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As microbiome research has progressed, it has become clear that most, if not all, eukaryotic organisms are hosts to microbiomes composed of prokaryotes, other eukaryotes, and viruses. Fungi have only recently been considered holobionts with their own microbiomes, as filamentous fungi have been found to harbor bacteria (including cyanobacteria), mycoviruses, other fungi, and whole algal cells within their hyphae. Constituents of this complex endohyphal microbiome have been interrogated using multi-omic approaches. However, a lack of tools, techniques, and standardization for integrative multi-omics for small-scale microbiomes (e.g., intracellular microbiomes) has limited progress towards investigating and understanding the total diversity of the endohyphal microbiome and its functional impacts on fungal hosts. Understanding microbiome impacts on fungal hosts will advance explorations of how “microbiomes within microbiomes” affect broader microbial community dynamics and ecological functions. Progress to date as well as ongoing challenges of performing integrative multi-omics on the endohyphal microbiome is discussed herein. Addressing the challenges associated with the sample extraction, sample preparation, multi-omic data generation, and multi-omic data analysis and integration will help advance current knowledge of the endohyphal microbiome and provide a road map for shrinking microbiome investigations to smaller scales.

 

Members of the fungal genusMorchellaare widely known for their important ecological roles and significant economic value. In this study, we used amplicon and genome sequencing to characterize bacterial communities associated with sexual fruiting bodies from wild specimens, as well as vegetative mycelium and sclerotia obtained fromMorchellaisolates grownin vitro. These investigations included diverse representatives from both Elata and EsculentaMorchellaclades. Unique bacterial community compositions were observed across the various structures examined, both within and across individualMorchellaisolates or specimens. However, specific bacterial taxa were frequently detected in association with certain structures, providing support for an associated core bacterial community. Bacteria from the genusPseudomonasandRalstoniaconstituted the core bacterial associates ofMorchellamycelia and sclerotia, while other genera (e.g.,Pedobacterspp.,Deviosaspp., andBradyrhizobiumspp.) constituted the core bacterial community of fruiting bodies. Furthermore, the importance ofPseudomonasas a key member of the bacteriome was supported by the isolation of severalPseudomonasstrains from mycelia duringin vitrocultivation. Four of the six mycelial-derivedPseudomonasisolates shared 16S rDNA sequence identity with amplicon sequences recovered directly from the examined fungal structures. Distinct interaction phenotypes (antagonistic or neutral) were observed in confrontation assays between these bacteria and variousMorchellaisolates. Genome sequences obtained from thesePseudomonasisolates revealed intriguing differences in gene content and annotated functions, specifically with respect to toxin-antitoxin systems, cell adhesion, chitinases, and insecticidal toxins. These genetic differences correlated with the interaction phenotypes. This study provides evidence thatPseudomonasspp. are frequently associated withMorchellaand these associations may greatly impact fungal physiology.