderia sp. SJ1, exploiting the stinkbug– Caballeronia gut symbiosis. This bacterium resembles symbionts by using wrapping motility to traverse the host’s sorting organ, inducing symbiotic organ morphogenesis and colonizing it. Unlike mutualists, however, it resists host digestion for nutrient acquisition, breaches the gut epithelium, and causes sepsis, rapidly killing the host. Colonization of the symbiotic organ is essential for its lethality. This case shows how pathogens can exploit mutualisms, highlighting the evolutionary pressures shaping partner-choice mechanisms and the fragility of even highly specialized mutualisms.