Combined Application of High-Throughput Sequencing and Metabolomics to Evaluate the Microbial Mechanisms of Plant-Growth-Promoting Bacteria in Enhancing the Remediation of Cd-Contaminated Soil by Hybrid Pennisetum

The contamination of soil with the heavy metal cadmium (Cd) is increasingly prominent and severely threatens food security in China. Owing to its low cost, suitable efficacy, and ability to address the shortcomings of plant remediation by enhancing the ability of plants to take up Cd, plant–microbe...

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Main Authors: Shan-Shan Gao, Ying-Jun Zhang, Yang Shao, B. Larry Li, Han Liu, Yu-Ying Li, Xue-Min Ren, Zhao-Jin Chen
Format: Article
Language:English
Published: MDPI AG 2024-10-01
Series:Agronomy
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Online Access:https://www.mdpi.com/2073-4395/14/10/2348
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author Shan-Shan Gao
Ying-Jun Zhang
Yang Shao
B. Larry Li
Han Liu
Yu-Ying Li
Xue-Min Ren
Zhao-Jin Chen
author_facet Shan-Shan Gao
Ying-Jun Zhang
Yang Shao
B. Larry Li
Han Liu
Yu-Ying Li
Xue-Min Ren
Zhao-Jin Chen
author_sort Shan-Shan Gao
collection DOAJ
description The contamination of soil with the heavy metal cadmium (Cd) is increasingly prominent and severely threatens food security in China. Owing to its low cost, suitable efficacy, and ability to address the shortcomings of plant remediation by enhancing the ability of plants to take up Cd, plant–microbe combination remediation technology has become a research hotspot in heavy metal pollution remediation. A pot experiment was performed to examine the effects of inoculation with the plant-growth-promoting bacterium <i>Brevibacillus</i> sp. SR-9 on the biomass, Cd accumulation, and soil nutrients of hybrid Pennisetum. The purpose of this study was to determine how <i>Brevibacillus</i> sp. SR-9 alleviates stress caused by heavy metal contamination. High-throughput sequencing and metabolomics were used to determine the effects of inoculation on the soil bacterial community composition and microbial metabolic functions associated with hybrid Pennisetum. The results suggest that mutation of <i>Brevibacillus</i> sp. SR-9 effectively alleviates Cd pollution stress, leading to increased biomass and accumulation of Cd in hybrid Pennisetum. The aboveground biomass and the root weight increased by 12.08% and 27.03%, respectively. Additionally, the accumulation of Cd in the aboveground sections and roots increased by 21.16% and 15.50%, respectively. Measurements of the physicochemical properties of the soil revealed that the strain <i>Brevibacillus</i> sp. SR-9 slightly increased the levels of available phosphorus, total nitrogen, total phosphorus, and available potassium. High-throughput DNA sequencing revealed that <i>Brevibacillus</i> sp. SR-9 implantation modified the composition of the soil bacterial community by increasing the average number of Actinobacteria and <i>Bacillus</i>. The total nitrogen content of the soil was positively correlated with the Actinobacteria abundance, total phosphorus level, and available phosphorus level. Metabolomic analysis revealed that inoculation affected the abundance of soil metabolites, and 59 differentially abundant metabolites were identified (<i>p</i> < 0.05). Among these, 14 metabolites presented increased abundance, whereas 45 metabolites presented decreased abundance. Fourteen metabolic pathways were enriched in these metabolites: the folate resistance pathway, the ABC transporter pathway, D-glutamine and D-glutamic acid metabolism, purine metabolism, and pyrimidine metabolism. The abundance of the metabolites was positively correlated with the levels of available phosphorus, total potassium, total phosphorus, and total nitrogen. According to correlation analyses, the development of hybrid Pennisetum and the accumulation of Cd are strongly associated with differentially abundant metabolites, which also impact the abundance of certain bacterial populations. This work revealed that by altering the makeup of microbial communities and their metabolic processes, bacteria that promote plant development can mitigate the stress caused by Cd. These findings reveal the microbiological mechanisms through which these bacteria increase the ability of hybrid Pennisetum to take up the Cd present in contaminated soils.
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spelling doaj-art-dc4ba11c5e624e29b02fa344e2e234b02025-08-20T02:10:57ZengMDPI AGAgronomy2073-43952024-10-011410234810.3390/agronomy14102348Combined Application of High-Throughput Sequencing and Metabolomics to Evaluate the Microbial Mechanisms of Plant-Growth-Promoting Bacteria in Enhancing the Remediation of Cd-Contaminated Soil by Hybrid PennisetumShan-Shan Gao0Ying-Jun Zhang1Yang Shao2B. Larry Li3Han Liu4Yu-Ying Li5Xue-Min Ren6Zhao-Jin Chen7College of Water Resource and Modern Agriculture, Nanyang Normal University, Nanyang 473061, ChinaCollege of Water Resource and Modern Agriculture, Nanyang Normal University, Nanyang 473061, ChinaCollege of Water Resource and Modern Agriculture, Nanyang Normal University, Nanyang 473061, ChinaOverseas Expertise Introduction Center for Discipline Innovation of Watershed Ecological Security in the Water Source Area of the Mid-Line Project of South-to-North Water Diversion, Nanyang 473061, ChinaCollege of Water Resource and Modern Agriculture, Nanyang Normal University, Nanyang 473061, ChinaOverseas Expertise Introduction Center for Discipline Innovation of Watershed Ecological Security in the Water Source Area of the Mid-Line Project of South-to-North Water Diversion, Nanyang 473061, ChinaCollege of Water Resource and Modern Agriculture, Nanyang Normal University, Nanyang 473061, ChinaOverseas Expertise Introduction Center for Discipline Innovation of Watershed Ecological Security in the Water Source Area of the Mid-Line Project of South-to-North Water Diversion, Nanyang 473061, ChinaThe contamination of soil with the heavy metal cadmium (Cd) is increasingly prominent and severely threatens food security in China. Owing to its low cost, suitable efficacy, and ability to address the shortcomings of plant remediation by enhancing the ability of plants to take up Cd, plant–microbe combination remediation technology has become a research hotspot in heavy metal pollution remediation. A pot experiment was performed to examine the effects of inoculation with the plant-growth-promoting bacterium <i>Brevibacillus</i> sp. SR-9 on the biomass, Cd accumulation, and soil nutrients of hybrid Pennisetum. The purpose of this study was to determine how <i>Brevibacillus</i> sp. SR-9 alleviates stress caused by heavy metal contamination. High-throughput sequencing and metabolomics were used to determine the effects of inoculation on the soil bacterial community composition and microbial metabolic functions associated with hybrid Pennisetum. The results suggest that mutation of <i>Brevibacillus</i> sp. SR-9 effectively alleviates Cd pollution stress, leading to increased biomass and accumulation of Cd in hybrid Pennisetum. The aboveground biomass and the root weight increased by 12.08% and 27.03%, respectively. Additionally, the accumulation of Cd in the aboveground sections and roots increased by 21.16% and 15.50%, respectively. Measurements of the physicochemical properties of the soil revealed that the strain <i>Brevibacillus</i> sp. SR-9 slightly increased the levels of available phosphorus, total nitrogen, total phosphorus, and available potassium. High-throughput DNA sequencing revealed that <i>Brevibacillus</i> sp. SR-9 implantation modified the composition of the soil bacterial community by increasing the average number of Actinobacteria and <i>Bacillus</i>. The total nitrogen content of the soil was positively correlated with the Actinobacteria abundance, total phosphorus level, and available phosphorus level. Metabolomic analysis revealed that inoculation affected the abundance of soil metabolites, and 59 differentially abundant metabolites were identified (<i>p</i> < 0.05). Among these, 14 metabolites presented increased abundance, whereas 45 metabolites presented decreased abundance. Fourteen metabolic pathways were enriched in these metabolites: the folate resistance pathway, the ABC transporter pathway, D-glutamine and D-glutamic acid metabolism, purine metabolism, and pyrimidine metabolism. The abundance of the metabolites was positively correlated with the levels of available phosphorus, total potassium, total phosphorus, and total nitrogen. According to correlation analyses, the development of hybrid Pennisetum and the accumulation of Cd are strongly associated with differentially abundant metabolites, which also impact the abundance of certain bacterial populations. This work revealed that by altering the makeup of microbial communities and their metabolic processes, bacteria that promote plant development can mitigate the stress caused by Cd. These findings reveal the microbiological mechanisms through which these bacteria increase the ability of hybrid Pennisetum to take up the Cd present in contaminated soils.https://www.mdpi.com/2073-4395/14/10/2348cadmiumplant–microbe remediationhybrid Pennisetumbacterial communitymetabolomics
spellingShingle Shan-Shan Gao
Ying-Jun Zhang
Yang Shao
B. Larry Li
Han Liu
Yu-Ying Li
Xue-Min Ren
Zhao-Jin Chen
Combined Application of High-Throughput Sequencing and Metabolomics to Evaluate the Microbial Mechanisms of Plant-Growth-Promoting Bacteria in Enhancing the Remediation of Cd-Contaminated Soil by Hybrid Pennisetum
Agronomy
cadmium
plant–microbe remediation
hybrid Pennisetum
bacterial community
metabolomics
title Combined Application of High-Throughput Sequencing and Metabolomics to Evaluate the Microbial Mechanisms of Plant-Growth-Promoting Bacteria in Enhancing the Remediation of Cd-Contaminated Soil by Hybrid Pennisetum
title_full Combined Application of High-Throughput Sequencing and Metabolomics to Evaluate the Microbial Mechanisms of Plant-Growth-Promoting Bacteria in Enhancing the Remediation of Cd-Contaminated Soil by Hybrid Pennisetum
title_fullStr Combined Application of High-Throughput Sequencing and Metabolomics to Evaluate the Microbial Mechanisms of Plant-Growth-Promoting Bacteria in Enhancing the Remediation of Cd-Contaminated Soil by Hybrid Pennisetum
title_full_unstemmed Combined Application of High-Throughput Sequencing and Metabolomics to Evaluate the Microbial Mechanisms of Plant-Growth-Promoting Bacteria in Enhancing the Remediation of Cd-Contaminated Soil by Hybrid Pennisetum
title_short Combined Application of High-Throughput Sequencing and Metabolomics to Evaluate the Microbial Mechanisms of Plant-Growth-Promoting Bacteria in Enhancing the Remediation of Cd-Contaminated Soil by Hybrid Pennisetum
title_sort combined application of high throughput sequencing and metabolomics to evaluate the microbial mechanisms of plant growth promoting bacteria in enhancing the remediation of cd contaminated soil by hybrid pennisetum
topic cadmium
plant–microbe remediation
hybrid Pennisetum
bacterial community
metabolomics
url https://www.mdpi.com/2073-4395/14/10/2348
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