Developmental biology of Xyleborus bispinatus (Coleoptera: Curculionidae) reared on an artificial medium and fungal cultivation of symbiotic fungi in the beetle's galleries

Cruz, Luisa F.; Rocio, S.A.; Durán, Laura; Menocal, Octavio; García-Ávila, Clemente de Jesús; Carrillo, Daniel

doi:10.1016/j.funeco.2018.07.007

Cited by 19 publications

(19 citation statements)

References 45 publications

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“…are true nutritional symbionts of ambrosia beetles and that other yeasts act as opportunistic organisms. However, the yeast species found in this study have been reported consistently in association with X. volvulus and other ambrosia beetles, including (i) C. berthetii with X. volvulus and Platypus externedentatus (http://www.westerdijkinstitute.nl/Collections/), (ii) Ambrosiozyma monospora with X. volvulus and X. bispinatus (33,34), (iii) Candida laemsonensis with Xyleborus affinis Eichhoff (47), and (iv) Candida nemodendra with Xyleborus aemulus Woll. (48).…”

Section: Discussionmentioning

confidence: 50%

“…Collection and rearing of beetles. Foundresses were collected from naturally infested logs from avocado orchards located in Homestead, FL (25°29=38== N 80°28=53== W), as reported by Cruz et al (33). Fully sclerotized X. volvulus females were morphologically identified according to Rabaglia et al (24) and reared in a sterile avocado sawdust medium in 50-ml centrifuge tubes as described in Menocal et al (34).…”

Section: Methodsmentioning

confidence: 99%

“…Pure fungal isolates were obtained by a single spore culture and identified as described in Cruz et al (33). Briefly, DNA was obtained by a modified cetyl trimethyl-ammonium bromide (CTAB) protocol (53), and portions of the nuclear large subunit 28S ribosomal DNA (rDNA) using primers LR0R/LR5 (54) and the small subunit rDNA with primers NS1/NS4 (55) were amplified.…”

Section: Methodsmentioning

confidence: 99%

“…Additionally, teneral adults and F 1 offspring adult females were aseptically excised and separately processed to isolate the symbionts associated with either the mycangium (heads) or the gut (abdomen). Identification was carried out using the primers listed above as described in Cruz et al (33).…”

Section: Methodsmentioning

confidence: 99%

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Xyleborus volvulus (Coleoptera: Curculionidae): Biology and Fungal Associates

Cruz

Menocal

Mantilla

et al. 2019

Appl Environ Microbiol

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The ambrosia beetle Xyleborus volvulus Fabricius has been reported as a potential vector of the plant pathogen Raffaelea lauricola T.C. Harr., Fraedrich & Aghayeva that is affecting avocado orchards in South Florida. In this study, we examined its life cycle, process of gallery formation, gallery structure, and fungal associates by rearing one generation on avocado sawdust medium under control conditions. The adult foundress excavated a vertical tunnel that constituted the main gallery with a length of 2.5 cm, followed by the construction of up to six secondary galleries with a total length of 4.4 cm. The time period for one generation (egg to adult) was 28 days. Teneral males emerged 3 days after the emergence of the first females. The F1 generation did not significantly contribute to gallery expansion. Four species of Raffaelea and nine yeast species were recovered from galleries and beetles. Raffaelea arxii and Candida berthetii were the most frequent symbionts recovered from new adults and galleries. Candida berthetii dominated during the early stages of the gallery development, whereas R. arxii was most frequent in later stages. Other Raffaelea species were inconsistently isolated from galleries, which suggests a strong association between Xyleborus volvulus and both R. arxii and C. berthetii. These results suggest that R. arxii is the primary nutritional symbiont of X. volvulus and that yeast species may be pioneer colonizers that assist with the growth of fungal symbionts. IMPORTANCE Ambrosia beetles cultivate fungi in tunnels bored into weakened host trees. This obligate interaction is required for their survival as beetles feed on these symbiotic fungi, and the fungi benefit from transportation by the beetles. Xyleborus volvulus carries many nonpathogenic symbionts; however, recently the acquisition of Raffaelea lauricola (the causal agent of a lethal vascular disease of lauraceous trees) by this beetle has altered its status from wood degrader to potential pest in avocado. We conducted a study to understand the relationship of this beetle and its fungal associates. Our results show that X. volvulus has a multipartite flexible association with different Raffaelea species. The lack of fidelity in the mutualistic association may explain the acquisition of R. lauricola. Knowing the beetle biology and its mutualistic interactions furthers an understanding of the beetle’s role as a potential vector and in disease transmission.

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Section: Discussionmentioning

confidence: 50%

Section: Methodsmentioning

confidence: 99%

Section: Methodsmentioning

confidence: 99%

Section: Methodsmentioning

confidence: 99%

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Xyleborus volvulus (Coleoptera: Curculionidae): Biology and Fungal Associates

Cruz

Menocal

Mantilla

et al. 2019

Appl Environ Microbiol

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“…Previous studies have indicated that fungal communities of ambrosia beetles are dynamic, both spatially within their galleries and temporally throughout development with the relative abundances of the different symbionts changing over time (34)(35)(36)(37)(38). A succession of different fungal (and bacterial) species should be expected, because as the gallery matures, the surrounding wood substrate dries out and is probably degraded by fungal enzymes (39).…”

mentioning

confidence: 99%

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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