Biochemical and multi-omics analyses of response mechanisms of rhizobacteria to long-term copper and salt stress: Effect on soil physicochemical properties and growth of Avicennia marina

Mangroves are of important economic and environmental value and research suggests that their carbon sequestration and climate change mitigation potential is significantly larger than other forests. However, increasing salinity and heavy metal pollution significantly affect mangrove ecosystem functio...

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Veröffentlicht in:Journal of hazardous materials 2024-03, Vol.466, p.133601, Article 133601
Hauptverfasser: Shang, Chenjing, Chen, Jiawen, Nkoh, Jackson Nkoh, Wang, Junjie, Chen, Si, Hu, Zhangli, Hussain, Quaid
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container_start_page 133601
container_title Journal of hazardous materials
container_volume 466
creator Shang, Chenjing
Chen, Jiawen
Nkoh, Jackson Nkoh
Wang, Junjie
Chen, Si
Hu, Zhangli
Hussain, Quaid
description Mangroves are of important economic and environmental value and research suggests that their carbon sequestration and climate change mitigation potential is significantly larger than other forests. However, increasing salinity and heavy metal pollution significantly affect mangrove ecosystem function and productivity. This study investigates the tolerance mechanisms of rhizobacteria in the rhizosphere of Avicennia marina under salinity and copper (Cu) stress during a 4-y stress period. The results exhibited significant differences in antioxidant levels, transcripts, and secondary metabolites. Under salt stress, the differentially expressed metabolites consisted of 30% organic acids, 26.78% nucleotides, 16.67% organic heterocyclic compounds, and 10% organic oxides as opposed to 27.27% organic acids, 24.24% nucleotides, 15.15% organic heterocyclic compounds, and 12.12% phenyl propane and polyketides under Cu stress. This resulted in differential regulation of metabolic pathways, with phenylpropanoid biosynthesis being unique to Cu stress and alanine/aspartate/glutamate metabolism and α-linolenic acid metabolism being unique to salt stress. The regulation of metabolic pathways enhanced antioxidant defenses, nutrient recycling, accumulation of osmoprotectants, stability of plasma membrane, and chelation of Cu, thereby improving the stress tolerance of rhizobacteria and A. marina. Even though the abundance and community structure of rhizobacteria were significantly changed, all the samples were dominated by Proteobacteria, Chloroflexi, Actinobacteriota, and Firmicutes. Since the response mechanisms were unbalanced between treatments, this led to differential growth trends for A. marina. Our study provides valuable inside on variations in diversity and composition of bacterial community structure from mangrove rhizosphere subjected to long-term salt and Cu stress. It also clarifies rhizobacterial adaptive mechanisms to these stresses and how they are important for mitigating abiotic stress and promoting plant growth. Therefore, this study can serve as a reference for future research aimed at developing long-term management practices for mangrove forests. [Display omitted] •Salt-copper (Cu) stress decreased bacterial abundance but increased diversity.•Low and high salt stress significantly increased bacterial abundance.•High salt stress significantly downregulated the content of free amino acids in the rhizosphere.•High Cu and salt-Cu stress promoted N reduction
doi_str_mv 10.1016/j.jhazmat.2024.133601
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However, increasing salinity and heavy metal pollution significantly affect mangrove ecosystem function and productivity. This study investigates the tolerance mechanisms of rhizobacteria in the rhizosphere of Avicennia marina under salinity and copper (Cu) stress during a 4-y stress period. The results exhibited significant differences in antioxidant levels, transcripts, and secondary metabolites. Under salt stress, the differentially expressed metabolites consisted of 30% organic acids, 26.78% nucleotides, 16.67% organic heterocyclic compounds, and 10% organic oxides as opposed to 27.27% organic acids, 24.24% nucleotides, 15.15% organic heterocyclic compounds, and 12.12% phenyl propane and polyketides under Cu stress. This resulted in differential regulation of metabolic pathways, with phenylpropanoid biosynthesis being unique to Cu stress and alanine/aspartate/glutamate metabolism and α-linolenic acid metabolism being unique to salt stress. The regulation of metabolic pathways enhanced antioxidant defenses, nutrient recycling, accumulation of osmoprotectants, stability of plasma membrane, and chelation of Cu, thereby improving the stress tolerance of rhizobacteria and A. marina. Even though the abundance and community structure of rhizobacteria were significantly changed, all the samples were dominated by Proteobacteria, Chloroflexi, Actinobacteriota, and Firmicutes. Since the response mechanisms were unbalanced between treatments, this led to differential growth trends for A. marina. Our study provides valuable inside on variations in diversity and composition of bacterial community structure from mangrove rhizosphere subjected to long-term salt and Cu stress. It also clarifies rhizobacterial adaptive mechanisms to these stresses and how they are important for mitigating abiotic stress and promoting plant growth. Therefore, this study can serve as a reference for future research aimed at developing long-term management practices for mangrove forests. 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However, increasing salinity and heavy metal pollution significantly affect mangrove ecosystem function and productivity. This study investigates the tolerance mechanisms of rhizobacteria in the rhizosphere of Avicennia marina under salinity and copper (Cu) stress during a 4-y stress period. The results exhibited significant differences in antioxidant levels, transcripts, and secondary metabolites. Under salt stress, the differentially expressed metabolites consisted of 30% organic acids, 26.78% nucleotides, 16.67% organic heterocyclic compounds, and 10% organic oxides as opposed to 27.27% organic acids, 24.24% nucleotides, 15.15% organic heterocyclic compounds, and 12.12% phenyl propane and polyketides under Cu stress. This resulted in differential regulation of metabolic pathways, with phenylpropanoid biosynthesis being unique to Cu stress and alanine/aspartate/glutamate metabolism and α-linolenic acid metabolism being unique to salt stress. The regulation of metabolic pathways enhanced antioxidant defenses, nutrient recycling, accumulation of osmoprotectants, stability of plasma membrane, and chelation of Cu, thereby improving the stress tolerance of rhizobacteria and A. marina. Even though the abundance and community structure of rhizobacteria were significantly changed, all the samples were dominated by Proteobacteria, Chloroflexi, Actinobacteriota, and Firmicutes. Since the response mechanisms were unbalanced between treatments, this led to differential growth trends for A. marina. Our study provides valuable inside on variations in diversity and composition of bacterial community structure from mangrove rhizosphere subjected to long-term salt and Cu stress. It also clarifies rhizobacterial adaptive mechanisms to these stresses and how they are important for mitigating abiotic stress and promoting plant growth. Therefore, this study can serve as a reference for future research aimed at developing long-term management practices for mangrove forests. [Display omitted] •Salt-copper (Cu) stress decreased bacterial abundance but increased diversity.•Low and high salt stress significantly increased bacterial abundance.•High salt stress significantly downregulated the content of free amino acids in the rhizosphere.•High Cu and salt-Cu stress promoted N reduction function but inhibited C metabolism.•Phenylpropanoid biosynthesis was unique to copper stress.</description><subject>alanine</subject><subject>Antioxidant enzymes</subject><subject>antioxidants</subject><subject>aspartic acid</subject><subject>Avicennia marina</subject><subject>bacterial communities</subject><subject>biosynthesis</subject><subject>carbon sequestration</subject><subject>chelation</subject><subject>Chloroflexi</subject><subject>climate change</subject><subject>community structure</subject><subject>copper</subject><subject>ecological function</subject><subject>ecological value</subject><subject>Firmicutes</subject><subject>gene expression regulation</subject><subject>glutamic acid</subject><subject>Heavy metal pollution</subject><subject>heavy metals</subject><subject>heterocyclic compounds</subject><subject>mangrove ecosystems</subject><subject>Metabolome</subject><subject>multiomics</subject><subject>nucleotides</subject><subject>osmotolerance</subject><subject>plant growth</subject><subject>plasma membrane</subject><subject>pollution</subject><subject>polyketides</subject><subject>propane</subject><subject>Proteobacteria</subject><subject>rhizosphere</subject><subject>rhizosphere bacteria</subject><subject>Salinity</subject><subject>salt stress</subject><subject>secondary metabolites</subject><subject>soil</subject><subject>stress tolerance</subject><subject>Transcriptomic</subject><issn>0304-3894</issn><issn>1873-3336</issn><issn>1873-3336</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2024</creationdate><recordtype>article</recordtype><recordid>eNqFUU1v1DAQjRCILoWfAPKRSxY7dpyYCypVaZEqcendcpxJ41ViB4-3aPvT-HV4mwWOPVlv9D7G84riPaNbRpn8tNvuRvM4m7StaCW2jHNJ2Ytiw9qGlzyjl8WGcipK3ipxVrxB3FFKWVOL18UZbzlVrFab4vdXF-wIs7NmIsb3ZN5PyZUhDzBjMx0QkISBRMAleAQygx2Ndziv49E9hs7YBNEZkgKZgr8vM5qJDcsC8ckUzZQIpuyBn8nVMIBNJHiCwU1kGQ_o7P8llhiyLDnAJ-l9DL_SeIy6eHAWvM8xs4nOm7fFq8FMCO9O73lx9-3q7vKmvP1x_f3y4ra0XLWplEIyrmoLwjDZKSH7rlaiBgqWN7KWAEMjVMsHw6uatZUVfTVYM1jegVI9Py8-rrZ5sZ97wKRnhxamyXgIe9Sc1aISjRTts9RKVZI2QlY8U-uVamNAjDDoJbr8r4NmVB8L1jt9KlgfC9ZrwVn34RSx72bo_6n-NpoJX1YC5JM8OIgarQNvoXcxn133wT0T8Qe3Cb4j</recordid><startdate>20240315</startdate><enddate>20240315</enddate><creator>Shang, Chenjing</creator><creator>Chen, Jiawen</creator><creator>Nkoh, Jackson Nkoh</creator><creator>Wang, Junjie</creator><creator>Chen, Si</creator><creator>Hu, Zhangli</creator><creator>Hussain, Quaid</creator><general>Elsevier B.V</general><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7X8</scope><scope>7S9</scope><scope>L.6</scope></search><sort><creationdate>20240315</creationdate><title>Biochemical and multi-omics analyses of response mechanisms of rhizobacteria to long-term copper and salt stress: Effect on soil physicochemical properties and growth of Avicennia marina</title><author>Shang, Chenjing ; 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However, increasing salinity and heavy metal pollution significantly affect mangrove ecosystem function and productivity. This study investigates the tolerance mechanisms of rhizobacteria in the rhizosphere of Avicennia marina under salinity and copper (Cu) stress during a 4-y stress period. The results exhibited significant differences in antioxidant levels, transcripts, and secondary metabolites. Under salt stress, the differentially expressed metabolites consisted of 30% organic acids, 26.78% nucleotides, 16.67% organic heterocyclic compounds, and 10% organic oxides as opposed to 27.27% organic acids, 24.24% nucleotides, 15.15% organic heterocyclic compounds, and 12.12% phenyl propane and polyketides under Cu stress. This resulted in differential regulation of metabolic pathways, with phenylpropanoid biosynthesis being unique to Cu stress and alanine/aspartate/glutamate metabolism and α-linolenic acid metabolism being unique to salt stress. The regulation of metabolic pathways enhanced antioxidant defenses, nutrient recycling, accumulation of osmoprotectants, stability of plasma membrane, and chelation of Cu, thereby improving the stress tolerance of rhizobacteria and A. marina. Even though the abundance and community structure of rhizobacteria were significantly changed, all the samples were dominated by Proteobacteria, Chloroflexi, Actinobacteriota, and Firmicutes. Since the response mechanisms were unbalanced between treatments, this led to differential growth trends for A. marina. Our study provides valuable inside on variations in diversity and composition of bacterial community structure from mangrove rhizosphere subjected to long-term salt and Cu stress. It also clarifies rhizobacterial adaptive mechanisms to these stresses and how they are important for mitigating abiotic stress and promoting plant growth. Therefore, this study can serve as a reference for future research aimed at developing long-term management practices for mangrove forests. [Display omitted] •Salt-copper (Cu) stress decreased bacterial abundance but increased diversity.•Low and high salt stress significantly increased bacterial abundance.•High salt stress significantly downregulated the content of free amino acids in the rhizosphere.•High Cu and salt-Cu stress promoted N reduction function but inhibited C metabolism.•Phenylpropanoid biosynthesis was unique to copper stress.</abstract><cop>Netherlands</cop><pub>Elsevier B.V</pub><pmid>38309159</pmid><doi>10.1016/j.jhazmat.2024.133601</doi></addata></record>
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subjects alanine
Antioxidant enzymes
antioxidants
aspartic acid
Avicennia marina
bacterial communities
biosynthesis
carbon sequestration
chelation
Chloroflexi
climate change
community structure
copper
ecological function
ecological value
Firmicutes
gene expression regulation
glutamic acid
Heavy metal pollution
heavy metals
heterocyclic compounds
mangrove ecosystems
Metabolome
multiomics
nucleotides
osmotolerance
plant growth
plasma membrane
pollution
polyketides
propane
Proteobacteria
rhizosphere
rhizosphere bacteria
Salinity
salt stress
secondary metabolites
soil
stress tolerance
Transcriptomic
title Biochemical and multi-omics analyses of response mechanisms of rhizobacteria to long-term copper and salt stress: Effect on soil physicochemical properties and growth of Avicennia marina
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