Intrinsic enzyme‐like activity of magnetite particles is enhanced by cultivation with Trichoderma guizhouense

Summary Fungal–mineral interactions can produce large amounts of biogenic nano‐size (~ 1–100 nm) minerals, yet their influence on fungal physiology and growth remains largely unexplored. Using Trichoderma guizhouense NJAU4742 and magnetite (Mt) as a model fungus and mineral system, we have shown for...

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Veröffentlicht in:Environmental microbiology 2021-02, Vol.23 (2), p.893-907
Hauptverfasser: Chi, Zhi‐Lai, Zhao, Xiang‐Yang, Chen, Ya‐Ling, Hao, Jia‐Long, Yu, Guang‐Hui, Goodman, Bernard A., Gadd, Geoffrey Michael
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container_end_page 907
container_issue 2
container_start_page 893
container_title Environmental microbiology
container_volume 23
creator Chi, Zhi‐Lai
Zhao, Xiang‐Yang
Chen, Ya‐Ling
Hao, Jia‐Long
Yu, Guang‐Hui
Goodman, Bernard A.
Gadd, Geoffrey Michael
description Summary Fungal–mineral interactions can produce large amounts of biogenic nano‐size (~ 1–100 nm) minerals, yet their influence on fungal physiology and growth remains largely unexplored. Using Trichoderma guizhouense NJAU4742 and magnetite (Mt) as a model fungus and mineral system, we have shown for the first time that biogenic Mt nanoparticles formed during fungal–mineral cultivation exhibit intrinsic peroxidase‐like activity. Specifically, the average peroxidase‐like activity of Mt nanoparticles after 72 h cultivation was ~ 2.4 times higher than that of the original Mt. Evidence from high resolution X‐ray photoelectron spectroscopy analyses indicated that the unique properties of magnetite nanoparticles largely stemmed from their high proportion of surface non‐lattice oxygen, through occupying surface oxygen‐vacant sites, rather than Fe redox chemistry, which challenges conventional Fenton reaction theories that assume iron to be the sole redox‐active centre. Nanoscale secondary ion mass spectrometry with a resolution down to 50 nm demonstrated that a thin (
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Using Trichoderma guizhouense NJAU4742 and magnetite (Mt) as a model fungus and mineral system, we have shown for the first time that biogenic Mt nanoparticles formed during fungal–mineral cultivation exhibit intrinsic peroxidase‐like activity. Specifically, the average peroxidase‐like activity of Mt nanoparticles after 72 h cultivation was ~ 2.4 times higher than that of the original Mt. Evidence from high resolution X‐ray photoelectron spectroscopy analyses indicated that the unique properties of magnetite nanoparticles largely stemmed from their high proportion of surface non‐lattice oxygen, through occupying surface oxygen‐vacant sites, rather than Fe redox chemistry, which challenges conventional Fenton reaction theories that assume iron to be the sole redox‐active centre. Nanoscale secondary ion mass spectrometry with a resolution down to 50 nm demonstrated that a thin (&lt; 1 μm) oxygen‐film was present on the surface of fungal hyphae. Furthermore, synchrotron radiation‐based micro‐FTIR spectra revealed that surface oxygen groups corresponded mainly to organic OH, mineral OH and carbonyl groups. Together, these findings highlight an important, but unrecognized, catalytic activity of mineral nanoparticles produced by fungal–mineral interactions and contribute substantially to our understanding of mineral nanoparticles in natural ecosystems.</description><identifier>ISSN: 1462-2912</identifier><identifier>EISSN: 1462-2920</identifier><identifier>DOI: 10.1111/1462-2920.15193</identifier><identifier>PMID: 32783346</identifier><language>eng</language><publisher>Hoboken, USA: John Wiley &amp; Sons, Inc</publisher><subject>Analytical methods ; Carbonyl compounds ; Carbonyl groups ; Carbonyls ; Catalytic activity ; Cultivation ; Fungi ; Hyphae ; Iron ; Magnetic properties ; Magnetite ; Mass spectrometry ; Mass spectroscopy ; Minerals ; Nanoparticles ; Oxidoreductions ; Oxygen ; Peroxidase ; Photoelectron spectroscopy ; Photoelectrons ; Radiation ; Resolution ; Secondary ion mass spectrometry ; Synchrotron radiation ; Synchrotrons ; Trichoderma</subject><ispartof>Environmental microbiology, 2021-02, Vol.23 (2), p.893-907</ispartof><rights>2020 Society for Applied Microbiology and John Wiley &amp; Sons Ltd</rights><rights>2020 Society for Applied Microbiology and John Wiley &amp; Sons Ltd.</rights><rights>2021 Society for Applied Microbiology and John Wiley &amp; Sons Ltd</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c4123-aa675f48b248837ec2563fe7d6ba039247dfb87f8c83ac6b318ddb34bb2228623</citedby><cites>FETCH-LOGICAL-c4123-aa675f48b248837ec2563fe7d6ba039247dfb87f8c83ac6b318ddb34bb2228623</cites><orcidid>0000-0002-5699-779X ; 0000-0001-6874-870X</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://onlinelibrary.wiley.com/doi/pdf/10.1111%2F1462-2920.15193$$EPDF$$P50$$Gwiley$$H</linktopdf><linktohtml>$$Uhttps://onlinelibrary.wiley.com/doi/full/10.1111%2F1462-2920.15193$$EHTML$$P50$$Gwiley$$H</linktohtml><link.rule.ids>314,776,780,1411,27901,27902,45550,45551</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/32783346$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Chi, Zhi‐Lai</creatorcontrib><creatorcontrib>Zhao, Xiang‐Yang</creatorcontrib><creatorcontrib>Chen, Ya‐Ling</creatorcontrib><creatorcontrib>Hao, Jia‐Long</creatorcontrib><creatorcontrib>Yu, Guang‐Hui</creatorcontrib><creatorcontrib>Goodman, Bernard A.</creatorcontrib><creatorcontrib>Gadd, Geoffrey Michael</creatorcontrib><title>Intrinsic enzyme‐like activity of magnetite particles is enhanced by cultivation with Trichoderma guizhouense</title><title>Environmental microbiology</title><addtitle>Environ Microbiol</addtitle><description>Summary Fungal–mineral interactions can produce large amounts of biogenic nano‐size (~ 1–100 nm) minerals, yet their influence on fungal physiology and growth remains largely unexplored. Using Trichoderma guizhouense NJAU4742 and magnetite (Mt) as a model fungus and mineral system, we have shown for the first time that biogenic Mt nanoparticles formed during fungal–mineral cultivation exhibit intrinsic peroxidase‐like activity. Specifically, the average peroxidase‐like activity of Mt nanoparticles after 72 h cultivation was ~ 2.4 times higher than that of the original Mt. Evidence from high resolution X‐ray photoelectron spectroscopy analyses indicated that the unique properties of magnetite nanoparticles largely stemmed from their high proportion of surface non‐lattice oxygen, through occupying surface oxygen‐vacant sites, rather than Fe redox chemistry, which challenges conventional Fenton reaction theories that assume iron to be the sole redox‐active centre. Nanoscale secondary ion mass spectrometry with a resolution down to 50 nm demonstrated that a thin (&lt; 1 μm) oxygen‐film was present on the surface of fungal hyphae. 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Together, these findings highlight an important, but unrecognized, catalytic activity of mineral nanoparticles produced by fungal–mineral interactions and contribute substantially to our understanding of mineral nanoparticles in natural ecosystems.</description><subject>Analytical methods</subject><subject>Carbonyl compounds</subject><subject>Carbonyl groups</subject><subject>Carbonyls</subject><subject>Catalytic activity</subject><subject>Cultivation</subject><subject>Fungi</subject><subject>Hyphae</subject><subject>Iron</subject><subject>Magnetic properties</subject><subject>Magnetite</subject><subject>Mass spectrometry</subject><subject>Mass spectroscopy</subject><subject>Minerals</subject><subject>Nanoparticles</subject><subject>Oxidoreductions</subject><subject>Oxygen</subject><subject>Peroxidase</subject><subject>Photoelectron spectroscopy</subject><subject>Photoelectrons</subject><subject>Radiation</subject><subject>Resolution</subject><subject>Secondary ion mass spectrometry</subject><subject>Synchrotron radiation</subject><subject>Synchrotrons</subject><subject>Trichoderma</subject><issn>1462-2912</issn><issn>1462-2920</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2021</creationdate><recordtype>article</recordtype><recordid>eNqFkLtOwzAUhi0EgnKZ2ZAl5kJsJ7EzIsSlUhFLmS3bOSGGXIrtUIWJR-AZeRJSUrrixT5H3_9b-hA6JdEFGc4liVM6pRkdxoRkbAdNtpvd7ZvQA3To_UsUEc54tI8OGOWCsTidoHbWBGcbbw2G5qOv4fvzq7KvgJUJ9t2GHrcFrtVzA8EGwEvlgjUVeGz9EChVYyDHusemqwZeBds2eGVDiRfOmrLNwdUKP3f2o2w7aDwco71CVR5ONvcRerq9WVzfT-ePd7Prq_nUxISyqVIpT4pYaBoLwTgYmqSsAJ6nWkUsozHPCy14IYxgyqSaEZHnmsVaU0pFStkROh97l65968AH-dJ2rhm-lDTOaMozzrOBuhwp41rvHRRy6WytXC9JJNeC5VqhXOuUv4KHxNmmt9M15Fv-z-gAJCOwshX0__XJm4fZWPwDo3WHwg</recordid><startdate>202102</startdate><enddate>202102</enddate><creator>Chi, Zhi‐Lai</creator><creator>Zhao, Xiang‐Yang</creator><creator>Chen, Ya‐Ling</creator><creator>Hao, Jia‐Long</creator><creator>Yu, Guang‐Hui</creator><creator>Goodman, Bernard A.</creator><creator>Gadd, Geoffrey Michael</creator><general>John Wiley &amp; 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Using Trichoderma guizhouense NJAU4742 and magnetite (Mt) as a model fungus and mineral system, we have shown for the first time that biogenic Mt nanoparticles formed during fungal–mineral cultivation exhibit intrinsic peroxidase‐like activity. Specifically, the average peroxidase‐like activity of Mt nanoparticles after 72 h cultivation was ~ 2.4 times higher than that of the original Mt. Evidence from high resolution X‐ray photoelectron spectroscopy analyses indicated that the unique properties of magnetite nanoparticles largely stemmed from their high proportion of surface non‐lattice oxygen, through occupying surface oxygen‐vacant sites, rather than Fe redox chemistry, which challenges conventional Fenton reaction theories that assume iron to be the sole redox‐active centre. Nanoscale secondary ion mass spectrometry with a resolution down to 50 nm demonstrated that a thin (&lt; 1 μm) oxygen‐film was present on the surface of fungal hyphae. 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source Wiley Online Library Journals Frontfile Complete
subjects Analytical methods
Carbonyl compounds
Carbonyl groups
Carbonyls
Catalytic activity
Cultivation
Fungi
Hyphae
Iron
Magnetic properties
Magnetite
Mass spectrometry
Mass spectroscopy
Minerals
Nanoparticles
Oxidoreductions
Oxygen
Peroxidase
Photoelectron spectroscopy
Photoelectrons
Radiation
Resolution
Secondary ion mass spectrometry
Synchrotron radiation
Synchrotrons
Trichoderma
title Intrinsic enzyme‐like activity of magnetite particles is enhanced by cultivation with Trichoderma guizhouense
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