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      Nitrogen hurdle of host alternation for a polyphagous aphid and the associated changes of endosymbionts

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          Abstract

          Low proportion of essential amino acids (EAAs) is one of the barriers for animals to use phloem as a diet. Endosymbionts with EAAs synthesis functions are considered crucial for ameliorating the lack of EAAs in insects’ diets. In this study, we transferred the insects from a cabbage-reared Myzus persicae population onto 3 new plant species including eggplant, tobacco and spinach. The performance on these plants was evaluated and the dynamics of endosymbionts in relation to this host alternation were recorded. We found that the EAAs ratio in phloem was largely determined by the concentrations of non-essential amino acids and the higher proportion of EAAs seemed to favor the population establishment on new plant species and the growth of primary endosymbionts inside insects, which indicated that nitrogen quality was an important factor for aphids to infest and spread on new plant hosts.

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          Most cited references27

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          Facultative bacterial symbionts in aphids confer resistance to parasitic wasps.

          Symbiotic relationships between animals and microorganisms are common in nature, yet the factors controlling the abundance and distributions of symbionts are mostly unknown. Aphids have an obligate association with the bacterium Buchnera aphidicola (the primary symbiont) that has been shown to contribute directly to aphid fitness. In addition, aphids sometimes harbor other vertically transmitted bacteria (secondary symbionts), for which few benefits of infection have been previously documented. We carried out experiments to determine the consequences of these facultative symbioses in Acyrthosiphon pisum (the pea aphid) for vulnerability of the aphid host to a hymenopteran parasitoid, Aphidius ervi, a major natural enemy in field populations. Our results show that, in a controlled genetic background, infection confers resistance to parasitoid attack by causing high mortality of developing parasitoid larvae. Compared with uninfected controls, experimentally infected aphids were as likely to be attacked by ovipositing parasitoids but less likely to support parasitoid development. This strong interaction between a symbiotic bacterium and a host natural enemy provides a mechanism for the persistence and spread of symbiotic bacteria.
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            Nutritional interactions in insect-microbial symbioses: aphids and their symbiotic bacteria Buchnera.

            A Douglas (1998)
            Most aphids possess intracellular bacteria of the genus Buchnera. The bacteria are transmitted vertically via the aphid ovary, and the association is obligate for both partners: Bacteria-free aphids grow poorly and produce few or no offspring, and Buchnera are both unknown apart from aphids and apparently unculturable. The symbiosis has a nutritional basis. Specifically, bacterial provisioning of essential amino acids has been demonstrated. Nitrogen recycling, however, is not quantitatively important to the nutrition of aphid species studied, and there is strong evidence against bacterial involvement in the lipid and sterol nutrition of aphids. Buchnera have been implicated in various non-nutritional functions. Of these, just one has strong experimental support: promotion of aphid transmission of circulative viruses. It is argued that strong parallels may exist between the nutritional interactions (including the underlying mechanisms) in the aphid-Buchnera association and other insect symbioses with intracellular microorganisms.
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              Independent origins and horizontal transfer of bacterial symbionts of aphids.

              Many insect groups have obligate associations with primary endosymbionts: mutualistic bacteria that are maternally transmitted and derived from an ancient infection. Often, the same insects are hosts to 'secondary' bacterial symbionts which are maternally transmitted but relatively labile within host lineages. To explore the dynamics of secondary symbiont associations in aphids, we characterized bacteria infecting 15 species of macrosiphine aphids using DNA sequencing, diagnostic polymerase chain reaction (PCR), diagnostic restriction digests, phylogenetic analyses, and electron microscopy to examine aphids from nature and from laboratory colonies. Three types of bacteria besides Buchnera were found repeatedly; all three fall within the Enterobacteriaceae. The R-type has a 16S rDNA less than 0.1% different from that of the secondary symbiont previously reported from Acyrthosiphon pisum and is related to Serratia species. The T-type includes a symbiont previously reported from a whitefly; the U-type comprises a new cluster near the T-type. The T-type was found in every one of 40 Uroleucon ambrosiae clones collected throughout the United States. In contrast, A. pisum individuals were infected by any combination of the three symbiont types. Secondary symbionts were maternally transmitted for 11 months within laboratory-reared A. pisum clones and were present in sexually produced eggs. PCR screens for a bacteriophage, APSE-1, indicated its presence in both A. pisum and U. ambrosiae containing secondary symbionts. Electron microscopy of R-type and T-type bacteria in A. pisum and in U. ambrosiae revealed rod-shaped organisms that attain extremely high densities within a few bacteriocytes.
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                Author and article information

                Journal
                Sci Rep
                Sci Rep
                Scientific Reports
                Nature Publishing Group
                2045-2322
                20 April 2016
                2016
                : 6
                : 24781
                Affiliations
                [1 ]State Key Laboratory of Crop Stress Biology for Arid Areas, and Key Laboratory of Integrated Pest Management on the Loess Plateau of Ministry of Agriculture, Northwest A&F University , Yangling, Shaanxi, 712100 China
                Author notes
                [*]

                These authors contributed equally to this work.

                Article
                srep24781
                10.1038/srep24781
                4837378
                27094934
                356117a4-9532-498f-8f78-84be59e7f108
                Copyright © 2016, Macmillan Publishers Limited

                This work is licensed under a Creative Commons Attribution 4.0 International License. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in the credit line; if the material is not included under the Creative Commons license, users will need to obtain permission from the license holder to reproduce the material. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/

                History
                : 28 July 2015
                : 31 March 2016
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