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      Microorganisms from aphid honeydew attract and enhance the efficacy of natural enemies

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          Abstract

          Aphids are one of the most serious pests of crops worldwide, causing major yield and economic losses. To control aphids, natural enemies could be an option but their efficacy is sometimes limited by their dispersal in natural environment. Here we report the first isolation of a bacterium from the pea aphid Acyrthosiphon pisum honeydew, Staphylococcus sciuri, which acts as a kairomone enhancing the efficiency of aphid natural enemies. Our findings represent the first case of a host-associated bacterium driving prey location and ovipositional preference for the natural enemy. We show that this bacterium has a key role in tritrophic interactions because it is the direct source of volatiles used to locate prey. Some specific semiochemicals produced by S. sciuri were also identified as significant attractants and ovipositional stimulants. The use of this host-associated bacterium could certainly provide a novel approach to control aphids in field and greenhouse systems.

          Abstract

          In this study, a bacterium is identified in the honeydew of aphids, which produces volatile chemicals and attracts hoverflies. The findings could aid the development of pest control systems for aphids.

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          Most cited references11

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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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            Aphid and Plant Volatiles Induce Oviposition in an Aphidophagous Hoverfly

            Episyrphus balteatus DeGeer (Diptera, Syrphidae) is an abundant and efficient aphid-specific predator. We tested the electroantennographic (EAG) response of this syrphid fly to the common aphid alarm pheromone, (E)-β-farnesene (EβF), and to several plant volatiles, including terpenoids (mono- and sesquiterpenes) and green leaf volatiles (C6 and C9 alcohols and aldehydes). Monoterpenes evoked significant EAG responses, whereas sesquiterpenes were inactive, except for the aphid alarm pheromone (EβF). The most pronounced antennal responses were elicited by six and nine carbon green leaf alcohols and aldehydes [i.e., (Z)-3-hexenol, (E)-2-hexenol, (E)-2-hexenal, and hexanal]. To investigate the behavioral activity of some of these EAG-active compounds, E. balteatus females were exposed to R-(+)-limonene (monoterpene), (Z)-3-hexenol (green leaf alcohol), and EβF (sesquiterpene, common aphid alarm pheromone). A single E. balteatus gravid female was exposed for 10 min to an aphid-free Vicia faba plant that was co-located with a semiochemical dispenser. Without additional semiochemical, hoverfly females were not attracted to this plant, and no oviposition was observed. The monoterpene R-(+)-limonene did not affect the females’ foraging behavior, whereas (Z)-3-hexenol and EβF increased the time of flight and acceptance of the host plant. Moreover, these two chemicals induced oviposition on aphid-free plants, suggesting that selection of the oviposition site by predatory hoverflies relies on the perception of a volatile blend composed of prey pheromone and typical plant green leaf volatiles.
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              On-line monitoring of microbial volatile metabolites by proton transfer reaction-mass spectrometry.

              A method for analysis of volatile organic compounds (VOCs) from microbial cultures was established using proton transfer reaction-mass spectrometry (PTR-MS). A newly developed sampling system was coupled to a PTR-MS instrument to allow on-line monitoring of VOCs in the dynamic headspaces of microbial cultures. The novel PTR-MS method was evaluated for four reference organisms: Escherichia coli, Shigella flexneri, Salmonella enterica, and Candida tropicalis. Headspace VOCs in sampling bottles containing actively growing cultures and uninoculated culture medium controls were sequentially analyzed by PTR-MS. Characteristic marker ions were found for certain microbial cultures: C. tropicalis could be identified by several unique markers compared with the other three organisms, and E. coli and S. enterica were distinguishable from each other and from S. flexneri by specific marker ions, demonstrating the potential of this method to differentiate between even closely related microorganisms. Although the temporal profiles of some VOCs were similar to the growth dynamics of the microbial cultures, most VOCs showed a different temporal profile, characterized by constant or decreasing VOC levels or by single or multiple peaks over 24 h of incubation. These findings strongly indicate that the temporal evolution of VOC emissions during growth must be considered if characterization or differentiation based on microbial VOC emissions is attempted. Our study may help to establish the analysis of VOCs by on-line PTR-MS as a routine method in microbiology and as a tool for monitoring environmental and biotechnological processes.
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                Author and article information

                Journal
                Nat Commun
                Nature Communications
                Nature Publishing Group
                2041-1723
                June 2011
                14 June 2011
                : 2
                : 348
                Affiliations
                [1 ]simpleDepartment of Functional and Evolutionary Entomology, University of Liege, Gembloux Agro-Bio Tech, Passage des Déportés 2 , 5030 Gembloux, Belgium.
                [2 ]simpleWalloon Center of Industrial Biology, University of Liege , B40, 4000 Sart-Tilman, Belgium.
                [3 ]simpleDepartment of Analytical Chemistry, University of Liege, Gembloux Agro-Bio Tech, Passage des Déportés 2 , 5030 Gembloux, Belgium.
                [4 ]simpleDepartment of Applied Statistics, Computer Science and Mathematics, University of Liege, Gembloux Agro-Bio Tech, Avenue de la Faculté 8 , 5030 Gembloux, Belgium.
                [5 ]simpleDepartment of Entomology, Penn State University , University Park, Pennsylvania 16802, USA.
                Author notes
                Article
                ncomms1347
                10.1038/ncomms1347
                3156822
                21673669
                515e649f-efa5-4cf0-8d72-7e2b37886eb0
                Copyright © 2011, Nature Publishing Group, a division of Macmillan Publishers Limited. All Rights Reserved.

                This work is licensed under a Creative Commons Attribution-NonCommercial-No Derivative Works 3.0 Unported License. To view a copy of this license, visit http://creativecommons.org/licenses/by-nc-nd/3.0/

                History
                : 30 November 2010
                : 11 May 2011
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