Fruitbody chemistry underlies the structure of endofungal bacterial communities across fungal guilds and phylogenetic groups

Abstract

Eukaryote-associated microbiomes vary across host taxa and environments but the key factors underlying their diversity and structure in fungi are still poorly understood. Here we determined the structure of bacterial communities in fungal fruitbodies in relation to the main chemical characteristics in ectomycorrhizal (EcM) and saprotrophic (SAP) mushrooms as well as in the surrounding soil. Our analyses revealed significant differences in the structure of endofungal bacterial communities across fungal phylogenetic groups and to a lesser extent across fungal guilds. These variations could be partly ascribed to differences in fruitbody chemistry, particularly the carbon-to-nitrogen ratio and pH. Fungal fruitbodies appear to represent nutrient-rich islands that derive their microbiome largely from the underlying continuous soil environment, with a larger overlap of operational taxonomic units observed between SAP fruitbodies and the surrounding soil, compared with EcM fungi. In addition, bacterial taxa involved in the decomposition of organic material were relatively more abundant in SAP fruitbodies, whereas those involved in release of minerals were relatively more enriched in EcM fruitbodies. Such contrasts in patterns and underlying processes of the microbiome structure between SAP and EcM fungi provide further evidence that bacteria can support the functional roles of these fungi in terrestrial ecosystems.

Bacterial Community Analysis and Potential Functions of Core Taxa in Different Parts of the Fungus Cantharellus cibarius

“…At the genus level, numerous members of the Allorhizobium-Neorhizobium-Pararhizobium-Rhizobium complex were distributed in the fruit bodies of C. cibarius , which was consistent with the observations of ( Pent et al (2017 , 2020) , Rinta-Kanto et al (2018) , and Gohar et al (2020) . Together with other symbiotic bacteria, these genera may play a key role in maintaining the health of the fruit body ( Gohar et al 2020 ).…”

“…These authors suggested that the soil pH and host identity were the predominant factors affecting bacterial community composition. Pent et al (2020) continued to merge high-throughput sequencing and chemical composition determination to compare and analyze the chemical content and bacterial community composition of the fruit bodies of EMF, including C. cibarius , and revealed that the differences in the chemical composition of fruit bodies also markedly impacted bacterial community composition. Recently, Gohar et al (2020) analyzed bacterial community potential function variation at different development stages (young, middle-aged, and old) and in internal (cap, stipe lower internal, stipe middle internal) and external (gills, cap surface, stipe lower external, and stipe middle external) compartments of fruit bodies of C. cibarius , and compared the bacteria with that of other ectomycorrhizae.…”

Let’s Get Physical: Bacterial-Fungal Interactions and Their Consequences in Agriculture and Health

“…As the field of bacterial-fungal interactions grows, we begin to understand the implications that these interactions have not only on the microorganisms, but also on plant and human hosts. This review shows that there are several areas of overlapping commonalities between BFIs in agriculture and clinical settings, including the use of fungal structures for bacterial dispersal [ 11 , 62 , 63 , 73 ], using ECM for bacterial attachment [ 14 , 18 ], and developmental changes that can occur in both fungi and bacteria [ 43 , 49 ] ( Figure 2 ). It is possible that there are even more commonalities that have yet to be discovered, including endosymbiosis in clinical settings.…”

“…Bacterial communities have been identified in ectomycorrhizal fungi and in saprotrophic mushrooms, where the community structure was dependent on the fungal phylogenetic groups. This variation has been attributed to variations in fruiting body chemistry, specifically to the C:N ratio and pH [ 43 ].…”

“…In both cases, endobacteria are found in the spores, suggesting that control of host sporulation by endobacteria is sufficient to regulate their own transmission. The attachment of Burkholderia glumae to F. graminearum results in increased sporulation in vitro, which suggests that the BFI may result in enhanced dispersal of the fungus in the field [ 43 ]. Bacterial interactions with Penicillium roqueforti resulted in faster rate of growth and sporulation in vitro [ 51 ].…”