Different Arbuscular Mycorrhizal Fungi Cocolonizing on a Single Plant Root System Recruit Distinct Microbiomes

Abstract

<p>Plant roots are usually colonized by various arbuscular mycorrhizal (AM) fungal species, which vary in morphological, physiological, and genetic traits. This colonization constitutes the mycorrhizal nutrient uptake pathway (MP) and supplements the pathway through roots. Simultaneously, the extraradical hyphae of each AM fungus is associated with a community of bacteria. However, whether the community structure and function of the microbiome on the extraradical hyphae differ between AM fungal species remains unknown. In order to understand the community structure and the predicted functions of the microbiome associated with different AM fungal species, a splitroot compartmented rhizobox cultivation system, which allowed us to inoculate two AM fungal species separately in two root compartments, was used. We inoculated two separate AM fungal species combinations, (i) F<em>unneliformis mosseae</em> and <em>Gigaspora margarita</em> and (ii) <em>Rhizophagus intraradices </em>and <em>G. margarita</em>, on a single root system of cotton. The hyphal exudate-fed, active microbiome was measured by combining <sup>13</sup>C-DNA stable isotope probing with MiSeq sequencing. We found that different AM fungal species, which were simultaneously colonizing a single root system, hosted active microbiomes that were distinct from one another. Moreover, the predicted potential functions of the different microbiomes were distinct. We conclude that the arbuscular mycorrhizal fungal component of the system is responsible for the recruitment of distinct microbiomes in the hyphosphere. We found that arbuscular mycorrhizal fungi cocolonizing on single plant roots recruit their own specific microbiomes, which should be considered in evaluating plant microbiome form and function. Our findings demonstrate the importance of understanding trophic interactions in order to gain insight into the plant-AM fungus-bacterium symbiosis</p>

The potential role of Mucoromycotina ‘fine root endophytes’ in plant nitrogen nutrition

“…Likewise, AMF phosphate acquisition from organic sources is likely dependent on interactions with phosphate-mineralizing bacteria associated with the hyphae (Jiang et al, 2021). Recent research has shown that different species of AMF colonising the same root system recruit distinct microbiomes around their extraradical mycelia with unknown impacts on soil nutrient cycling (Zhou et al, 2020). It is likely that MFRE also recruit their own distinct microbiomes, although the extent to which saprotrophic lineages require their microbiome to break down organic matter and transfer resulting nutrients on to the host plant requires further investigation.…”

Plant-associated fungi support bacterial resilience following water limitation

“…This suggests that R. irregularis and S. bescii modified edaphic conditions in some way that broadly supported bacterial resilience to water limitation. Plant-associated fungi can exude plant-derived C 24,[29][30][31][32] , promote biofilm formation 88 , enhance soil aggregation through their interactions with other soil biota 14,89 , and facilitate bacterial transport through soil 90 . Together, these fungalmediated processes could help maintain soil connectivity, microbial activity, and nutrient cycling under water-limited conditions, thereby preventing bacterial dormancy and death despite a substantial decline in soil moisture.…”

“…While both fungal lineages supported bacterial resilience, R. irregularis elicited a stronger positive response than S. bescii-both with respect to the number of ASVs and the magnitude of individual responses. Distinct microbial consortia associate with different mycorrhizal lineages 18,19,31,89 . Although empirical evidence remains sparse, different mycorrhizal exudate profiles, growth habits, and other functional traits may shape the composition and activity of the surrounding microbial community 48,89,95,96 , a phenomenon that has been documented more extensively for root-microbe interactions [97][98][99] .…”

“…Distinct bacterial communities form in proximity to different fungal lineages 18,19,31 . However, we have a limited understanding of how different plant-associated fungi may shape the soil microbiome's response to environmental stress.…”

Sculpting the soil microbiota

“…Soil structure results from structural clusters of mineral particles, encrusted organic matter, polysaccharides, plant roots and other biotic materials (Huang et al ., 2015; Lucas et al ., 2019; Volikov et al ., 2016; Zhou et al . 2020a). These particles are classified in micro‐aggregates (<250 μm) and macro‐aggregates (0.25–2 mm) that contain a patchy distribution of mineral particles and nutrients (Asano and Wagai, 2014, 2015).…”