Fungal oxidative dissolution of the Mn(II)-bearing mineral rhodochrosite and the role of metabolites in manganese oxide formation
Summary Microbially mediated oxidation of Mn(II) to Mn(III/IV) oxides influences the cycling of metals and remineralization of carbon. Despite the prevalence of Mn(II)‐bearing minerals in nature, little is known regarding the ability of microbes to oxidize mineral‐hosted Mn(II). Here, we explored ox...
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| Veröffentlicht in: | Environmental microbiology 2013-04, Vol.15 (4), p.1063-1077 |
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| creator | Tang, Yuanzhi Zeiner, Carolyn A. Santelli, Cara M. Hansel, Colleen M. |
| description | Summary
Microbially mediated oxidation of Mn(II) to Mn(III/IV) oxides influences the cycling of metals and remineralization of carbon. Despite the prevalence of Mn(II)‐bearing minerals in nature, little is known regarding the ability of microbes to oxidize mineral‐hosted Mn(II). Here, we explored oxidation of the Mn(II)‐bearing mineral rhodochrosite (MnCO3) and characteristics of ensuing Mn oxides by six Mn(II)‐oxidizing Ascomycete fungi. All fungal species substantially enhanced rhodochrosite dissolution and surface modification. Mineral‐hosted Mn(II) was oxidized resulting in formation of Mn(III/IV) oxides that were all similar to δ‐MnO2 but varied in morphology and distribution in relation to cellular structures and the MnCO3 surface. For four fungi, Mn(II) oxidation occurred along hyphae, likely mediated by cell wall‐associated proteins. For two species, Mn(II) oxidation occurred via reaction with fungal‐derived superoxide produced at hyphal tips. This pathway ultimately resulted in structurally unique Mn oxide clusters formed at substantial distances from any cellular structure. Taken together, findings for these two fungi strongly point to a role for fungal‐derived organic molecules in Mn(III) complexation and Mn oxide templation. Overall, this study illustrates the importance of fungi in rhodochrosite dissolution, extends the relevance of biogenic superoxide‐based Mn(II) oxidation and highlights the potential role of mycogenic exudates in directing mineral precipitation. |
| doi_str_mv | 10.1111/1462-2920.12029 |
| format | Article |
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Microbially mediated oxidation of Mn(II) to Mn(III/IV) oxides influences the cycling of metals and remineralization of carbon. Despite the prevalence of Mn(II)‐bearing minerals in nature, little is known regarding the ability of microbes to oxidize mineral‐hosted Mn(II). Here, we explored oxidation of the Mn(II)‐bearing mineral rhodochrosite (MnCO3) and characteristics of ensuing Mn oxides by six Mn(II)‐oxidizing Ascomycete fungi. All fungal species substantially enhanced rhodochrosite dissolution and surface modification. Mineral‐hosted Mn(II) was oxidized resulting in formation of Mn(III/IV) oxides that were all similar to δ‐MnO2 but varied in morphology and distribution in relation to cellular structures and the MnCO3 surface. For four fungi, Mn(II) oxidation occurred along hyphae, likely mediated by cell wall‐associated proteins. For two species, Mn(II) oxidation occurred via reaction with fungal‐derived superoxide produced at hyphal tips. This pathway ultimately resulted in structurally unique Mn oxide clusters formed at substantial distances from any cellular structure. Taken together, findings for these two fungi strongly point to a role for fungal‐derived organic molecules in Mn(III) complexation and Mn oxide templation. Overall, this study illustrates the importance of fungi in rhodochrosite dissolution, extends the relevance of biogenic superoxide‐based Mn(II) oxidation and highlights the potential role of mycogenic exudates in directing mineral precipitation.</description><identifier>ISSN: 1462-2912</identifier><identifier>EISSN: 1462-2920</identifier><identifier>DOI: 10.1111/1462-2920.12029</identifier><identifier>PMID: 23157705</identifier><language>eng</language><publisher>Oxford: Blackwell Publishing Ltd</publisher><subject>Animal, plant and microbial ecology ; Ascomycetes ; Ascomycota - metabolism ; Biological and medical sciences ; Carbon - chemistry ; Dissolution ; Fundamental and applied biological sciences. Psychology ; Fungi ; Fungi - metabolism ; General aspects ; Geologic Sediments - chemistry ; Geologic Sediments - microbiology ; Hyphae - metabolism ; Manganese - chemistry ; Manganese Compounds - chemistry ; Metals - chemistry ; Microbial ecology ; Microbiology ; Minerals - chemistry ; Miscellaneous ; Mycology ; Oxidation-Reduction ; Oxides - chemistry ; Oxides - metabolism ; Superoxides - metabolism ; Surface Properties</subject><ispartof>Environmental microbiology, 2013-04, Vol.15 (4), p.1063-1077</ispartof><rights>2012 Society for Applied Microbiology and Blackwell Publishing Ltd</rights><rights>2014 INIST-CNRS</rights><rights>2012 Society for Applied Microbiology and Blackwell Publishing Ltd.</rights><rights>Copyright © 2013 Society for Applied Microbiology and Blackwell Publishing Ltd</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c5659-4916d86dac0442caaa6cccda137935a2c4476f6237bb04e335739e6636b338573</citedby><cites>FETCH-LOGICAL-c5659-4916d86dac0442caaa6cccda137935a2c4476f6237bb04e335739e6636b338573</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://onlinelibrary.wiley.com/doi/pdf/10.1111%2F1462-2920.12029$$EPDF$$P50$$Gwiley$$H</linktopdf><linktohtml>$$Uhttps://onlinelibrary.wiley.com/doi/full/10.1111%2F1462-2920.12029$$EHTML$$P50$$Gwiley$$H</linktohtml><link.rule.ids>230,314,776,780,881,1411,27901,27902,45550,45551</link.rule.ids><backlink>$$Uhttp://pascal-francis.inist.fr/vibad/index.php?action=getRecordDetail&idt=27275687$$DView record in Pascal Francis$$Hfree_for_read</backlink><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/23157705$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink><backlink>$$Uhttps://www.osti.gov/biblio/1109706$$D View this record in Osti.gov$$Hfree_for_read</backlink></links><search><creatorcontrib>Tang, Yuanzhi</creatorcontrib><creatorcontrib>Zeiner, Carolyn A.</creatorcontrib><creatorcontrib>Santelli, Cara M.</creatorcontrib><creatorcontrib>Hansel, Colleen M.</creatorcontrib><creatorcontrib>Brookhaven National Laboratory (BNL)</creatorcontrib><title>Fungal oxidative dissolution of the Mn(II)-bearing mineral rhodochrosite and the role of metabolites in manganese oxide formation</title><title>Environmental microbiology</title><addtitle>Environ Microbiol</addtitle><description>Summary
Microbially mediated oxidation of Mn(II) to Mn(III/IV) oxides influences the cycling of metals and remineralization of carbon. Despite the prevalence of Mn(II)‐bearing minerals in nature, little is known regarding the ability of microbes to oxidize mineral‐hosted Mn(II). Here, we explored oxidation of the Mn(II)‐bearing mineral rhodochrosite (MnCO3) and characteristics of ensuing Mn oxides by six Mn(II)‐oxidizing Ascomycete fungi. All fungal species substantially enhanced rhodochrosite dissolution and surface modification. Mineral‐hosted Mn(II) was oxidized resulting in formation of Mn(III/IV) oxides that were all similar to δ‐MnO2 but varied in morphology and distribution in relation to cellular structures and the MnCO3 surface. For four fungi, Mn(II) oxidation occurred along hyphae, likely mediated by cell wall‐associated proteins. For two species, Mn(II) oxidation occurred via reaction with fungal‐derived superoxide produced at hyphal tips. This pathway ultimately resulted in structurally unique Mn oxide clusters formed at substantial distances from any cellular structure. Taken together, findings for these two fungi strongly point to a role for fungal‐derived organic molecules in Mn(III) complexation and Mn oxide templation. Overall, this study illustrates the importance of fungi in rhodochrosite dissolution, extends the relevance of biogenic superoxide‐based Mn(II) oxidation and highlights the potential role of mycogenic exudates in directing mineral precipitation.</description><subject>Animal, plant and microbial ecology</subject><subject>Ascomycetes</subject><subject>Ascomycota - metabolism</subject><subject>Biological and medical sciences</subject><subject>Carbon - chemistry</subject><subject>Dissolution</subject><subject>Fundamental and applied biological sciences. Psychology</subject><subject>Fungi</subject><subject>Fungi - metabolism</subject><subject>General aspects</subject><subject>Geologic Sediments - chemistry</subject><subject>Geologic Sediments - microbiology</subject><subject>Hyphae - metabolism</subject><subject>Manganese - chemistry</subject><subject>Manganese Compounds - chemistry</subject><subject>Metals - chemistry</subject><subject>Microbial ecology</subject><subject>Microbiology</subject><subject>Minerals - chemistry</subject><subject>Miscellaneous</subject><subject>Mycology</subject><subject>Oxidation-Reduction</subject><subject>Oxides - chemistry</subject><subject>Oxides - metabolism</subject><subject>Superoxides - metabolism</subject><subject>Surface Properties</subject><issn>1462-2912</issn><issn>1462-2920</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2013</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNqNkktv1DAUhSMEoqWwZocsEFJZhPrtZAlVO4zUlg2oEhvLcW46Lond2gm0S_45zsx0kNiAN359x-fax0XxkuD3JLcjwiUtaU3zlGJaPyr2dyuPd2NC94pnKV1jTBRT-GmxRxkRSmGxX_w6nfyV6VG4c60Z3Q9ArUsp9NPogkehQ-MK0Lk_XC7flQ2Y6PwVGpyHmDVxFdpgVzEkNwIyvl3DMfQwCwcYTRP6vJWQ82gw2cdDgrUVoC7Ewcwmz4snnekTvNj2B8XX05Mvx5_Ks8-L5fGHs9IKKeqS10S2lWyNxZxTa4yR1trWEKZqJgy1nCvZScpU02AOjAnFapCSyYaxKk8Oitebc0ManU42F2ZXNngPdtSE4FphmaHDDXQTw-0EadSDSxb6PpcepqQJ4xWvMRP4P1DKWY0pma3f_IVehyn6fNuZYpJXuKKZOtpQNr9oitDpm-gGE-81wXpOW8956jlbvU47K15tz52aAdod_xBvBt5uAZOs6btovHXpD6eoErKaCxQb7qfr4f5fvvrkfPlQQLnRuTTC3U5n4nct81cT-vJikV2-ycVHeqEv2W_Q-841</recordid><startdate>201304</startdate><enddate>201304</enddate><creator>Tang, Yuanzhi</creator><creator>Zeiner, Carolyn A.</creator><creator>Santelli, Cara M.</creator><creator>Hansel, Colleen M.</creator><general>Blackwell Publishing Ltd</general><general>Blackwell</general><general>Wiley Subscription Services, Inc</general><scope>BSCLL</scope><scope>IQODW</scope><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>7QH</scope><scope>7QL</scope><scope>7ST</scope><scope>7T7</scope><scope>7TN</scope><scope>7U9</scope><scope>7UA</scope><scope>8FD</scope><scope>C1K</scope><scope>F1W</scope><scope>FR3</scope><scope>H94</scope><scope>H95</scope><scope>H97</scope><scope>L.G</scope><scope>M7N</scope><scope>P64</scope><scope>SOI</scope><scope>7X8</scope><scope>OTOTI</scope></search><sort><creationdate>201304</creationdate><title>Fungal oxidative dissolution of the Mn(II)-bearing mineral rhodochrosite and the role of metabolites in manganese oxide formation</title><author>Tang, Yuanzhi ; Zeiner, Carolyn A. ; Santelli, Cara M. ; Hansel, Colleen M.</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c5659-4916d86dac0442caaa6cccda137935a2c4476f6237bb04e335739e6636b338573</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2013</creationdate><topic>Animal, plant and microbial ecology</topic><topic>Ascomycetes</topic><topic>Ascomycota - metabolism</topic><topic>Biological and medical sciences</topic><topic>Carbon - chemistry</topic><topic>Dissolution</topic><topic>Fundamental and applied biological sciences. Psychology</topic><topic>Fungi</topic><topic>Fungi - metabolism</topic><topic>General aspects</topic><topic>Geologic Sediments - chemistry</topic><topic>Geologic Sediments - microbiology</topic><topic>Hyphae - metabolism</topic><topic>Manganese - chemistry</topic><topic>Manganese Compounds - chemistry</topic><topic>Metals - chemistry</topic><topic>Microbial ecology</topic><topic>Microbiology</topic><topic>Minerals - chemistry</topic><topic>Miscellaneous</topic><topic>Mycology</topic><topic>Oxidation-Reduction</topic><topic>Oxides - chemistry</topic><topic>Oxides - metabolism</topic><topic>Superoxides - metabolism</topic><topic>Surface Properties</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Tang, Yuanzhi</creatorcontrib><creatorcontrib>Zeiner, Carolyn A.</creatorcontrib><creatorcontrib>Santelli, Cara M.</creatorcontrib><creatorcontrib>Hansel, Colleen M.</creatorcontrib><creatorcontrib>Brookhaven National Laboratory (BNL)</creatorcontrib><collection>Istex</collection><collection>Pascal-Francis</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Aqualine</collection><collection>Bacteriology Abstracts (Microbiology B)</collection><collection>Environment Abstracts</collection><collection>Industrial and Applied Microbiology Abstracts (Microbiology A)</collection><collection>Oceanic Abstracts</collection><collection>Virology and AIDS Abstracts</collection><collection>Water Resources Abstracts</collection><collection>Technology Research Database</collection><collection>Environmental Sciences and Pollution Management</collection><collection>ASFA: Aquatic Sciences and Fisheries Abstracts</collection><collection>Engineering Research Database</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>Aquatic Science & Fisheries Abstracts (ASFA) 1: Biological Sciences & Living Resources</collection><collection>Aquatic Science & Fisheries Abstracts (ASFA) 3: Aquatic Pollution & Environmental Quality</collection><collection>Aquatic Science & Fisheries Abstracts (ASFA) Professional</collection><collection>Algology Mycology and Protozoology Abstracts (Microbiology C)</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Environment Abstracts</collection><collection>MEDLINE - Academic</collection><collection>OSTI.GOV</collection><jtitle>Environmental microbiology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Tang, Yuanzhi</au><au>Zeiner, Carolyn A.</au><au>Santelli, Cara M.</au><au>Hansel, Colleen M.</au><aucorp>Brookhaven National Laboratory (BNL)</aucorp><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Fungal oxidative dissolution of the Mn(II)-bearing mineral rhodochrosite and the role of metabolites in manganese oxide formation</atitle><jtitle>Environmental microbiology</jtitle><addtitle>Environ Microbiol</addtitle><date>2013-04</date><risdate>2013</risdate><volume>15</volume><issue>4</issue><spage>1063</spage><epage>1077</epage><pages>1063-1077</pages><issn>1462-2912</issn><eissn>1462-2920</eissn><abstract>Summary
Microbially mediated oxidation of Mn(II) to Mn(III/IV) oxides influences the cycling of metals and remineralization of carbon. Despite the prevalence of Mn(II)‐bearing minerals in nature, little is known regarding the ability of microbes to oxidize mineral‐hosted Mn(II). Here, we explored oxidation of the Mn(II)‐bearing mineral rhodochrosite (MnCO3) and characteristics of ensuing Mn oxides by six Mn(II)‐oxidizing Ascomycete fungi. All fungal species substantially enhanced rhodochrosite dissolution and surface modification. Mineral‐hosted Mn(II) was oxidized resulting in formation of Mn(III/IV) oxides that were all similar to δ‐MnO2 but varied in morphology and distribution in relation to cellular structures and the MnCO3 surface. For four fungi, Mn(II) oxidation occurred along hyphae, likely mediated by cell wall‐associated proteins. For two species, Mn(II) oxidation occurred via reaction with fungal‐derived superoxide produced at hyphal tips. This pathway ultimately resulted in structurally unique Mn oxide clusters formed at substantial distances from any cellular structure. Taken together, findings for these two fungi strongly point to a role for fungal‐derived organic molecules in Mn(III) complexation and Mn oxide templation. Overall, this study illustrates the importance of fungi in rhodochrosite dissolution, extends the relevance of biogenic superoxide‐based Mn(II) oxidation and highlights the potential role of mycogenic exudates in directing mineral precipitation.</abstract><cop>Oxford</cop><pub>Blackwell Publishing Ltd</pub><pmid>23157705</pmid><doi>10.1111/1462-2920.12029</doi><tpages>15</tpages></addata></record> |
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| ispartof | Environmental microbiology, 2013-04, Vol.15 (4), p.1063-1077 |
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| subjects | Animal, plant and microbial ecology Ascomycetes Ascomycota - metabolism Biological and medical sciences Carbon - chemistry Dissolution Fundamental and applied biological sciences. Psychology Fungi Fungi - metabolism General aspects Geologic Sediments - chemistry Geologic Sediments - microbiology Hyphae - metabolism Manganese - chemistry Manganese Compounds - chemistry Metals - chemistry Microbial ecology Microbiology Minerals - chemistry Miscellaneous Mycology Oxidation-Reduction Oxides - chemistry Oxides - metabolism Superoxides - metabolism Surface Properties |
| title | Fungal oxidative dissolution of the Mn(II)-bearing mineral rhodochrosite and the role of metabolites in manganese oxide formation |
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