Spores of arbuscular mycorrhizal fungi host surprisingly diverse communities of endobacteria

Abstract

Summary Arbuscular mycorrhizal fungi (AMF) are ubiquitous plant root symbionts, which can house two endobacteria: Ca. Moeniiplasma glomeromycotorum (CaMg) and Ca. Glomeribacter gigasporarum (CaGg). However, little is known about their distribution and population structure in natural AMF populations and whether AMF can harbour other endobacteria. We isolated AMF from two environments and conducted detailed analyses of endobacterial communities associated with surface‐sterilised AMF spores. Consistent with the previous reports, we found that CaMg were extremely abundant (80%) and CaGg were extremely rare (2%) in both environments. Unexpectedly, we discovered an additional and previously unknown level of bacterial diversity within AMF spores, which extended beyond the known endosymbionts, with bacteria belonging to 10 other phyla detected across our spore data set. Detailed analysis revealed that: CaGg were not limited in distribution to the Gigasporaceae family of AMF, as previously thought; CaMg population structure was driven by AMF host genotype; and a significant inverse correlation existed between the diversity of CaMg and diversity of all other endobacteria. Based on these data, we generate novel testable hypotheses regarding the function of CaMg in AMF biology by proposing that they might act as conditional mutualists of AMF.

Desert plants, arbuscular mycorrhizal fungi and associated bacteria: Exploring the diversity and role of symbiosis under drought

“…All the AMF spores analysed by microscopy (ca. 30 spores) revealed the presence of endofungal bacteria, suggesting a high prevalence of these symbionts in AMF, as shown in different environments (Lastovetsky et al, 2018 , 2024 ).…”

“…Studies focused on the interactions of AMF with microorganisms revealed, since 1970 (Mosse, 1970 ), that some AMF harbour morphologically diverse lineages of endofungal bacteria (Agnolucci et al, 2019 ; Araldi‐Brondolo et al, 2017 ; Bianciotto et al, 1996 , 2000 ; Bonfante & Anca, 2009 ; Lumini et al, 2007 ; Scannerini & Bonfante, 1991 ; Uehling et al, 2023 ). Most of the endofungal bacteria hitherto reported in Glomeromycotina have been classified into two main lineages: BRE for Burkholderia ‐related endobacteria and MRE for Mycoplasma ‐related endobacteria (Bianciotto et al, 2003 ; Naito et al, 2017 ; Naumann et al, 2010 ) being MRE most diverse and frequent in AMF than BRE (Lastovetsky et al, 2018 , 2024 ).…”

“…The impact of this group of endobacteria in AMF biology remains a tantalizing mystery, as AMF spores devoid of these MRE symbionts have yet to be obtained, and efforts to cultivate Ca Mg outside their fungal hosts have been unsuccessful to date. However, it has been hypothesized that Ca Mg may be non‐lethal parasites of Glomeromycotina and Mortierellomycotina fungi (Desiro et al, 2018 ; Naito et al, 2017 ) or conditional mutualists of their AMF hosts (Lastovetsky et al, 2024 ).…”

“…Besides BRE and MRE, some reports have suggested that AMF could harbour a greater diversity of bacterial endosymbionts, but to date, evidence of their role in the plant‐fungal symbiosis does not exist (Faghihinia et al, 2023 ; Lastovetsky et al, 2024 ; Pandit et al, 2022 ; Wang et al, 2022 ).…”

Functional team selection: a framework for local adaptation in plants and their belowground microbiomes

“…Adding a protist to the experimental system was shown to further increase the nitrogen gained by the AM fungus by at least 65% (Rozmoš et al 2022), which illustrates how trophic complexity within microbial communities can enhance nutrient availability and ultimately, host plant performance. Lastly, a recent study by Lastovetsky et al (2024) found that a single AM fungus spore can contain up to 227 endobacterial taxa, most of which have unknown functions but are proposed to be both parasitic and conditional mutualists.…”