Infections with Arsenophonus Facultative Endosymbionts Alter Performance of Aphids (Aphis gossypii) on an Amino-Acid-Deficient Diet

Abstract

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.

Keywords: Aphis gossypii; Arsenophonus; amino acid; genotype; host specialization; net reproductive rate.

FIG 1

Infection frequency (%) of facultative endosymbionts in aphids collected from cotton and cucumber.

FIG 2

Titer of 15 free amino acids in cotton and cucumber leaves. * and ** indicate significant differences between cotton and cucumber using the t test followed by the Bonferroni correction at P = 0.05/15 and P = 0.01/15, respectively. ns, no significant differences at P > 0.05/15.

FIG 3

Net reproductive rates (R₀s) of 12 genotypes aphids (five Arsenophonus infected [Ars⁺], and seven Arsenophonus free [Ars⁻]) on the complete amino acid diet when they were treated or not treated with antibiotics. * and ** indicate significant differences in the net reproductive rates of a genotype between antibiotic treatment and no treatment at P = 0.05 and P = 0.01, respectively. ns, no significant differences.

FIG 4

Relative density of Buchnera in Arsenophonus-infected (Ars⁺) and Arsenophonus-cured (Ars⁻) aphids. * indicates significant difference between infect and cured lineages at P = 0.05. ns, no significant differences.

FIG 5

The net reproductive rates (R₀s) of five aphid genotypes on the complete-amino-acid diet (A) or Leu-free (B), Arg-free (C), Ile-free (D), Val-free (E), and Phe-free (F) diets before (Ars⁺) and after (Ars⁻) antibiotic treatment. * and ** indicate significant differences between antibiotic treatment and no treatment at P = 0.05 and P = 0.01, respectively. ns, no significant differences.

FIG 6

A mode of the facultative endosymbiont-mediated host specialization in aphids.