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Spiroplasma affects host aphid proteomics feeding on two nutritional resources.

ABSTRACT: Bacterial symbionts are broadly distributed among insects, influencing their bioecology to different degrees. Aphids carry a number of secondary symbionts that can influence aphid physiology and fitness attributes. Spiroplasma is seldom reported as an aphid symbiont, but a high level of infection has been observed in one population of the tropical aphid Aphis citricidus. We used sister isolines of Spiroplasma-infected (Ac-BS) and Spiroplasma-free (Ac-B) aphids reared on sweet orange (optimum host) and orange jasmine (suboptimum host) to demonstrate the effects of Spiroplasma infection in the aphid proteome profile. A higher number of proteins were differently abundant in aphids feeding on orange jasmine, indicating an impact of host plant quality. In both host plants, the majority of proteins affected by Spiroplasma infection were heat shock proteins, proteins linked to cell function and structure, and energy metabolism. Spiroplasma also induced changes in proteins involved in antimicrobial activity, carbohydrate processing and metabolism, amino acid synthesis and metabolism in aphids feeding on orange jasmine. We discuss on how the aphid host proteome is differentially affected by Spiroplasma infection when the host is exploiting host plants with different nutritional values.

SUBMITTER: Guidolin AS

PROVIDER: S-EPMC5802742 | biostudies-literature | 2018 Feb

REPOSITORIES: biostudies-literature

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Spiroplasma affects host aphid proteomics feeding on two nutritional resources.

Guidolin Aline Sartori AS Cataldi Thaís Regiani TR Labate Carlos Alberto CA Francis Frederic F Cônsoli Fernando Luis FL

Scientific reports 20180206 1

Bacterial symbionts are broadly distributed among insects, influencing their bioecology to different degrees. Aphids carry a number of secondary symbionts that can influence aphid physiology and fitness attributes. Spiroplasma is seldom reported as an aphid symbiont, but a high level of infection has been observed in one population of the tropical aphid Aphis citricidus. We used sister isolines of Spiroplasma-infected (Ac-BS) and Spiroplasma-free (Ac-B) aphids reared on sweet orange (optimum hos ...[more]

PMID: 29410456

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Project description:Nutritional symbioses play a central role in the ability of insects to thrive on unbalanced diets and in ensuring their evolutionary success. A genomic model for nutritional symbiosis comprises the hemipteran Acyrthosiphon pisum, and the gamma-3-proteobacterium, Buchnera aphidicola, with genomes encoding highly integrated metabolic pathways. A. pisum feeds exclusively on plant phloem sap, a nutritionally unbalanced diet highly variable in composition, thus raising the question of how this symbiotic system responds to nutritional stress. We addressed this by combining transcriptomic, phenotypic and life history trait analyses to determine the organismal impact of deprivation of tyrosine and phenylalanine. These two aromatic amino acids are essential for aphid development, are synthesized in a metabolic pathway for which the aphid host and the endosymbiont are interdependent, and their concentration can be highly variable in plant phloem sap. We found that this nutritional challenge does not have major phenotypic effects on the pea aphid, except for a limited weight reduction and a 2-day delay in onset of nymph laying. Transcriptomic analyses through aphid development showed a prominent response in bacteriocytes (the core symbiotic tissue which houses the symbionts), but not in gut, thus highlighting the role of bacteriocytes as major modulators of this homeostasis. This response does not involve a direct regulation of tyrosine and phenylalanine biosynthetic pathway and transporter genes. Instead, we observed an extensive transcriptional reprogramming of the bacteriocyte with a rapid down-regulation of genes encoding sugar transporters and genes required for sugar metabolism. Consistently, we observed continued overexpression of the A. pisum homolog of RRAD, a small GTPase implicated in repressing aerobic glycolysis. In addition, we found increased transcription of genes involved in proliferation, cell size control and signaling. We experimentally confirmed the significance of these gene expression changes detecting an increase in bacteriocyte number and cell size in vivo under tyrosine and phenylalanine depletion. Our results support a central role of bacteriocytes in the aphid response to amino acid deprivation: their transcriptional and cellular responses fine-tune host physiology providing the host insect with an effective way to cope with the challenges posed by the variability in composition of phloem sap.

Project description:BackgroundA polyphagous insect herbivore has a wide range of host plants. However, it has been found that many polyphagous herbivores commonly exhibit a strong preference for a subset of species in their broad host range, and various host biotypes exist in herbivore populations. Nutrition and secondary metabolites in plants affect herbivore preference and performance, but it is still not clear which factors determine the host range and host preference of polyphagous herbivores.MethodCotton-melon aphids, Aphis gossypii Glover, collected from cotton and cucumber crops, were used in this study. The genetic backgrounds of these aphids were detected using microsatellite PCR and six genotypes were evaluated. Performance of these six aphid genotypes on excised leaves and plants of cotton and cucumber seedlings were examined through a reciprocal transplant experiment. In order to detect whether the feeding experience on artificial diet would alter aphid host range, the six genotypes of aphids fed on artificial diet for seven days were transferred onto cotton and cucumber leaves, and then their population growth on these two host plants was surveyed.ResultsAphids from cotton and cucumber plants could not colonize the excised leaves and intact plants of cucumber and cotton seedlings, respectively. All six genotypes of aphids collected from cotton and cucumber plants could survive and produce offspring on artificial diet, which lacked plant secondary metabolites. The feeding experience on the artificial diet did not alter the ability of all six genotypes to use their native host plants. However, after feeding on this artificial diet for seven days, two aphid genotypes from cotton and one from cucumber acquired the ability to use both of the excised leaves from cucumber and cotton plants. The two aphid genotypes from cotton conditioned by the feeding experience on artificial diet and then reared on excised cucumber leaves for >12 generations still maintained the ability to use intact cotton plants but did not establish a population on cucumber plants. However, one cucumber genotype conditioned by artificial diet and then reared on excised cotton leaves could use both the intact cotton and cucumber plants, showing that the expansion of host range was mediated by feeding experience.ConclusionFeeding experience on artificial diet induced the expansion of host range of the cucurbit-specialized A. gossypii, and this expansion was genotype-specific. We speculated that feeding on a constant set of host plants in the life cycle of aphids may contribute to the formation of host specialization.

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Spiroplasma affects host aphid proteomics feeding on two nutritional resources.

Publications

Spiroplasma affects host aphid proteomics feeding on two nutritional resources.

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