A dual insect symbiont and plant pathogen improves insect host fitness under arginine limitation.

Some facultative bacterial symbionts are known to benefit insects, but nutritional advantages are rare among these non-obligate symbionts. Here, we demonstrate that the facultative symbiont Candidatus Liberibacter psyllaurous enhances the fitness of its psyllid insect host, Bactericera cockerelli, by providing nutritional benefits. L. psyllaurous, an unculturable pathogen of solanaceous crops, also establishes a close relationship with its insect vector, B. cockerelli, increasing in titer during insect development, vertically transmitting through eggs, and colonizing various tissues, including the bacteriome, which houses the obligate nutritional symbiont, Carsonella. Carsonella supplies essential amino acids to its insect host but has gaps in some of its essential amino acid pathways that the psyllid complements with its own genes, many of which have been acquired through horizontal gene transfer (HGT) from bacteria. Our findings reveal that L. psyllaurous increases psyllid fitness on plants by reducing developmental time and increasing adult weight. In addition, through metagenomic sequencing, we reveal that L. psyllaurous maintains complete pathways for synthesizing the essential amino acids arginine, lysine, and threonine, unlike the psyllid's other resident microbiota, Carsonella, and two co-occurring Wolbachia strains. RNA sequencing reveals the downregulation of a HGT collaborative psyllid gene (ASL), which indicates a reduced demand for arginine supplied by Carsonella when the psyllid is infected with L. psyllaurous. Notably, artificial diet assays show that L. psyllaurous enhances psyllid fitness on an arginine-deplete diet. These results corroborate the role of L. psyllaurous as a beneficial insect symbiont, contributing to the nutrition of its insect host.IMPORTANCEUnlike obligate symbionts that are permanently associated with their hosts, facultative symbionts rarely show direct nutritional contributions, especially under nutrient-limited conditions. This study demonstrates, for the first time, that Candidatus Liberibacter psyllaurous, a facultative symbiont and a plant pathogen, enhances the fitness of its Bactericera cockerelli host by supplying an essential nutrient arginine that is lacking in the plant sap diet. Our findings reveal how facultative symbionts can play a vital role in helping their insect hosts adapt to nutrient-limited environments. This work provides new insights into the dynamic interactions between insect hosts, their symbiotic microbes, and their shared ecological niches, broadening our understanding of symbiosis and its role in shaping adaptation and survival.