Genetic polymorphism and endosymbiont infection are ubiquitous in aphid populations. It has been known that the obligate symbiont Buchnera provides aphids with essential amino acids which cannot be ingested from plant sap. Buchnera often coexists with facultative endosymbionts in aphids. However, it is unclear whether the facultative endosymbionts affect the aphid’s amino acid requirements from diet. In this study, we found that the facultative endosymbiont status in populations of the cotton-melon aphid Aphis gossypii was associated with aphid genotype or host plant. The infection frequency of Arsenophonus in aphids living on cotton was significantly higher than that in aphids on cucumber, and cucumber leaves contained higher titers of free amino acids than cotton leaves, especially amino acids Leu, Arg, Ile, Val, and Phe. The net reproductive rates of five aphid genotypes infected with Arsenophonus were not different on the complete-amino-acid diet, but the values were significantly different among seven Arsenophonus-free aphid genotypes. Moreover, the net reproductive rates of aphids on the amino-acid-deficient diet were significantly affected by Arsenophonus infection and aphid genotype. Arsenophonus infection decreased aphid performance on the Phe-free diet but improved performance on the Leu-free diet and did not affect the performance on the Ile-free or Val-free diet. Arsenophonus infections altered aphid requirements for amino acids that were significantly different in cotton and cucumber leaves, suggesting this endosymbiont would modulate the host specialization of this aphid. IMPORTANCE The facultative endosymbiont Arsenophonus plays an important role in regulating reproduction through son killing, enemy resistance, and the dietary breadth of its insect hosts. In this study, we found Arsenophonus could alter aphid performance on the amino-acid-deficient diets. Arsenophonus infection increased aphid requirements for the amino acid Phe, but decreased requirements for the Leu. Cotton and cucumber leaves contained drastically different titers of free amino acids Phe and Leu, and aphids living on these two plants were infected with different incidences of Arsenophonus. We hypothesize that host specialization or the host plant range of aphids may be mediated by Arsenophonus.

Summary Transmission rate and role in hosts contribute to the prevalence of an endosymbiont. However, factors affecting transmission and role of facultative endosymbionts are still not well understood. Here, we illustrated that host plants and environmental temperatures affected the transmission, relative abundance and role of Arsenophonus in the cotton aphid Aphis gossypii. The transmission rate of this endosymbiont from mother aphids to offspring was relatively lower. High temperatures impeded the transmission, and infection rates declined as aphids were exposed to 30°C. Contents of amino acids and secondary metabolites were remarkably different among host plants. Aphids feeding on zucchini leaves containing a higher titre of amino acids and lower secondary metabolites harboured a relatively lower abundance of Arsenophonus. Concentrations of an amino acid and a plant secondary metabolite, cucurbitacin B, in aphid diet were not associated with Arsenophonus abundance. However, gossypol, another plant secondary metabolite, was strongly related with the abundance. Arsenophonus imparted a fitness benefit to aphids, and the benefit was dependent on host plants and gossypol concentration. In sum, plant secondary metabolite and environmental temperature affect transmission, relative abundance and role of Arsenophonus, which determine the endosymbiont prevalence in aphid populations.

The obligate symbiont Buchnera can synthesize amino acids for aphids. In this study, we found that a facultative symbiont, Arsenophonus , can help improve aphids’ growth performance under amino acid deficiency stress by changing the relative abundance of Buchnera and the expression levels of amino acid synthase genes. This study highlights the interaction between Arsenophonus and Buchnera to ameliorate aphid growth under amino acid stress.