Plant-associated fungi support bacterial resilience following water limitation

Abstract

Drought disrupts soil microbial activity and many biogeochemical processes. Although plant-associated fungi can support plant performance and nutrient cycling during drought, their effects on nearby drought-exposed soil microbial communities are not well resolved. We used H218O quantitative stable isotope probing (qSIP) and 16S rRNA gene profiling to investigate bacterial community dynamics following water limitation in the hyphospheres of two distinct fungal lineages (Rhizophagus irregularis and Serendipita bescii) grown with the bioenergy model grass Panicum hallii. In uninoculated soil, a history of water limitation resulted in significantly lower bacterial growth potential and growth efficiency, as well as lower diversity in the actively growing bacterial community. In contrast, both fungal lineages had a protective effect on hyphosphere bacterial communities exposed to water limitation: bacterial growth potential, growth efficiency, and the diversity of the actively growing bacterial community were not suppressed by a history of water limitation in soils inoculated with either fungus. Despite their similar effects at the community level, the two fungal lineages did elicit different taxon-specific responses, and bacterial growth potential was greater in R. irregularis compared to S. bescii-inoculated soils. Several of the bacterial taxa that responded positively to fungal inocula belong to lineages that are considered drought susceptible. Overall, H218O qSIP highlighted treatment effects on bacterial community structure that were less pronounced using traditional 16S rRNA gene profiling. Together, these results indicate that fungal–bacterial synergies may support bacterial resilience to moisture limitation.

Deciphering microbiomes dozens of meters under our feet and their edaphoclimatic and spatial drivers

“…There was a positive correlation between aridity and bacteria‐fungi associations in the topsoil, but we observed an opposite correlation in the deep soil (Figure S14). As we know, when water availability is scarce, plant‐associated fungi can support bacterial resilience through fungal‐bacterial synergies (Hestrin et al., 2022), and then induce species coexistence (Lozano et al., 2021; Zelezniak et al., 2015). For example, interactions between rhizobacteria (PGPR) and arbuscular mycorrhizal fungi (AMF) using plants as a medium can induce plant tolerance to water limitation (De Vries et al., 2020).…”

Arbuscular mycorrhizal fungi induced different proline accumulations in two sorghum accessions in a response to drought stress

“…These results show that AMF has an important role in reducing drought stress in soil ecosystems. AMF can maintain soil moisture stability under drought stress conditions, ensuring that the microorganism community surrounding the root area is not adversely affected (Bahadur et al 2019;Hestrin et al 2022). However, under normal conditions, the AMF inoculation did not show a significant effect on the increase in total soil microbial activity.…”

“…However, research on the effects of AMF application on soil microbial communities is still scarce. AMF has been shown to not only improve the adaptability and resistance of its host plants but also to maintain the stability of the soil microbi-al community (Hestrin et al 2022). Hestrin et al (2022) demonstrated that applying AMF simultaneously can provide a protective effect on soil microbial communities exposed to drought stress.…”

“…AMF has been shown to not only improve the adaptability and resistance of its host plants but also to maintain the stability of the soil microbi-al community (Hestrin et al 2022). Hestrin et al (2022) demonstrated that applying AMF simultaneously can provide a protective effect on soil microbial communities exposed to drought stress. Soil inoculated with AMF had a higher microbial growth efficiency than soil not inoculated with AMF.…”

Arbuscular mycorrhiza convey significant plant carbon to a diverse hyphosphere microbial food web and mineral‐associated organic matter

“…Bacteria can also attach to non-living hyphae and use them as a substrate (Toljander et al, 2006(Toljander et al, , 2007. Our prior work suggests AMF have diverse effects on nearby hyphosphere microbiomes: stimulating organic matter decomposition and nitrogen (N) transfer (Nuccio et al, 2013), supporting water transport (Kakouridis et al, 2022) and drought resilience (Hestrin et al, 2022), and stimulating cross-kingdom trophic interactions (Nuccio et al, 2022). However, these small-scale interactions can be difficult to directly measure, and under native soil conditions, it is particularly challenging to directly evaluate the hyphosphere effects without the influence of roots and rhizosphere organisms.…”