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.

Transovarial Transmission of Bacteriome-Associated Symbionts in the Cicada Pycna repanda (Hemiptera: Cicadidae)

“…Additionally, Arsenopho-nus together with Hamiltonella contributed to the fitness of Aphis gossypii by enhancing its performance but not through parasitoid resistance (44). It has been shown that Arsenophonus infection increased A. gossypii requirements for the amino acid phenylalanine but decreased requirements for leucine (45). Our results revealed that Arsenophonus can coexist with "Ca.…”

Benefits and costs of hosting facultative symbionts in plant‐sucking insects: A meta‐analysis

“…We aim to provide a broad analysis of symbiont effects in plant‐sucking insects, yet we cannot escape that an important amount of the experimental work on symbiont effects has been performed on aphids, predominantly on the model pea aphid species. After more than two decades of research, experimental work directly measuring the costs and benefits of hosting symbionts in aphids is being replaced by work aiming to understand the ecological and evolutionary consequences of these interactions, and the mechanisms behind specific effects (Oliver & Higashi, 2019; Tian et al, 2019). For whitefly, most of the work is on a single species and its symbionts, with more recent focus on understanding mechanisms underlying these interactions (Santos‐Garcia et al, 2020; Wang, Ren, et al, 2020; Zchori‐Fein et al, 2014).…”

Insight into the bacterial communities of the subterranean aphid Anoecia corni

“…Bacteriophages required for protective symbiosis were found in various strains of the symbiont [ 99 ], but no defensive properties were found in Aphis glycines infected by Arsenophonus [ 98 ]. Recent studies suggest that Arsenophonus may be involved in host nutrition, probably by mediating host plant range [ 35 , 100 – 102 ]. In whiteflies, comparative genomics suggests that Arsenophonus is a source of B vitamins [ 82 ].…”

“…Arsenophonus sp. [ 8 , 9 ], Regiella insecticola [ 10 , 11 ], Serratia symbiotica [ 12 , 13 ], Hamiltonella defensa [ 14 , 15 ], Rickettsiella viridis [ 16 , 17 ] and Candidatus Fukatsuia symbiotica [ 18 , 19 ]], α-proteobacteria [e.g. the genus Rickettsia [ 20 , 21 ] and Wolbachia [ 22 , 23 ]] and Mollicutes of Spiroplasma genus [ 24 , 25 ].…”