Insights into Nitrate-Reducing Fe(II) Oxidation Mechanisms through Analysis of Cell-Mineral Associations, Cell Encrustation, and Mineralogy in the Chemolithoautotrophic Enrichment Culture KS
Most described nitrate-reducing Fe(II)-oxidizing bacteria (NRFeOB) are mixotrophic and depend on organic cosubstrates for growth. Encrustation of cells in Fe(III) minerals has been observed for mixotrophic NRFeOB but not for autotrophic phototrophic and microaerophilic Fe(II) oxidizers. So far, litt...
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description | Most described nitrate-reducing Fe(II)-oxidizing bacteria (NRFeOB) are mixotrophic and depend on organic cosubstrates for growth. Encrustation of cells in Fe(III) minerals has been observed for mixotrophic NRFeOB but not for autotrophic phototrophic and microaerophilic Fe(II) oxidizers. So far, little is known about cell-mineral associations in the few existing autotrophic NRFeOB. Here, we investigate whether the designated autotrophic Fe(II)-oxidizing strain (closely related to
and
) or the heterotrophic nitrate reducers that are present in the autotrophic nitrate-reducing Fe(II)-oxidizing enrichment culture KS form mineral crusts during Fe(II) oxidation under autotrophic and mixotrophic conditions. In the mixed culture, we found no significant encrustation of any of the cells both during autotrophic oxidation of 8 to 10 mM Fe(II) coupled to nitrate reduction and during cultivation under mixotrophic conditions with 8 to 10 mM Fe(II), 5 mM acetate, and 4 mM nitrate, where higher numbers of heterotrophic nitrate reducers were present. Two pure cultures of heterotrophic nitrate reducers (
and
) isolated from culture KS were analyzed under mixotrophic growth conditions. We found green rust formation, no cell encrustation, and only a few mineral particles on some cell surfaces with 5 mM Fe(II) and some encrustation with 10 mM Fe(II). Our findings suggest that enzymatic, autotrophic Fe(II) oxidation coupled to nitrate reduction forms poorly crystalline Fe(III) oxyhydroxides and proceeds without cellular encrustation while indirect Fe(II) oxidation via heterotrophic nitrate-reduction-derived nitrite can lead to green rust as an intermediate mineral and significant cell encrustation. The extent of encrustation caused by indirect Fe(II) oxidation by reactive nitrogen species depends on Fe(II) concentrations and is probably negligible under environmental conditions in most habitats.
Most described nitrate-reducing Fe(II)-oxidizing bacteria (NRFeOB) are mixotrophic (their growth depends on organic cosubstrates) and can become encrusted in Fe(III) minerals. Encrustation is expected to be harmful and poses a threat to cells if it also occurs under environmentally relevant conditions. Nitrite produced during heterotrophic denitrification reacts with Fe(II) abiotically and is probably the reason for encrustation in mixotrophic NRFeOB. Little is known about cell-mineral associations in autotrophic NRFeOB such as the enrichment culture KS. Here, we show that no encrustati |
doi_str_mv | 10.1128/AEM.00752-17 |
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and
) or the heterotrophic nitrate reducers that are present in the autotrophic nitrate-reducing Fe(II)-oxidizing enrichment culture KS form mineral crusts during Fe(II) oxidation under autotrophic and mixotrophic conditions. In the mixed culture, we found no significant encrustation of any of the cells both during autotrophic oxidation of 8 to 10 mM Fe(II) coupled to nitrate reduction and during cultivation under mixotrophic conditions with 8 to 10 mM Fe(II), 5 mM acetate, and 4 mM nitrate, where higher numbers of heterotrophic nitrate reducers were present. Two pure cultures of heterotrophic nitrate reducers (
and
) isolated from culture KS were analyzed under mixotrophic growth conditions. We found green rust formation, no cell encrustation, and only a few mineral particles on some cell surfaces with 5 mM Fe(II) and some encrustation with 10 mM Fe(II). Our findings suggest that enzymatic, autotrophic Fe(II) oxidation coupled to nitrate reduction forms poorly crystalline Fe(III) oxyhydroxides and proceeds without cellular encrustation while indirect Fe(II) oxidation via heterotrophic nitrate-reduction-derived nitrite can lead to green rust as an intermediate mineral and significant cell encrustation. The extent of encrustation caused by indirect Fe(II) oxidation by reactive nitrogen species depends on Fe(II) concentrations and is probably negligible under environmental conditions in most habitats.
Most described nitrate-reducing Fe(II)-oxidizing bacteria (NRFeOB) are mixotrophic (their growth depends on organic cosubstrates) and can become encrusted in Fe(III) minerals. Encrustation is expected to be harmful and poses a threat to cells if it also occurs under environmentally relevant conditions. Nitrite produced during heterotrophic denitrification reacts with Fe(II) abiotically and is probably the reason for encrustation in mixotrophic NRFeOB. Little is known about cell-mineral associations in autotrophic NRFeOB such as the enrichment culture KS. Here, we show that no encrustation occurs in culture KS under autotrophic and mixotrophic conditions while heterotrophic nitrate-reducing isolates from culture KS become encrusted. These findings support the hypothesis that encrustation in mixotrophic cultures is caused by the abiotic reaction of Fe(II) with nitrite and provide evidence that Fe(II) oxidation in culture KS is enzymatic. Furthermore, we show that the extent of encrustation caused by indirect Fe(II) oxidation by reactive nitrogen species depends on Fe(II) concentrations and is probably negligible in most environmental habitats.</description><identifier>ISSN: 0099-2240</identifier><identifier>EISSN: 1098-5336</identifier><identifier>DOI: 10.1128/AEM.00752-17</identifier><identifier>PMID: 28455336</identifier><language>eng</language><publisher>United States: American Society for Microbiology</publisher><subject>Acetates - metabolism ; Acetic acid ; Bacteria ; Bacteria - genetics ; Bacteria - growth & development ; Bacteria - metabolism ; Cell culture ; Cells ; Chemoautotrophic Growth ; Crusts ; Cultivation ; Encrustation ; Enrichment ; Environmental conditions ; Ferric Compounds - metabolism ; Ferrous Compounds - metabolism ; Geomicrobiology ; Green rust ; Growth conditions ; Iron ; Mineralogy ; Minerals ; Minerals - metabolism ; Mixed culture ; Nitrate reduction ; Nitrates ; Nitrates - metabolism ; Nitrites - metabolism ; Oxidation ; Oxidation-Reduction ; Oxidizing agents ; Reactive nitrogen species ; Reduction</subject><ispartof>Applied and environmental microbiology, 2017-07, Vol.83 (13)</ispartof><rights>Copyright © 2017 American Society for Microbiology.</rights><rights>Copyright American Society for Microbiology Jul 2017</rights><rights>Copyright © 2017 American Society for Microbiology. 2017 American Society for Microbiology</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c412t-20926385d27699483d9c19c95a62ed27b0c10e0bf4332cf6e47034ec480eba2d3</citedby><cites>FETCH-LOGICAL-c412t-20926385d27699483d9c19c95a62ed27b0c10e0bf4332cf6e47034ec480eba2d3</cites><orcidid>0000-0001-8304-9149</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC5478975/pdf/$$EPDF$$P50$$Gpubmedcentral$$H</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC5478975/$$EHTML$$P50$$Gpubmedcentral$$H</linktohtml><link.rule.ids>230,315,728,781,785,886,3189,27929,27930,53796,53798</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/28455336$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><contributor>Kostka, Joel E.</contributor><creatorcontrib>Nordhoff, M</creatorcontrib><creatorcontrib>Tominski, C</creatorcontrib><creatorcontrib>Halama, M</creatorcontrib><creatorcontrib>Byrne, J M</creatorcontrib><creatorcontrib>Obst, M</creatorcontrib><creatorcontrib>Kleindienst, S</creatorcontrib><creatorcontrib>Behrens, S</creatorcontrib><creatorcontrib>Kappler, A</creatorcontrib><title>Insights into Nitrate-Reducing Fe(II) Oxidation Mechanisms through Analysis of Cell-Mineral Associations, Cell Encrustation, and Mineralogy in the Chemolithoautotrophic Enrichment Culture KS</title><title>Applied and environmental microbiology</title><addtitle>Appl Environ Microbiol</addtitle><description>Most described nitrate-reducing Fe(II)-oxidizing bacteria (NRFeOB) are mixotrophic and depend on organic cosubstrates for growth. Encrustation of cells in Fe(III) minerals has been observed for mixotrophic NRFeOB but not for autotrophic phototrophic and microaerophilic Fe(II) oxidizers. So far, little is known about cell-mineral associations in the few existing autotrophic NRFeOB. Here, we investigate whether the designated autotrophic Fe(II)-oxidizing strain (closely related to
and
) or the heterotrophic nitrate reducers that are present in the autotrophic nitrate-reducing Fe(II)-oxidizing enrichment culture KS form mineral crusts during Fe(II) oxidation under autotrophic and mixotrophic conditions. In the mixed culture, we found no significant encrustation of any of the cells both during autotrophic oxidation of 8 to 10 mM Fe(II) coupled to nitrate reduction and during cultivation under mixotrophic conditions with 8 to 10 mM Fe(II), 5 mM acetate, and 4 mM nitrate, where higher numbers of heterotrophic nitrate reducers were present. Two pure cultures of heterotrophic nitrate reducers (
and
) isolated from culture KS were analyzed under mixotrophic growth conditions. We found green rust formation, no cell encrustation, and only a few mineral particles on some cell surfaces with 5 mM Fe(II) and some encrustation with 10 mM Fe(II). Our findings suggest that enzymatic, autotrophic Fe(II) oxidation coupled to nitrate reduction forms poorly crystalline Fe(III) oxyhydroxides and proceeds without cellular encrustation while indirect Fe(II) oxidation via heterotrophic nitrate-reduction-derived nitrite can lead to green rust as an intermediate mineral and significant cell encrustation. The extent of encrustation caused by indirect Fe(II) oxidation by reactive nitrogen species depends on Fe(II) concentrations and is probably negligible under environmental conditions in most habitats.
Most described nitrate-reducing Fe(II)-oxidizing bacteria (NRFeOB) are mixotrophic (their growth depends on organic cosubstrates) and can become encrusted in Fe(III) minerals. Encrustation is expected to be harmful and poses a threat to cells if it also occurs under environmentally relevant conditions. Nitrite produced during heterotrophic denitrification reacts with Fe(II) abiotically and is probably the reason for encrustation in mixotrophic NRFeOB. Little is known about cell-mineral associations in autotrophic NRFeOB such as the enrichment culture KS. Here, we show that no encrustation occurs in culture KS under autotrophic and mixotrophic conditions while heterotrophic nitrate-reducing isolates from culture KS become encrusted. These findings support the hypothesis that encrustation in mixotrophic cultures is caused by the abiotic reaction of Fe(II) with nitrite and provide evidence that Fe(II) oxidation in culture KS is enzymatic. Furthermore, we show that the extent of encrustation caused by indirect Fe(II) oxidation by reactive nitrogen species depends on Fe(II) concentrations and is probably negligible in most environmental habitats.</description><subject>Acetates - metabolism</subject><subject>Acetic acid</subject><subject>Bacteria</subject><subject>Bacteria - genetics</subject><subject>Bacteria - growth & development</subject><subject>Bacteria - metabolism</subject><subject>Cell culture</subject><subject>Cells</subject><subject>Chemoautotrophic Growth</subject><subject>Crusts</subject><subject>Cultivation</subject><subject>Encrustation</subject><subject>Enrichment</subject><subject>Environmental conditions</subject><subject>Ferric Compounds - metabolism</subject><subject>Ferrous Compounds - metabolism</subject><subject>Geomicrobiology</subject><subject>Green rust</subject><subject>Growth conditions</subject><subject>Iron</subject><subject>Mineralogy</subject><subject>Minerals</subject><subject>Minerals - metabolism</subject><subject>Mixed culture</subject><subject>Nitrate reduction</subject><subject>Nitrates</subject><subject>Nitrates - metabolism</subject><subject>Nitrites - metabolism</subject><subject>Oxidation</subject><subject>Oxidation-Reduction</subject><subject>Oxidizing agents</subject><subject>Reactive nitrogen species</subject><subject>Reduction</subject><issn>0099-2240</issn><issn>1098-5336</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2017</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNpdkk1vEzEQhi0EomnhxhlZ4tJK2WJ7vbv2BSlapRDRUImPs-V4vVlXu3bwByJ_jt-Gk4YKOI0088yrd0YvAK8wusaYsLeL5foaoaYiBW6egBlGnBVVWdZPwQwhzgtCKDoD5yHcI4QoqtlzcEYYrQ7MDPxa2WC2QwzQ2OjgJxO9jLr4rLukjN3CG325Wl3Bu5-mk9E4C9daDdKaMAUYB-_SdoALK8d9MAG6HrZ6HIu1sdrLES5CcMoc98L8OIJLq3wK8dibQ2k7eILddp8tZE0N20FPbjRxcDJFF73bDUblTW_UMGkbYZvGmLyGH7-8AM96OQb98lQvwLeb5df2Q3F7937VLm4LRTGJBUGc1CWrOtLUnFNWdlxhrngla6Jzc4MURhptelqWRPW1pg0qqVaUIb2RpCsvwLsH3V3aTLpT2UX2LHbeTNLvhZNG_DuxZhBb90NUtGG8qbLA5UnAu-9JhygmE1T-iLTapSAw42VFeYPrjL75D713yecfZ4pXNWWckCZT8wdKeReC1_2jGYzEIRgiB0McgyHwAX_99wGP8J8klL8Bn4S2_w</recordid><startdate>20170701</startdate><enddate>20170701</enddate><creator>Nordhoff, M</creator><creator>Tominski, C</creator><creator>Halama, M</creator><creator>Byrne, J M</creator><creator>Obst, M</creator><creator>Kleindienst, S</creator><creator>Behrens, S</creator><creator>Kappler, A</creator><general>American Society for Microbiology</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>7QL</scope><scope>7QO</scope><scope>7SN</scope><scope>7SS</scope><scope>7ST</scope><scope>7T7</scope><scope>7TM</scope><scope>7U9</scope><scope>8FD</scope><scope>C1K</scope><scope>FR3</scope><scope>H94</scope><scope>M7N</scope><scope>P64</scope><scope>RC3</scope><scope>SOI</scope><scope>7X8</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0001-8304-9149</orcidid></search><sort><creationdate>20170701</creationdate><title>Insights into Nitrate-Reducing Fe(II) Oxidation Mechanisms through Analysis of Cell-Mineral Associations, Cell Encrustation, and Mineralogy in the Chemolithoautotrophic Enrichment Culture KS</title><author>Nordhoff, M ; Tominski, C ; Halama, M ; Byrne, J M ; Obst, M ; Kleindienst, S ; Behrens, S ; Kappler, A</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c412t-20926385d27699483d9c19c95a62ed27b0c10e0bf4332cf6e47034ec480eba2d3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2017</creationdate><topic>Acetates - metabolism</topic><topic>Acetic acid</topic><topic>Bacteria</topic><topic>Bacteria - genetics</topic><topic>Bacteria - growth & development</topic><topic>Bacteria - metabolism</topic><topic>Cell culture</topic><topic>Cells</topic><topic>Chemoautotrophic Growth</topic><topic>Crusts</topic><topic>Cultivation</topic><topic>Encrustation</topic><topic>Enrichment</topic><topic>Environmental conditions</topic><topic>Ferric Compounds - metabolism</topic><topic>Ferrous Compounds - metabolism</topic><topic>Geomicrobiology</topic><topic>Green rust</topic><topic>Growth conditions</topic><topic>Iron</topic><topic>Mineralogy</topic><topic>Minerals</topic><topic>Minerals - metabolism</topic><topic>Mixed culture</topic><topic>Nitrate reduction</topic><topic>Nitrates</topic><topic>Nitrates - metabolism</topic><topic>Nitrites - metabolism</topic><topic>Oxidation</topic><topic>Oxidation-Reduction</topic><topic>Oxidizing agents</topic><topic>Reactive nitrogen species</topic><topic>Reduction</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Nordhoff, M</creatorcontrib><creatorcontrib>Tominski, C</creatorcontrib><creatorcontrib>Halama, M</creatorcontrib><creatorcontrib>Byrne, J M</creatorcontrib><creatorcontrib>Obst, M</creatorcontrib><creatorcontrib>Kleindienst, S</creatorcontrib><creatorcontrib>Behrens, S</creatorcontrib><creatorcontrib>Kappler, A</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Bacteriology Abstracts (Microbiology B)</collection><collection>Biotechnology Research Abstracts</collection><collection>Ecology Abstracts</collection><collection>Entomology Abstracts (Full archive)</collection><collection>Environment Abstracts</collection><collection>Industrial and Applied Microbiology Abstracts (Microbiology A)</collection><collection>Nucleic Acids Abstracts</collection><collection>Virology and AIDS Abstracts</collection><collection>Technology Research Database</collection><collection>Environmental Sciences and Pollution Management</collection><collection>Engineering Research Database</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>Algology Mycology and Protozoology Abstracts (Microbiology C)</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Genetics Abstracts</collection><collection>Environment Abstracts</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Applied and environmental microbiology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Nordhoff, M</au><au>Tominski, C</au><au>Halama, M</au><au>Byrne, J M</au><au>Obst, M</au><au>Kleindienst, S</au><au>Behrens, S</au><au>Kappler, A</au><au>Kostka, Joel E.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Insights into Nitrate-Reducing Fe(II) Oxidation Mechanisms through Analysis of Cell-Mineral Associations, Cell Encrustation, and Mineralogy in the Chemolithoautotrophic Enrichment Culture KS</atitle><jtitle>Applied and environmental microbiology</jtitle><addtitle>Appl Environ Microbiol</addtitle><date>2017-07-01</date><risdate>2017</risdate><volume>83</volume><issue>13</issue><issn>0099-2240</issn><eissn>1098-5336</eissn><abstract>Most described nitrate-reducing Fe(II)-oxidizing bacteria (NRFeOB) are mixotrophic and depend on organic cosubstrates for growth. Encrustation of cells in Fe(III) minerals has been observed for mixotrophic NRFeOB but not for autotrophic phototrophic and microaerophilic Fe(II) oxidizers. So far, little is known about cell-mineral associations in the few existing autotrophic NRFeOB. Here, we investigate whether the designated autotrophic Fe(II)-oxidizing strain (closely related to
and
) or the heterotrophic nitrate reducers that are present in the autotrophic nitrate-reducing Fe(II)-oxidizing enrichment culture KS form mineral crusts during Fe(II) oxidation under autotrophic and mixotrophic conditions. In the mixed culture, we found no significant encrustation of any of the cells both during autotrophic oxidation of 8 to 10 mM Fe(II) coupled to nitrate reduction and during cultivation under mixotrophic conditions with 8 to 10 mM Fe(II), 5 mM acetate, and 4 mM nitrate, where higher numbers of heterotrophic nitrate reducers were present. Two pure cultures of heterotrophic nitrate reducers (
and
) isolated from culture KS were analyzed under mixotrophic growth conditions. We found green rust formation, no cell encrustation, and only a few mineral particles on some cell surfaces with 5 mM Fe(II) and some encrustation with 10 mM Fe(II). Our findings suggest that enzymatic, autotrophic Fe(II) oxidation coupled to nitrate reduction forms poorly crystalline Fe(III) oxyhydroxides and proceeds without cellular encrustation while indirect Fe(II) oxidation via heterotrophic nitrate-reduction-derived nitrite can lead to green rust as an intermediate mineral and significant cell encrustation. The extent of encrustation caused by indirect Fe(II) oxidation by reactive nitrogen species depends on Fe(II) concentrations and is probably negligible under environmental conditions in most habitats.
Most described nitrate-reducing Fe(II)-oxidizing bacteria (NRFeOB) are mixotrophic (their growth depends on organic cosubstrates) and can become encrusted in Fe(III) minerals. Encrustation is expected to be harmful and poses a threat to cells if it also occurs under environmentally relevant conditions. Nitrite produced during heterotrophic denitrification reacts with Fe(II) abiotically and is probably the reason for encrustation in mixotrophic NRFeOB. Little is known about cell-mineral associations in autotrophic NRFeOB such as the enrichment culture KS. Here, we show that no encrustation occurs in culture KS under autotrophic and mixotrophic conditions while heterotrophic nitrate-reducing isolates from culture KS become encrusted. These findings support the hypothesis that encrustation in mixotrophic cultures is caused by the abiotic reaction of Fe(II) with nitrite and provide evidence that Fe(II) oxidation in culture KS is enzymatic. Furthermore, we show that the extent of encrustation caused by indirect Fe(II) oxidation by reactive nitrogen species depends on Fe(II) concentrations and is probably negligible in most environmental habitats.</abstract><cop>United States</cop><pub>American Society for Microbiology</pub><pmid>28455336</pmid><doi>10.1128/AEM.00752-17</doi><orcidid>https://orcid.org/0000-0001-8304-9149</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | Acetates - metabolism Acetic acid Bacteria Bacteria - genetics Bacteria - growth & development Bacteria - metabolism Cell culture Cells Chemoautotrophic Growth Crusts Cultivation Encrustation Enrichment Environmental conditions Ferric Compounds - metabolism Ferrous Compounds - metabolism Geomicrobiology Green rust Growth conditions Iron Mineralogy Minerals Minerals - metabolism Mixed culture Nitrate reduction Nitrates Nitrates - metabolism Nitrites - metabolism Oxidation Oxidation-Reduction Oxidizing agents Reactive nitrogen species Reduction |
title | Insights into Nitrate-Reducing Fe(II) Oxidation Mechanisms through Analysis of Cell-Mineral Associations, Cell Encrustation, and Mineralogy in the Chemolithoautotrophic Enrichment Culture KS |
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