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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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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[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><identifier>ISSN: 0304-3894</identifier><identifier>ISSN: 1873-3336</identifier><identifier>EISSN: 1873-3336</identifier><identifier>DOI: 10.1016/j.jhazmat.2024.133601</identifier><identifier>PMID: 38309159</identifier><language>eng</language><publisher>Netherlands: Elsevier B.V</publisher><subject>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</subject><ispartof>Journal of hazardous materials, 2024-03, Vol.466, p.133601, Article 133601</ispartof><rights>2024 Elsevier B.V.</rights><rights>Copyright © 2024 Elsevier B.V. All rights reserved.</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c398t-6461395ce4a16b946db5945e0ec37656eef74983fa325182c4d2fcafc3be99d3</citedby><cites>FETCH-LOGICAL-c398t-6461395ce4a16b946db5945e0ec37656eef74983fa325182c4d2fcafc3be99d3</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktohtml>$$Uhttps://www.sciencedirect.com/science/article/pii/S0304389424001808$$EHTML$$P50$$Gelsevier$$H</linktohtml><link.rule.ids>314,776,780,3537,27901,27902,65306</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/38309159$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Shang, Chenjing</creatorcontrib><creatorcontrib>Chen, Jiawen</creatorcontrib><creatorcontrib>Nkoh, Jackson Nkoh</creatorcontrib><creatorcontrib>Wang, Junjie</creatorcontrib><creatorcontrib>Chen, Si</creatorcontrib><creatorcontrib>Hu, Zhangli</creatorcontrib><creatorcontrib>Hussain, Quaid</creatorcontrib><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><title>Journal of hazardous materials</title><addtitle>J Hazard Mater</addtitle><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 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 ; Chen, Jiawen ; Nkoh, Jackson Nkoh ; Wang, Junjie ; Chen, Si ; Hu, Zhangli ; Hussain, Quaid</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c398t-6461395ce4a16b946db5945e0ec37656eef74983fa325182c4d2fcafc3be99d3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2024</creationdate><topic>alanine</topic><topic>Antioxidant enzymes</topic><topic>antioxidants</topic><topic>aspartic acid</topic><topic>Avicennia marina</topic><topic>bacterial communities</topic><topic>biosynthesis</topic><topic>carbon sequestration</topic><topic>chelation</topic><topic>Chloroflexi</topic><topic>climate change</topic><topic>community structure</topic><topic>copper</topic><topic>ecological function</topic><topic>ecological value</topic><topic>Firmicutes</topic><topic>gene expression regulation</topic><topic>glutamic acid</topic><topic>Heavy metal pollution</topic><topic>heavy metals</topic><topic>heterocyclic compounds</topic><topic>mangrove ecosystems</topic><topic>Metabolome</topic><topic>multiomics</topic><topic>nucleotides</topic><topic>osmotolerance</topic><topic>plant growth</topic><topic>plasma membrane</topic><topic>pollution</topic><topic>polyketides</topic><topic>propane</topic><topic>Proteobacteria</topic><topic>rhizosphere</topic><topic>rhizosphere bacteria</topic><topic>Salinity</topic><topic>salt stress</topic><topic>secondary metabolites</topic><topic>soil</topic><topic>stress tolerance</topic><topic>Transcriptomic</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Shang, Chenjing</creatorcontrib><creatorcontrib>Chen, Jiawen</creatorcontrib><creatorcontrib>Nkoh, Jackson Nkoh</creatorcontrib><creatorcontrib>Wang, Junjie</creatorcontrib><creatorcontrib>Chen, Si</creatorcontrib><creatorcontrib>Hu, Zhangli</creatorcontrib><creatorcontrib>Hussain, Quaid</creatorcontrib><collection>PubMed</collection><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><collection>AGRICOLA</collection><collection>AGRICOLA - Academic</collection><jtitle>Journal of hazardous materials</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Shang, Chenjing</au><au>Chen, Jiawen</au><au>Nkoh, Jackson Nkoh</au><au>Wang, Junjie</au><au>Chen, Si</au><au>Hu, Zhangli</au><au>Hussain, Quaid</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>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</atitle><jtitle>Journal of hazardous materials</jtitle><addtitle>J Hazard Mater</addtitle><date>2024-03-15</date><risdate>2024</risdate><volume>466</volume><spage>133601</spage><pages>133601-</pages><artnum>133601</artnum><issn>0304-3894</issn><issn>1873-3336</issn><eissn>1873-3336</eissn><abstract>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 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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