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Drought Stress Triggers Shifts in the Root Microbial Community and Alters Functional Categories in the Microbial Gene Pool

ABSTRACT: Drought is a major threat to crop productivity and causes decreased plant growth, poor yields, and crop failure. Nevertheless, the frequency of droughts is expected to increase in the coming decades. The microbial communities associated with crop plants can influence how plants respond to various stresses; hence, microbiome manipulation is fast becoming an effective strategy for improving the stress tolerance of plants. The effect of drought stress on the root microbiome of perennial woody plants is currently poorly understood. Using Populus trees as a model ecosystem, we found that the diversity of the root microbial community decreased during drought treatment and that compositional shifts in microbes during drought stress were driven by the relative abundances of a large number of dominant phyla, including Actinobacteria, Firmicutes, and Proteobacteria. A subset of microbes, including Streptomyces rochei, Bacillus arbutinivorans, B. endophyticus, B. megaterium, Aspergillus terreus, Penicillium raperi, Trichoderma ghanense, Gongronella butleri, and Rhizopus stolonifer, was isolated from the drought-treated poplar rhizosphere soils, which have potentially beneficial to plant fitness. Further controlled inoculation experiments showed that the isolated bacterial and fungal isolates positively impacted plant growth and drought tolerance. Collectively, our results demonstrate the impact of drought on root microbiome structure and provide a novel example of manipulating root microbiomes to improve plant tolerance.

SUBMITTER: Xie J

PROVIDER: S-EPMC8566882 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:Mixing plant litters of multiple species can alter litter decomposition, a key driver of carbon and nutrient cycling in terrestrial ecosystems. Changes in microbial decomposer communities is proposed as one of the mechanisms explaining this litter-mixture effect, but the underlying mechanism is unclear. In a microcosm litterbag experiment, we found that, at the early stage of decomposition, litter mixing promoted tomato root litter decomposition, thus generating a synergistic nonadditive litter-mixture effect. The transplanting decomposer community experiment showed that changes in microbial decomposer communities contributed to the nonadditive litter-mixture effect on tomato root litter decomposition. Moreover, litter mixing altered the abundance and diversity of bacterial and fungal communities on tomato root litter. Litter mixing also stimulated several putative keystone operational taxonomic units (OTUs) in the microbial correlation network, such as Fusarium sp. fOTU761 and Microbacterium sp. bOTU6632. Then, we isolated and cultured representative isolates of these two taxa, named Fusarium sp. F13 and Microbacterium sp. B26. Subsequent in vitro tests found that F13, but not B26, had strong decomposing ability; moreover, these two isolates developed synergistic interaction, thus promoted litter decomposition in coculture. Addition of F13 or B26 both promoted the decomposing activity of the resident decomposer community on tomato root litter, confirming their importance for litter decomposition. Overall, litter mixing promoted tomato root litter decomposition through altering microbial decomposers, especially through stimulating certain putative keystone taxa. IMPORTANCE Microbial decomposer community plays a key role in litter decomposition, which is an important regulator of soil carbon and nutrient cycling. Though changes in decomposer communities has been proposed as one of the potential underlying mechanisms driving the litter-mixture effects, direct evidence is still lacking. Here, we demonstrated that litter mixing stimulated litter decomposition through altering microbial decomposers at the early stage of decomposition. Moreover, certain putative keystone taxa stimulated by litter mixing contributed to the nonadditive litter-mixture effect. In vitro culturing validated the role of these taxa in litter decomposition. This study also highlights the possibility of regulating litter decomposition through manipulating certain microbial taxa.

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Drought Stress Triggers Shifts in the Root Microbial Community and Alters Functional Categories in the Microbial Gene Pool

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