The ambrosia symbiosis is specific in some species and promiscuous in others: evidence from community pyrosequencing

Abstract

Symbioses are increasingly seen as dynamic ecosystems with multiple associates and varying fidelity. Symbiont specificity remains elusive in one of the most ecologically successful and economically damaging eukaryotic symbioses: the ambrosia symbiosis of wood-boring beetles and fungi. We used multiplexed pyrosequencing of amplified internal transcribed spacer II (ITS2) ribosomal DNA (rDNA) libraries to document the communities of fungal associates and symbionts inside the mycangia (fungus transfer organ) of three ambrosia beetle species, Xyleborus affinis, Xyleborus ferrugineus and Xylosandrus crassiusculus. We processed 93 beetle samples from 5 locations across Florida, including reference communities. Fungal communities within mycangia included 14-20 fungus species, many more than reported by culture-based studies. We recovered previously known nutritional symbionts as members of the core community. We also detected several other fungal taxa that are equally frequent but whose function is unknown and many other transient species. The composition of fungal assemblages was significantly correlated with beetle species but not with locality. The type of mycangium appears to determine specificity: two Xyleborus with mandibular mycangia had multiple dominant associates with even abundances; Xylosandrus crassiusculus (mesonotal mycangium) communities were dominated by a single symbiont, Ambrosiella sp. Beetle mycangia also carried many fungi from the environment, including plant pathogens and endophytes. The ITS2 marker proved useful for ecological analyses, but the taxonomic resolution was limited to fungal genus or family, particularly in Ophiostomatales, which are under-represented in our amplicons as well as in public databases. This initial analysis of three beetle species suggests that each clade of ambrosia beetles and each mycangium type may support a functionally and taxonomically distinct symbiosis.

Metagenomic approach of associated fungi with <i>Megaplatypus mutatus</i> (Coleoptera: Platypodinae)

“…These results could be due to the known problems of using ITS markers with certain groups of ambrosial fungi (Fraedrich et al 2008;Kostovcik et al 2015). Ceriani-Nakamurakare et al (2016), using a culture dependent approach, reported Raffaelea arxii and three additional Raffaelea species.…”

“…However, an increasing number of studies suggest that certain beetle species can have multiple fungal associates (Batra 1966;Gebhardt et al 2004;Ceriani-Nakamurakare et al 2016). Moreover, Kostovcik et al (2015) suggested that the ambrosia interaction is ecologically dynamic and more species-rich than any other insect-fungus interaction. Ceriani-Nakamurakare et al (2016) characterized the fungal community associated with M. mutatus and Populus deltoides based on culture dependent methods.…”

“…Several studies have applied a metagenomic approach in microbes-beetle interactions, i.e. bacterial communities of Dendroctonus ponderosae (Adams et al 2013); fungal communities associated with bark beetles (Miller et al 2016) and fungal communities in mycangia of ambrosia beetles (Kostovcik et al 2015).…”

Novel ophiostomatalean fungi from galleries of Cyrtogenius africus (Scolytinae) infesting dying Euphorbia ingens

“…Many ambrosia beetles carry more than one fungal partner and these fungi are often isolated together (Carrillo et al 2014, Kostovcik et al 2015. The association of ophiostomatalean fungi with C.…”

Laurel Wilt in Natural and Agricultural Ecosystems: Understanding the Drivers and Scales of Complex Pathosystems

“…The movement of symbionts amongst ambrosia beetle species had been recognized previously [69,71,73,74]. However, the magnitude and speed with which this has occurred for R. lauricola is unprecedented [70].…”