Mycoplasma-related endobacteria within Mortierellomycotina fungi: diversity, distribution and functional insights into their lifestyle

Abstract

Bacterial interactions with animals and plants have been examined for over a century; by contrast, the study of bacterial-fungal interactions has received less attention. Bacteria interact with fungi in diverse ways, and endobacteria that reside inside fungal cells represent the most intimate interaction. The most significant bacterial endosymbionts that have been studied are associated with Mucoromycota and include two main groups: Burkholderia-related and Mycoplasma-related endobacteria (MRE). Examples of Burkholderia-related endobacteria have been reported in the three Mucoromycota subphyla. By contrast, MRE have only been identified in Glomeromycotina and Mucoromycotina. This study aims to understand whether MRE dwell in Mortierellomycotina and, if so, to determine their impact on the fungal host. We carried out a large-scale screening of 394 Mortierellomycotina strains and employed a combination of microscopy, molecular phylogeny, next-generation sequencing and qPCR. We detected MRE in 12 strains. These endosymbionts represent novel bacterial phylotypes and show evidence of recombination. Their presence in Mortierellomycotina demonstrates that MRE occur within fungi across Mucoromycota and they may have lived in their common ancestor. We cured the fungus of its endosymbionts with antibiotics and observed improved biomass production in isogenic lines lacking MRE, demonstrating that these endobacteria impose some fitness costs to their fungal host. Here we provided the first functional insights into the lifestyle of MRE. Our findings indicate that MRE may be antagonistic to their fungal hosts, and adapted to a non-lethal parasitic lifestyle in the mycelium of Mucoromycota. However, context-dependent adaptive benefits to their host at minimal cost cannot not be excluded. Finally, we conclude that Mortierellomycotina represent attractive model organisms for exploring interactions between MRE and fungi.

Genome and evolution of the arbuscular mycorrhizal fungus Diversispora epigaea (formerly Glomus versiforme) and its bacterial endosymbionts

“…This result suggests that the assembled De MREII and De MREI‐1 genomes are complete or nearly complete. The divergence of 16S rRNA sequences between De MREI‐1/ De MREI‐2 and De MREII is 15%, which exceeds the criterion proposed for species discrimination in Mollicutes (Desirò et al ., ). The divergence on a genomic scale is much higher: only 22% of De MREI‐1/ De MREI‐2 genomes show synteny with the De MREII genome (Fig.…”

“…The BRE are found only in the family Gigasporaceae (Bonfante & Desirò, ), and loss of BRE impairs fungal growth (Lumini et al ., ). By contrast, the MRE are distributed broadly among the AM fungi, but their functions are largely unknown, although a fitness cost has been demonstrated recently in Mortierella harboring MRE (Desirò et al ., ). The MRE population in AM fungi is diverse and, based on 16S rRNA phylogeny, there are two major phylotypes (Naumann et al ., ; Ghignone et al ., ; Bonfante & Desirò, ; Desirò et al ., ) that coexist in many AM fungal lineages.…”

“…By contrast, the MRE are distributed broadly among the AM fungi, but their functions are largely unknown, although a fitness cost has been demonstrated recently in Mortierella harboring MRE (Desirò et al ., ). The MRE population in AM fungi is diverse and, based on 16S rRNA phylogeny, there are two major phylotypes (Naumann et al ., ; Ghignone et al ., ; Bonfante & Desirò, ; Desirò et al ., ) that coexist in many AM fungal lineages. A complete genome assembly of MRE from Dentiscutata heterogama ( Dh MRE) (Torres‐Cortés et al ., ) and three metagenome assemblies of MRE from Racocetra verrucosa ( Rv MRE), Rhizophagus clarus ( Rc MRE), and Claroideoglomus etunicatum ( Ce MRE) (Naito et al ., ) have provided initial insights into their ancient association with AM fungi; however, the full extent of diversity within a single AM fungus remains to be explored.…”

Distribution and population structure of endobacteria in arbuscular mycorrhizal fungi at North Atlantic dunes

“…This was largely unexpected, as molecular evolution patterns suggest that CaMg may be a parasite of AMF [13,14]. Moreover, there is experimental evidence indicating that endobacteria closely related to CaMg are conditional parasites of Mortierellomycotina, another group of Mucoromycota fungi [41]. Although the exact role of CaMg in the biology of AMF has not been established, two evolutionary scenarios could account for the persistence of a heritable parasite in AMF populations: (i) occasional horizontal transmission [42,43], and (ii) conditional mutualism [44][45][46].…”

Metabolome changes are induced in the arbuscular mycorrhizal fungus Gigaspora margarita by germination and by its bacterial endosymbiont

“…For example, the PLS-DA of the unidentified features ( (ESI) conditions bias the analysis towards polar and water-soluble metabolites. Whereas this paper is focused on the detection of polar metabolites, future profiling of the lipidome is also likely to yield valuable information, and previous reports have shown that lipids play a role in the endosymbiosis between the fungi and bacteria (Desirò et al 2018;Lastovetsky et al 2016;Pétriacq et al 2017).The detected features could be assigned to a number of compound classes: amino acids, nucleotides, organic acids, and sugars. Unidentified features that showed a high level of differentiation between groups could be further characterized to determine biological significance.…”