Patterns of coevolution between ambrosia beetle mycangia and the <i>Ceratocystidaceae</i>, with five new fungal genera and seven new species

Mayers, Chase G.; Harrington, T. C.; Masuya, Hayato; Jordal, Bjarte H.; McNew, Douglas; Shih, Hsiu-Hui; Roets, Francois; Kietzka, Gabriella J.

doi:10.3767/persoonia.2020.44.02

Cited by 42 publications

(70 citation statements)

References 117 publications

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“…Proven nutritional mutualists are the so-called ambrosia fungi in the ascomycete orders Ophiostomatales (e.g., genus Raffaelea ), Microascales (e.g., genus Ambrosiella ), and less frequently, Hypocreales ( 1 , 12 , 25 ). Each genus of ambrosia fungi is typically associated with a specific lineage of beetles and a specific type of mycetangia ( 29 – 31 ). Within these lineages, some beetle species can exchange their primary ambrosia fungi ( 32 , 33 ), whereas others do appear to have species-specific mutualisms (e.g., reference 29 ).…”

Section: Introductionmentioning

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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Section: Introductionmentioning

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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“…Snyd. & Hans [ 26 , 42 – 45 ]. On the other hand, several other fungal species, including Geosmithia pallida , Epicoccum nigrum and Bionectria sp., have been found in association with the black twig borer on Mediterranean maquis plants [ 26 ].…”

Section: Introductionmentioning

confidence: 99%

Seasonal changes in population structure of the ambrosia beetle Xylosandrus compactus and its associated fungi in a southern Mediterranean environment

et al. 2020

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Exotic ambrosia beetles are increasing in Europe due to global trade and global warming. Among these xylomycetophagous insects, Xylosandrus compactus (Eichhoff) (Coleoptera: Curculionidae) is a serious threat for several Mediterranean host plants. Carob trees growing in Sicily (Italy) have been extensively attacked by beetles leading to rapid tree decline. Although X. compactus has been found in Europe for several years, most aspects of its ecology are still unknown. We thus studied the population structure and dynamics of X. compactus, together with its twig size preference during a sampling of infested carob trees in south east Sicily. In addition, fungi associated with insects or galleries were isolated and characterized. The results showed that, in this newly-colonized environment and host plant, adult X. compactus overwinters inside twigs and starts to fly and reproduce in mid spring, completing five generations before overwintering in late fall. The mean diameter of carob twigs infested by the beetle varied significantly over the seasons, with the insect tending to infest larger twigs as season progresses. The mean number of adults/gallery was 19.21, ranging from 6 to 28. The minimum temperature significantly affected the overwintering adult mortality. Ambrosiella xylebori and Fusarium solani were the main symbionts associated with the pest in this study. Acremonium sp. was instead recorded for the first time in Europe inside X. compactus galleries. Several other fungi species were also found for the first time in association with X. compactus. Our findings provide useful insights into the sustainable management of this noxious pest.

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“…An additional eight genera have recently been added to the family ( De Beer et al 2017 , 2018 , Mayers et al . 2015 , Mayers et al . 2020 , Nel et al 2018 ).…”

Section: Introductionmentioning

confidence: 99%

Epitypification of Ceratocystis fimbriata

Marincowitz¹,

Barnes²,

Beer³

et al. 2020

Fungal Systematics and Evolution

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Ceratocystis accommodates many important pathogens of agricultural crops and woody plants. Ceratocystis fimbriata, the type species of the genus is based on a type that is unsuitable for a precise application and interpretation of the species. This is because no culture or DNA data exist for the type specimen. The aim of this study was to select a reference specimen that can serve to stabilize the name of this important fungus. We selected a strain, CBS 114723, isolated from sweet potato in North Carolina, USA, in 1998 for this purpose. The strain was selected based on the availability of a living culture in a public depository. A draft genome sequence is also available for this strain. Its morphological characteristics were studied and compared with the existing and unsuitable type specimen as well as with the original descriptions of C. fimbriata. The selected strain fits the existing concept of the species fully and we have consequently designated it as an epitype to serve as a reference specimen for C. fimbriata.

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Patterns of coevolution between ambrosia beetle mycangia and the Ceratocystidaceae, with five new fungal genera and seven new species

Cited by 42 publications

References 117 publications

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

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

Seasonal changes in population structure of the ambrosia beetle Xylosandrus compactus and its associated fungi in a southern Mediterranean environment

Epitypification of Ceratocystis fimbriata

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