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Bacteriocyte-associated gammaproteobacterial symbionts of the Adelges nordmannianae/piceae complex (Hemiptera: Adelgidae).

ABSTRACT: Adelgids (Insecta: Hemiptera: Adelgidae) are known as severe pests of various conifers in North America, Canada, Europe and Asia. Here, we present the first molecular identification of bacteriocyte-associated symbionts in these plant sap-sucking insects. Three geographically distant populations of members of the Adelges nordmannianae/piceae complex, identified based on coI and ef1alpha gene sequences, were investigated. Electron and light microscopy revealed two morphologically different endosymbionts, coccoid or polymorphic, which are located in distinct bacteriocytes. Phylogenetic analyses of their 16S and 23S rRNA gene sequences assigned both symbionts to novel lineages within the Gammaproteobacteria sharing <92% 16S rRNA sequence similarity with each other and showing no close relationship with known symbionts of insects. Their identity and intracellular location were confirmed by fluorescence in situ hybridization, and the names 'Candidatus Steffania adelgidicola' and 'Candidatus Ecksteinia adelgidicola' are proposed for tentative classification. Both symbionts were present in all individuals of all investigated populations and in different adelgid life stages including eggs, suggesting vertical transmission from mother to offspring. An 85 kb genome fragment of 'Candidatus S. adelgidicola' was reconstructed based on a metagenomic library created from purified symbionts. Genomic features including the frequency of pseudogenes, the average length of intergenic regions and the presence of several genes which are absent in other long-term obligate symbionts, suggested that 'Candidatus S. adelgidicola' is an evolutionarily young bacteriocyte-associated symbiont, which has been acquired after diversification of adelgids from their aphid sister group.

SUBMITTER: Toenshoff ER

PROVIDER: S-EPMC3260495 | biostudies-literature | 2012 Feb

REPOSITORIES: biostudies-literature

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Bacteriocyte-associated gammaproteobacterial symbionts of the Adelges nordmannianae/piceae complex (Hemiptera: Adelgidae).

Toenshoff Elena R ER Penz Thomas T Narzt Thomas T Collingro Astrid A Schmitz-Esser Stephan S Pfeiffer Stefan S Klepal Waltraud W Wagner Michael M Weinmaier Thomas T Rattei Thomas T Horn Matthias M

The ISME journal 20110811 2

Adelgids (Insecta: Hemiptera: Adelgidae) are known as severe pests of various conifers in North America, Canada, Europe and Asia. Here, we present the first molecular identification of bacteriocyte-associated symbionts in these plant sap-sucking insects. Three geographically distant populations of members of the Adelges nordmannianae/piceae complex, identified based on coI and ef1alpha gene sequences, were investigated. Electron and light microscopy revealed two morphologically different endosym ...[more]

PMID: 21833037

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Project description:Adelgidae are a sister group of Aphididae and Phylloxeridae within Hemiptera, Aphidoidea and occur exclusively on Pinaceae. The piercing-sucking mouthparts of Adelgidae are similar to those of aphids and it is believed that adelgids ingest sap from both the non-vascular and vascular (phloem) tissues. The aim of the present study was to identify and characterize the adelgid stylet activities during their penetration in plant tissues. The probing behavior of Adelges laricis Vallot (Hemiptera: Adelgidae) on European larch Larix decidua Mill. and sucrose diets was monitored using the DC-EPG (Electrical Penetration Graph technique = electropenetrography). The EPG waveforms were described based on amplitude, frequency, voltage level, and electrical origin of the observed traces, and associated with putative behavioral activities based on analogy with aphid activities. Waveform frequency, duration, and sequence were analysed as well. A. laricis generated EPG signals at two clearly distinct voltage levels positive and negative, suggesting extracellular and intracellular stylet penetration, respectively. The adelgid EPG patterns were ascribed to four behavioral phases, which were non-probing, pathway, phloem, and xylem phases. Non-probing referred to the position of the stylets outside the plant tissues. Pathway phase was represented by three waveform patterns that visualized extracellular stylet penetration in non-vascular tissues without potential drops (AC1), with serial short (1.2-1.5 s) potential drops (AC2), and with 'aphid-like' (5-10 s) potential drops (AC3). Phloem phase comprised three waveform patterns at intracellular level, which in all probability represented phloem salivation (AE1), and phloem sap passive (AE2) and active ingestion (AE3). AE3 was a newly described waveform, previously unreported from Hemiptera. Waveform AG represented the ingestion of xylem sap. The comparative analysis demonstrated that the gymnosperm-associated adelgids show certain similarities in probing behavior typical of aphids and phylloxerids on angiosperm plants. The present work is the first detailed analysis of specific adelgid stylet activities on gymnosperms.

Project description:Sap-sucking insects typically engage in obligate relationships with symbiotic bacteria that play nutritional roles in synthesizing nutrients unavailable or in scarce supply from the plant-sap diets of their hosts. Adelgids are sap-sucking insects with complex life cycles that involve alternation between conifer tree species. While all adelgid species feed on spruce during the sexual phase of their life cycle, each adelgid species belongs to a major lineage that feeds on a distinct genus of conifers as their alternate host. Previous work on adelgid symbionts had discovered pairs of symbionts within each host species, and unusual diversity across the insect family, but left several open questions regarding the status of bacterial associates. Here, we explored the consistency of symbionts within and across adelgid lineages, and sought evidence for facultative vs. obligate symbiont status. Representative species were surveyed for symbionts using 16S ribosomal DNA gene sequencing, confirming that different symbiont pairs were consistently present within each major adelgid lineage. Several approaches were used to establish whether symbionts exhibited characteristics of long-term, obligate mutualists. Patterns of symbiont presence across adelgid species and diversification with host insects suggested obligate relationships. Fluorescent in situ hybridization and electron microscopy localized symbionts to bacteriocyte cells within the bacteriome of each species (with one previously known exception), and detection of symbionts in eggs indicated their vertical transmission. Common characteristics of long-term obligate symbionts, such as nucleotide compositional bias and pleomorphic symbiont cell shape were also observed. Superimposing microbial symbionts on the adelgid phylogeny revealed a dynamic pattern of symbiont gains and losses over a relatively short period of time compared to other symbionts associated with sap-sucking insects, with each adelgid species possessing an older, "senior" symbiont and a younger "junior" symbiont. A hypothesis relating adelgid life cycles to relaxed constraints on symbionts is proposed, with the degradation of senior symbionts and repeated acquisition of more junior symbionts creating opportunities for repeated colonization of new alternate-conifer hosts by adelgids.

Dataset Information

Bacteriocyte-associated gammaproteobacterial symbionts of the Adelges nordmannianae/piceae complex (Hemiptera: Adelgidae).

Publications

Bacteriocyte-associated gammaproteobacterial symbionts of the Adelges nordmannianae/piceae complex (Hemiptera: Adelgidae).

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