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Weak magnetic field promotes denitrification by stimulating ferromagnetic ion-containing metalloprotein expression

•Denitrification is sustained by magnetic field stimulus under decreasing C:N ratios.•Magnetic field specifically enhances ferromagnetic ion-containing protein expression.•Genome-centric metaproteomics reveals taxon-specific responses to magnetic field.•Magnetic field shows intensity-dependent selec...

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Published in:Water research (Oxford) 2024-09, Vol.262, p.122116, Article 122116
Main Authors: Lin, Yuan, Chen, Yanting, Wang, Haiyue, Yu, Yuexin, Wang, Yanru, Ma, Sijia, Wang, Laichun, Ren, Hongqiang, Xu, Ke
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container_title Water research (Oxford)
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Chen, Yanting
Wang, Haiyue
Yu, Yuexin
Wang, Yanru
Ma, Sijia
Wang, Laichun
Ren, Hongqiang
Xu, Ke
description •Denitrification is sustained by magnetic field stimulus under decreasing C:N ratios.•Magnetic field specifically enhances ferromagnetic ion-containing protein expression.•Genome-centric metaproteomics reveals taxon-specific responses to magnetic field.•Magnetic field shows intensity-dependent selective pressure on microbial composition. Weak magnetic field (WMF) has been recognized to promote biological denitrification processes; however, the underlying mechanisms remain largely unexplored, hindering the optimization of its effectiveness. Here, we systematically investigated the effects of WMF on denitrification performance, enzyme activity, microbial community, and metaproteome in packed bed bioreactors treating high nitrate wastewater under different WMF intensities and C:N ratios. Results showed that WMFs significantly promoted denitrification by consistently stimulating the activities of denitrifying reductases and NAD+/NADH biosynthesis across decreasing C:N ratios. Reductases and electron transfer enzymes involved in denitrification were overproduced due to the significantly enriched overexpression of ferromagnetic ion-containing (FIC) metalloproteins. We also observed WMFs’ intensity-dependent selective pressure on microbial community structures despite the effects being limited compared to those caused by changing C:N ratios. By coupling genome-centric metaproteomics and structure prediction, we found the dominant denitrifier, Halomonas, was outcompeted by Pseudomonas and Azoarcus under WMFs, likely due to its structural deficiencies in iron uptake, suggesting that advantageous ferromagnetic ion acquisition capacity was necessary to satisfy the substrate demand for FIC metalloprotein overproduction. This study advances our understanding of the biomagnetic effects in the context of complex communities and highlights WMF's potential for manipulating FIC protein-associated metabolism and fine-tuning community structure. [Display omitted]
doi_str_mv 10.1016/j.watres.2024.122116
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Weak magnetic field (WMF) has been recognized to promote biological denitrification processes; however, the underlying mechanisms remain largely unexplored, hindering the optimization of its effectiveness. Here, we systematically investigated the effects of WMF on denitrification performance, enzyme activity, microbial community, and metaproteome in packed bed bioreactors treating high nitrate wastewater under different WMF intensities and C:N ratios. Results showed that WMFs significantly promoted denitrification by consistently stimulating the activities of denitrifying reductases and NAD+/NADH biosynthesis across decreasing C:N ratios. Reductases and electron transfer enzymes involved in denitrification were overproduced due to the significantly enriched overexpression of ferromagnetic ion-containing (FIC) metalloproteins. We also observed WMFs’ intensity-dependent selective pressure on microbial community structures despite the effects being limited compared to those caused by changing C:N ratios. By coupling genome-centric metaproteomics and structure prediction, we found the dominant denitrifier, Halomonas, was outcompeted by Pseudomonas and Azoarcus under WMFs, likely due to its structural deficiencies in iron uptake, suggesting that advantageous ferromagnetic ion acquisition capacity was necessary to satisfy the substrate demand for FIC metalloprotein overproduction. This study advances our understanding of the biomagnetic effects in the context of complex communities and highlights WMF's potential for manipulating FIC protein-associated metabolism and fine-tuning community structure. [Display omitted]</description><identifier>ISSN: 0043-1354</identifier><identifier>ISSN: 1879-2448</identifier><identifier>EISSN: 1879-2448</identifier><identifier>DOI: 10.1016/j.watres.2024.122116</identifier><identifier>PMID: 39032337</identifier><language>eng</language><publisher>England: Elsevier Ltd</publisher><subject>Advanced denitrification ; Azoarcus ; Biomagnetic effect ; Bioreactors ; biosynthesis ; community structure ; Denitrification ; denitrifying microorganisms ; electron transfer ; enzyme activity ; ferromagnetism ; Genome-centric metaproteomics ; Halomonas ; Magnetic Fields ; Metalloprotein ; metalloproteins ; Metalloproteins - metabolism ; microbial communities ; nitrates ; oxidoreductases ; prediction ; Pseudomonas ; wastewater ; Wastewater - chemistry ; water</subject><ispartof>Water research (Oxford), 2024-09, Vol.262, p.122116, Article 122116</ispartof><rights>2024 Elsevier Ltd</rights><rights>Copyright © 2024 Elsevier Ltd. 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Weak magnetic field (WMF) has been recognized to promote biological denitrification processes; however, the underlying mechanisms remain largely unexplored, hindering the optimization of its effectiveness. Here, we systematically investigated the effects of WMF on denitrification performance, enzyme activity, microbial community, and metaproteome in packed bed bioreactors treating high nitrate wastewater under different WMF intensities and C:N ratios. Results showed that WMFs significantly promoted denitrification by consistently stimulating the activities of denitrifying reductases and NAD+/NADH biosynthesis across decreasing C:N ratios. Reductases and electron transfer enzymes involved in denitrification were overproduced due to the significantly enriched overexpression of ferromagnetic ion-containing (FIC) metalloproteins. We also observed WMFs’ intensity-dependent selective pressure on microbial community structures despite the effects being limited compared to those caused by changing C:N ratios. By coupling genome-centric metaproteomics and structure prediction, we found the dominant denitrifier, Halomonas, was outcompeted by Pseudomonas and Azoarcus under WMFs, likely due to its structural deficiencies in iron uptake, suggesting that advantageous ferromagnetic ion acquisition capacity was necessary to satisfy the substrate demand for FIC metalloprotein overproduction. This study advances our understanding of the biomagnetic effects in the context of complex communities and highlights WMF's potential for manipulating FIC protein-associated metabolism and fine-tuning community structure. [Display omitted]</description><subject>Advanced denitrification</subject><subject>Azoarcus</subject><subject>Biomagnetic effect</subject><subject>Bioreactors</subject><subject>biosynthesis</subject><subject>community structure</subject><subject>Denitrification</subject><subject>denitrifying microorganisms</subject><subject>electron transfer</subject><subject>enzyme activity</subject><subject>ferromagnetism</subject><subject>Genome-centric metaproteomics</subject><subject>Halomonas</subject><subject>Magnetic Fields</subject><subject>Metalloprotein</subject><subject>metalloproteins</subject><subject>Metalloproteins - metabolism</subject><subject>microbial communities</subject><subject>nitrates</subject><subject>oxidoreductases</subject><subject>prediction</subject><subject>Pseudomonas</subject><subject>wastewater</subject><subject>Wastewater - chemistry</subject><subject>water</subject><issn>0043-1354</issn><issn>1879-2448</issn><issn>1879-2448</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2024</creationdate><recordtype>article</recordtype><recordid>eNqFkUlLxDAYhoMoOi7_QKRHLx2zNWkugogbCF4UjyFNv0rGNh2TjMu_N0NHj3oKIc_7LXkQOiZ4TjARZ4v5h0kB4pxiyueEUkLEFpqRWqqScl5voxnGnJWEVXwP7ce4wBhTytQu2mMKM8qYnKHwDOa1GMyLh-Rs0Tno22IZxmFMEIsWvEvBdc6a5EZfNF9FTG5Y9fnqX4oOQiZ_shko7eiTcX79OEAyfT_mWgmcL-BzmYeNGTpEO53pIxxtzgP0dH31eHlb3j_c3F1e3JeWSp5KWVMhmelqYau6UYRWgteNyMsq2mLWCIIb6KrW5mUlphmQxFqbU5RRJTk7QKdT3TzC2wpi0oOLFvreeBhXUTNSMSErVYn_UVwzSrhSdUb5hNowxhig08vgBhO-NMF6LUYv9CRGr8XoSUyOnWw6rJoB2t_Qj4kMnE8A5C95dxB0tA68hdYFsEm3o_u7wzek2aHx</recordid><startdate>20240915</startdate><enddate>20240915</enddate><creator>Lin, Yuan</creator><creator>Chen, Yanting</creator><creator>Wang, Haiyue</creator><creator>Yu, Yuexin</creator><creator>Wang, Yanru</creator><creator>Ma, Sijia</creator><creator>Wang, Laichun</creator><creator>Ren, Hongqiang</creator><creator>Xu, Ke</creator><general>Elsevier Ltd</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7X8</scope><scope>7S9</scope><scope>L.6</scope></search><sort><creationdate>20240915</creationdate><title>Weak magnetic field promotes denitrification by stimulating ferromagnetic ion-containing metalloprotein expression</title><author>Lin, Yuan ; 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Weak magnetic field (WMF) has been recognized to promote biological denitrification processes; however, the underlying mechanisms remain largely unexplored, hindering the optimization of its effectiveness. Here, we systematically investigated the effects of WMF on denitrification performance, enzyme activity, microbial community, and metaproteome in packed bed bioreactors treating high nitrate wastewater under different WMF intensities and C:N ratios. Results showed that WMFs significantly promoted denitrification by consistently stimulating the activities of denitrifying reductases and NAD+/NADH biosynthesis across decreasing C:N ratios. Reductases and electron transfer enzymes involved in denitrification were overproduced due to the significantly enriched overexpression of ferromagnetic ion-containing (FIC) metalloproteins. 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subjects Advanced denitrification
Azoarcus
Biomagnetic effect
Bioreactors
biosynthesis
community structure
Denitrification
denitrifying microorganisms
electron transfer
enzyme activity
ferromagnetism
Genome-centric metaproteomics
Halomonas
Magnetic Fields
Metalloprotein
metalloproteins
Metalloproteins - metabolism
microbial communities
nitrates
oxidoreductases
prediction
Pseudomonas
wastewater
Wastewater - chemistry
water
title Weak magnetic field promotes denitrification by stimulating ferromagnetic ion-containing metalloprotein expression
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