Root microbiome assembly of As‐hyperaccumulator <scp><i>Pteris vittata</i></scp> and its efficacy in arsenic requisition

Xiao, Enzong; Cui, Jinli; Sun, Weimin; Jiang, Shiming; Huang, Minyi; Kong, Deguan; Wu, Qihang; Xiao, Tangfu; Sun, Xiaoxu; Ning, Zengping

doi:10.1111/1462-2920.15299

Cited by 30 publications

(9 citation statements)

References 90 publications

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“…Das et al (2017) and Yu et al (2020) also demonstrated that soil arsenic pollution significantly reduced bacterial diversity in the P. vittata rhizosphere. Many studies concerning the effects of arsenic on microbial diversity in the rhizosphere of P. vittata have focused on culturable bacterial and fungal groups (Turpeinen et al, 2004;Das et al, 2016Das et al, , 2017Xiao et al, 2021). These studies have usually reported a reduced diversity of culturable bacteria and fungi due to arsenic pollution (Das et al, 2016), and they have also shown that arsenic pollution leads to an increase in the relative abundance of bacteria and fungi species/strains with tolerance and/or metabolic functions for arsenic (Turpeinen et al, 2004;Das et al, 2017).…”

Section: Discussionmentioning

confidence: 99%

“…The perennial fern Pteris vittata (Chinese brake fern) was the first known arsenic hyperaccumulator to be highly tolerant and efficient in accumulating arsenic. Pteris vittata has been reported to accumulate up to 22,630 mg kg −1 dry weight of arsenic in fronds (Ma et al, 2001), arousing extensive research interest in its application in the phytoremediation of arseniccontaminated soil (Xie et al, 2009;Xiao et al, 2021). Studies have shown that the root exudates of P. vittata can affect soil pH, thereby altering the bioavailability of arsenic in soil (Yang et al, 2022), which is one of the main factors limiting the arsenic absorption efficiency of P. vittata.…”

Section: Introductionmentioning

confidence: 99%

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Microbial community composition in the rhizosphere of Pteris vittata and its effects on arsenic phytoremediation under a natural arsenic contamination gradient

Jia

Zhang

et al. 2022

Front. Microbiol.

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Arsenic contamination causes numerous health problems for humans and wildlife via bioaccumulation in the food chain. Phytoremediation of arsenic-contaminated soils with the model arsenic hyperaccumulator Pteris vittata provides a promising way to reduce the risk, in which the growth and arsenic absorption ability of plants and the biotransformation of soil arsenic may be greatly affected by rhizosphere microorganisms. However, the microbial community composition in the rhizosphere of P. vittata and its functional role in arsenic phytoremediation are still poorly understood. To bridge this knowledge gap, we carried out a field investigation and pot experiment to explore the composition and functional implications of microbial communities in the rhizosphere of four P. vittata populations with a natural arsenic contamination gradient. Arsenic pollution significantly reduced bacterial and fungal diversity in the rhizosphere of P. vittata (p < 0.05) and played an important role in shaping the microbial community structure. The suitability of soil microbes for the growth of P. vittata gradually decreased following increased soil arsenic levels, as indicated by the increased abundance of pathogenic fungi and parasitic bacteria and the decrease in symbiotic fungi. The analysis of arsenic-related functional gene abundance with AsChip revealed the gradual enrichment of the microbial genes involved in As(III) oxidation, As(V) reduction, and arsenic methylation and demethylation in the rhizosphere of P. vittata following increased arsenic levels (p < 0.05). The regulation of indigenous soil microbes through the field application of fungicide, but not bactericide, significantly reduced the remediation efficiency of P. vittata grown under an arsenic contamination gradient, indicating the important role of indigenous fungal groups in the remediation of arsenic-contaminated soil. This study has important implications for the functional role and application prospects of soil microorganisms in the phytoremediation of arsenic-polluted soil.

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Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Microbial community composition in the rhizosphere of Pteris vittata and its effects on arsenic phytoremediation under a natural arsenic contamination gradient

Jia

Zhang

et al. 2022

Front. Microbiol.

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“…The current results showed that the OTUs could be classified into two groups, those in the rhizosphere and those in the bulk soils, in both the AE and the NAE of S. alfredii ( Figure 2 ). Importantly, the rhizosphere soil-enriched OTUs were mainly identified as fast-growing bacteria that use various carbon sources, whereas the bulk soil-enriched OTUs were mainly identified as slow-growing bacteria that use only a few carbon sources ( Leff et al, 2015 ; Xiao et al, 2021a ). This result was agreed to prior work that plant roots recruit microorganisms from the associated bulk soils on the basis of their lifestyles ( Leff et al, 2015 ).…”

Section: Discussionmentioning

confidence: 99%

The rhizosphere microbiome improves the adaptive capabilities of plants under high soil cadmium conditions

Fan

Deng²,

Shao³

et al. 2022

Front. Plant Sci.

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Cadmium (Cd) contamination of agricultural soils poses a potential public health issue for humans. Phytoremediation-based accumulating plants are an effective and sustainable technology for Cadmium remediation of contaminated agricultural soil. The rhizosphere microbiome can promote the growth and Cadmium accumulation in hyperaccumulators, but its taxonomic and functional traits remain elusive. The present study used two ecotypes of Sedum alfredii, an accumulating ecotype (AE) and a non-accumulating ecotype (NAE), as model plants to investigate the rhizosphere microbiome assemblages and influence on plant growth under high cadmium conditions. Our results showed that distinct root microbiomes assembled in association with both ecotypes of S. alfredii and that the assemblages were based largely on the lifestyles of the two ecotypes. In addition, we demonstrated that the functions of the microbes inhabiting the rhizosphere soils were closely associated with root-microbe interactions in both ecotypes of S. alfredii. Importantly, our results also demonstrated that the rhizosphere microbiome assembled in the AE rhizosphere soils contributed to plant growth and cadmium uptake under high cadmium conditions through functions such as nitrogen fixation, phosphorus solubilization, indole acetic acid (IAA) synthesis, and siderophore metabolism. However, this phenomenon was not clearly observed in the NAE. Our results suggest that the rhizosphere microbiome plays important roles in biogeochemical nutrient and metal cycling that can contribute to host plant fitness.

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“…Phytoextraction, the use of metal (hyper)accumulating plants to remove metal(loid)s from soils by concentrating them in the harvestable parts, has been proven as an eco-friendly and cost-effective alternative to remediate contaminated soils [33] and has received global attention due to its potential to restore soil quality and some functional capacities [34,35]. Moreover, a growing number of studies have shown that the association of hyperaccumulators with different microbial communities results in contrasting phytoremediation ability [36][37][38]. As a result, the metal hyperaccumulating plant has emerged as a model for disentangling the links between core microbiomes and plant functional characteristics, such as plant uptake and accumulation of heavy metals.…”

Section: Introductionmentioning

confidence: 99%

Host signature as major driver of root and rhizosphere core microbiomes that differently affect plant functional traits

Luo,

Wang,

Zhang

et al. 2023

Preprint

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BackgroundPlant can evolve with a core root microbiome that maintains essential functions for host performance. However, the relative importance of plant traits and soil factors on the structure, assembly, co-occurrence networks of the core root microbiomes and their relevance for plant characteristics remain elusive. Here, we investigated how plant species identity and soil environment affect the core bacterial communities in the bulk soil, rhizosphere and root endosphere of four plants with a gradient of Cd/Zn accumulation capacity under controlled and field environments. We further tested on the role of the core bacterial isolates in plant growth and accumulation of metal and nutrients.ResultsWe identified root compartment and plant species rather than environmental parameters as the primary driver of Cd-accumulator root microbiome. Stochastic processes were more important for the assembly of endosphere generalists (58.5%) than rhizosphere counterparts (45.2%), indicating that generalists were more robust to environmental changes. Increasing host selection from epiphytes to endophytes resulted in the existence of the endosphere and rhizosphere generalist core microbiota common to different plants under varying growth environments, highlighting that shared environmental and physiological features of host plants are decisive for core microbiome establishment. Further, endophytic core microbiota conferred greater biotic connectivity within networks and was more important predictors of plant metal accumulation, whereas the rhizosphere cores were more closely linked to plant biomass and nutrient status. The divergent functions of rhizosphere and endosphere core microbes on plant characteristics were also validated by inoculating the synthetic communities comprising bacterial isolates belonging to the core microbiota.ConclusionThis study indicated the pivotal role of plant trait in the assembly of conserved and functionally important core microbiome common to different Cd-accumulators, which brings us closer to manipulating the persistent root microbial associations to accelerate the rejuvenation of metal-disturbed soils through host genetics.

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Root microbiome assembly of As‐hyperaccumulator Pteris vittata and its efficacy in arsenic requisition

Cited by 30 publications

References 90 publications

Microbial community composition in the rhizosphere of Pteris vittata and its effects on arsenic phytoremediation under a natural arsenic contamination gradient

Microbial community composition in the rhizosphere of Pteris vittata and its effects on arsenic phytoremediation under a natural arsenic contamination gradient

The rhizosphere microbiome improves the adaptive capabilities of plants under high soil cadmium conditions

Host signature as major driver of root and rhizosphere core microbiomes that differently affect plant functional traits

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