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Wild Apple-Associated Fungi and Bacteria Compete to Colonize the Larval Gut of an Invasive Wood-Borer Agrilus mali in Tianshan Forests

ABSTRACT: The gut microflora of insects plays important roles throughout their lives. Different foods and geographic locations change gut bacterial communities. The invasive wood-borer Agrilus mali causes extensive mortality of wild apple, Malus sieversii, which is considered a progenitor of all cultivated apples, in Tianshan forests. Recent analysis showed that the gut microbiota of larvae collected from Tianshan forests showed rich bacterial diversity but the absence of fungal species. In this study, we explored the antagonistic ability of the gut bacteria to address this absence of fungi in the larval gut. The results demonstrated that the gut bacteria were able to selectively inhibit wild apple tree-associated fungi. Among them, Pseudomonas synxantha showed strong antagonistic ability, producing antifungal compounds. Using different analytical methods, such as column chromatography, mass spectrometry, HPLC, and NMR, an antifungal compound, phenazine-1-carboxylic acid (PCA), was identified. Activity of the compound was determined by the minimum inhibitory concentration method and electron microscopy. Moreover, our study showed that the gut bacteria could originate from noninfested apple microflora during infestation. Overall, the results showed that in newly invaded locations, A. mali larvae changed their gut microbiota and adopted new gut bacteria that prevented fungal colonization in the gut.

SUBMITTER: Bozorov T

PROVIDER: S-EPMC8554297 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:BackgroundInsects rely on olfaction to locate food, mates, and suitable oviposition sites for successful completion of their life cycle. Agrilus planipennis Fairmaire (emerald ash borer) is a serious invasive insect pest that has killed tens of millions of North American ash (Fraxinus spp) trees and threatens the very existence of the genus Fraxinus. Adult A. planipennis are attracted to host volatiles and conspecifics; however, to date no molecular knowledge exists on olfaction in A. planipennis. Hence, we undertook an antennae-specific transcriptomic study to identify the repertoire of odor processing genes involved in A. planipennis olfaction.Methodology and principal findingsWe acquired 139,085 Roche/454 GS FLX transcriptomic reads that were assembled into 30,615 high quality expressed sequence tags (ESTs), including 3,249 isotigs and 27,366 non-isotigs (contigs and singletons). Intriguingly, the majority of the A. planipennis antennal transcripts (59.72%) did not show similarity with sequences deposited in the non-redundant database of GenBank, potentially representing novel genes. Functional annotation and KEGG analysis revealed pathways associated with signaling and detoxification. Several odor processing genes (9 odorant binding proteins, 2 odorant receptors, 1 sensory neuron membrane protein and 134 odorant/xenobiotic degradation enzymes, including cytochrome P450s, glutathione-S-transferases; esterases, etc.) putatively involved in olfaction processes were identified. Quantitative PCR of candidate genes in male and female A. planipennis in different developmental stages revealed developmental- and sex-biased expression patterns.Conclusions and significanceThe antennal ESTs derived from A. planipennis constitute a rich molecular resource for the identification of genes potentially involved in the olfaction process of A. planipennis. These findings should help in understanding the processing of antennally-active compounds (e.g. 7-epi-sesquithujene) previously identified in this serious invasive pest.

Dataset Information

Wild Apple-Associated Fungi and Bacteria Compete to Colonize the Larval Gut of an Invasive Wood-Borer Agrilus mali in Tianshan Forests

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