Impact of Rearing Conditions on the Ambrosia Beetle’s Microbiome

Ibarra-Juárez, Luis A.; Desgarennes, Damaris; Vázquez-Rosas-Landa, Mirna; Villafán, Emanuel; Alonso-Sánchez, Alexandro; Ferrera-Rodríguez, Ofelia; Moya, Andrés; Carrillo, Daniel; Cruz, Luisa F.; Carrión, Gloria; López-Buenfil, Abel; García-Ávila, Clemente de Jesús; Ibarra-Laclette, Enrique; Lamelas, Araceli

doi:10.3390/life8040063

Cited by 22 publications

(21 citation statements)

References 59 publications

(73 reference statements)

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“…Second, their metabarcoding methods were inadequate for the ambrosia beetles that we focus on, because their models are associated with Ophiostomatales fungi for which internal transcribed spacer (ITS) metabarcoding does not work ( 63 – 65 ). In contrast, our 18S metabarcoding approach delivered results that are consistent with a previous isolation study, which has shown a lower abundance of OTUs in lab-reared ambrosia beetles than in wild-reared ambrosia beetles ( 46 ).…”

Section: Discussionsupporting

confidence: 89%

“…Among these OTUs, the five most abundant OTUs belonged to the genera Saccharomycopsis, Candida, and Raffaelea. These results correspond with the culturing results from other bark and ambrosia beetles (25,38,46,71). Both our metabarcoding and SEM visualizations showed that the yeasts are dominant in young galleries, after which filamentous Raffaelea species follow.…”

Section: Figsupporting

confidence: 88%

“…The most abundant and widely distributed bacterial genera were Enterobacter and Stenotrophomonas. Both genera have been isolated from other bark and ambrosia beetles ( 4 , 27 , 46 , 66 – 70 ). Their relative abundance negatively correlated with the diversity of bacteria, suggesting that they might be able to structure (i.e., dominate) the bacterial communities, possibly by secondary metabolites (see Fig.…”

Section: Discussionmentioning

confidence: 99%

“…To gain insights into the metabolic potential of the fungi associated with the ambrosia beetles, available genomes of the phylogenetically most closely related fungi (n ϭ 33 genomes; see Table S5 at https://doi.org/10.6084/m9.figshare.12477593) were selected, and the core genome and their metabolic profile were determined following the methodology reported by Ibarra-Juarez et al (46). Additionally, the presence of genes and specific metabolic pathways (degradation of plant and fungal cell wall components; biosynthesis of essential amino acids, cofactors and vitamins; nitrogen fixation; quorum sensing and biofilm production) were analyzed and plotted in a heatmap using "ggplot2" and "vegan" for R (v. To infer the metabolic capability of the bacterial microbiome in specific pathways, the relative frequencies of all genes involved in these pathways were calculated per sample.…”

Section: Methodsmentioning

confidence: 99%

“…There is a long history of studying fungal and bacterial associates in ambrosia beetles, e.g., by using traditional culturing techniques ( 32 , 34 , 36 – 38 , 45 ) or culture-independent approaches ( 4 , 27 , 46 , 47 ). Some of these studies have monitored fungal symbionts over time ( 37 , 38 , 48 – 50 ).…”

Section: Introductionmentioning

confidence: 99%

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Evidence for Succession and Putative Metabolic Roles of Fungi and Bacteria in the Farming Mutualism of the Ambrosia Beetle Xyleborus affinis

et al. 2020

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The bacterial and fungal community involved in ambrosia beetle fungiculture remains poorly studied compared to the famous fungus-farming ants and termites. Here we studied microbial community dynamics of laboratory nests, adults, and brood during the life cycle of the sugarcane shot hole borer, Xyleborus affinis. We identified a total of 40 fungal and 428 bacterial operational taxonomic units (OTUs), from which only five fungi (a Raffaelea fungus and four ascomycete yeasts) and four bacterial genera (Stenotrophomonas, Enterobacter, Burkholderia, and Ochrobactrum) can be considered the core community playing the most relevant symbiotic role. Both the fungal and bacterial populations varied significantly during the beetle’s life cycle. While the ascomycete yeasts were the main colonizers of the gallery early on, the Raffaelea and other filamentous fungi appeared after day 10, at the time when larval hatching happened. Regarding bacteria, Stenotrophomonas and Enterobacter dominated overall but decreased in foundresses and brood with age. Finally, inferred analyses of the putative metabolic capabilities of the bacterial microbiome revealed that they are involved in (i) degradation of fungal and plant polymers, (ii) fixation of atmospheric nitrogen, and (iii) essential amino acid, cofactor, and vitamin provisioning. Overall, our results suggest that yeasts and bacteria are more strongly involved in supporting the beetle-fungus farming symbiosis than previously thought. IMPORTANCE Ambrosia beetles farm their own food fungi within tunnel systems in wood and are among the three insect lineages performing agriculture (the others are fungus-farming ants and termites). In ambrosia beetles, primary ambrosia fungus cultivars have been regarded essential, whereas other microbes have been more or less ignored. Our KEGG analyses suggest so far unknown roles of yeasts and bacterial symbionts, by preparing the tunnel walls for the primary ambrosia fungi. This preparation includes enzymatic degradation of wood, essential amino acid production, and nitrogen fixation. The latter is especially exciting because if it turns out to be present in vivo in ambrosia beetles, all farming animals (including humans) are dependent on atmospheric nitrogen fertilization of their crops. As previous internal transcribed spacer (ITS) metabarcoding approaches failed on covering the primary ambrosia fungi, our 18S metabarcoding approach can also serve as a template for future studies on the ambrosia beetle-fungus symbiosis.

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