Integrative chemical and omics analyses reveal copper biosorption and tolerance mechanisms of Bacillus cereus strain T6

A comprehensive understanding of the cellular response of microbes to metal stress is necessary for the rational development of microbe-based biosorbents for metal removal. The present study investigated the copper (Cu) sorption and resistance mechanism of Bacillus cereus strain T6, a newly isolated...

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Veröffentlicht in:Journal of hazardous materials 2022-08, Vol.435, p.129002-129002, Article 129002
Hauptverfasser: Wu, Ping, Rane, Niraj R., Xing, Chao, Patil, Swapnil M., Roh, Hyun-Seog, Jeon, Byong-Hun, Li, Xiaofang
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container_end_page 129002
container_issue
container_start_page 129002
container_title Journal of hazardous materials
container_volume 435
creator Wu, Ping
Rane, Niraj R.
Xing, Chao
Patil, Swapnil M.
Roh, Hyun-Seog
Jeon, Byong-Hun
Li, Xiaofang
description A comprehensive understanding of the cellular response of microbes to metal stress is necessary for the rational development of microbe-based biosorbents for metal removal. The present study investigated the copper (Cu) sorption and resistance mechanism of Bacillus cereus strain T6, a newly isolated Cu-resistant bacterium, by integrative analyses of physiochemistry, genomics, transcriptomics, and metabolomics. The growth inhibition assay and biosorption determination showed that this bacterium exhibited high tolerance to Cu, with a minimum inhibitory concentration of 4.0 mM, and accumulated Cu by both extracellular adsorption and intracellular binding. SEM microscopic images and FTIR spectra showed significant cellular surface changes at the high Cu level but not at low, and the involvement of surface functional groups in the biosorption of Cu, respectively. Transcriptomic and untargeted metabolomic analyses detected 362 differentially expressed genes and 60 significantly altered metabolites, respectively. Integrative omics analyses revealed that Cu exposure dramatically induced a broad spectrum of genes involved in Cu transport and iron homeostasis, and suppressed the denitrification pathway, leading to significant accumulation of metabolites for metal transporter synthesis, membrane remolding, and antioxidant activities. The results presented here provide a new perspective on the intricate regulatory network of Cu homeostasis in bacteria. [Display omitted] •A Cu-resistant Bacillus cereus strain T6 was isolated and characterized.•Chemical and omics tools were integrated to explore its Cu resistance mechanism.•A cellular view was achieved for T6′s Cu sorption and resistance.•Cell wall structure and intracellular processes are important for T6′s Cu binding.•Cu homeostasis and denitrification pathways were drastically impacted by Cu.
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The present study investigated the copper (Cu) sorption and resistance mechanism of Bacillus cereus strain T6, a newly isolated Cu-resistant bacterium, by integrative analyses of physiochemistry, genomics, transcriptomics, and metabolomics. The growth inhibition assay and biosorption determination showed that this bacterium exhibited high tolerance to Cu, with a minimum inhibitory concentration of 4.0 mM, and accumulated Cu by both extracellular adsorption and intracellular binding. SEM microscopic images and FTIR spectra showed significant cellular surface changes at the high Cu level but not at low, and the involvement of surface functional groups in the biosorption of Cu, respectively. Transcriptomic and untargeted metabolomic analyses detected 362 differentially expressed genes and 60 significantly altered metabolites, respectively. Integrative omics analyses revealed that Cu exposure dramatically induced a broad spectrum of genes involved in Cu transport and iron homeostasis, and suppressed the denitrification pathway, leading to significant accumulation of metabolites for metal transporter synthesis, membrane remolding, and antioxidant activities. The results presented here provide a new perspective on the intricate regulatory network of Cu homeostasis in bacteria. [Display omitted] •A Cu-resistant Bacillus cereus strain T6 was isolated and characterized.•Chemical and omics tools were integrated to explore its Cu resistance mechanism.•A cellular view was achieved for T6′s Cu sorption and resistance.•Cell wall structure and intracellular processes are important for T6′s Cu binding.•Cu homeostasis and denitrification pathways were drastically impacted by Cu.</description><identifier>ISSN: 0304-3894</identifier><identifier>EISSN: 1873-3336</identifier><identifier>DOI: 10.1016/j.jhazmat.2022.129002</identifier><identifier>PMID: 35490635</identifier><language>eng</language><publisher>Netherlands: Elsevier B.V</publisher><subject>Adsorption ; Bacillus cereus - genetics ; Biosorption ; Copper - analysis ; Copper - toxicity ; Copper resistant bacterium ; Hydrogen-Ion Concentration ; Intracellular bioaccumulation ; Kinetics ; Multi-omics analysis ; Resistance mechanism</subject><ispartof>Journal of hazardous materials, 2022-08, Vol.435, p.129002-129002, Article 129002</ispartof><rights>2022 Elsevier B.V.</rights><rights>Copyright © 2022 Elsevier B.V. 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The present study investigated the copper (Cu) sorption and resistance mechanism of Bacillus cereus strain T6, a newly isolated Cu-resistant bacterium, by integrative analyses of physiochemistry, genomics, transcriptomics, and metabolomics. The growth inhibition assay and biosorption determination showed that this bacterium exhibited high tolerance to Cu, with a minimum inhibitory concentration of 4.0 mM, and accumulated Cu by both extracellular adsorption and intracellular binding. SEM microscopic images and FTIR spectra showed significant cellular surface changes at the high Cu level but not at low, and the involvement of surface functional groups in the biosorption of Cu, respectively. Transcriptomic and untargeted metabolomic analyses detected 362 differentially expressed genes and 60 significantly altered metabolites, respectively. Integrative omics analyses revealed that Cu exposure dramatically induced a broad spectrum of genes involved in Cu transport and iron homeostasis, and suppressed the denitrification pathway, leading to significant accumulation of metabolites for metal transporter synthesis, membrane remolding, and antioxidant activities. The results presented here provide a new perspective on the intricate regulatory network of Cu homeostasis in bacteria. 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subjects Adsorption
Bacillus cereus - genetics
Biosorption
Copper - analysis
Copper - toxicity
Copper resistant bacterium
Hydrogen-Ion Concentration
Intracellular bioaccumulation
Kinetics
Multi-omics analysis
Resistance mechanism
title Integrative chemical and omics analyses reveal copper biosorption and tolerance mechanisms of Bacillus cereus strain T6
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