Tags

Type your tag names separated by a space and hit enter

Insights into Nitrate-Reducing Fe(II) Oxidation Mechanisms through Analysis of Cell-Mineral Associations, Cell Encrustation, and Mineralogy in the Chemolithoautotrophic Enrichment Culture KS.
Appl Environ Microbiol. 2017 07 01; 83(13)AE

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 Gallionella and Sideroxydans) 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 (Nocardioides and Rhodanobacter) 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.IMPORTANCE 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.

Authors+Show Affiliations

Geomicrobiology, Center for Applied Geosciences, University of Tuebingen, Tuebingen, Germany.Geomicrobiology, Center for Applied Geosciences, University of Tuebingen, Tuebingen, Germany.Geomicrobiology, Center for Applied Geosciences, University of Tuebingen, Tuebingen, Germany.Geomicrobiology, Center for Applied Geosciences, University of Tuebingen, Tuebingen, Germany.Bayreuth Center for Ecology and Environmental Research, University of Bayreuth, Bayreuth, Germany.Geomicrobiology, Center for Applied Geosciences, University of Tuebingen, Tuebingen, Germany.Geomicrobiology, Center for Applied Geosciences, University of Tuebingen, Tuebingen, Germany. Department of Civil, Environmental, and Geo-Engineering, University of Minnesota, Minneapolis, Minnesota, USA.Geomicrobiology, Center for Applied Geosciences, University of Tuebingen, Tuebingen, Germany andreas.kappler@uni-tuebingen.de. Center for Geomicrobiology, Department of Bioscience, Aarhus University, Aarhus, Denmark.

Pub Type(s)

Journal Article
Research Support, Non-U.S. Gov't

Language

eng

PubMed ID

28455336

Citation

Nordhoff, M, et al. "Insights Into Nitrate-Reducing Fe(II) Oxidation Mechanisms Through Analysis of Cell-Mineral Associations, Cell Encrustation, and Mineralogy in the Chemolithoautotrophic Enrichment Culture KS." Applied and Environmental Microbiology, vol. 83, no. 13, 2017.
Nordhoff M, Tominski C, Halama M, et al. Insights into Nitrate-Reducing Fe(II) Oxidation Mechanisms through Analysis of Cell-Mineral Associations, Cell Encrustation, and Mineralogy in the Chemolithoautotrophic Enrichment Culture KS. Appl Environ Microbiol. 2017;83(13).
Nordhoff, M., Tominski, C., Halama, M., Byrne, J. M., Obst, M., Kleindienst, S., Behrens, S., & Kappler, A. (2017). Insights into Nitrate-Reducing Fe(II) Oxidation Mechanisms through Analysis of Cell-Mineral Associations, Cell Encrustation, and Mineralogy in the Chemolithoautotrophic Enrichment Culture KS. Applied and Environmental Microbiology, 83(13). https://doi.org/10.1128/AEM.00752-17
Nordhoff M, et al. Insights Into Nitrate-Reducing Fe(II) Oxidation Mechanisms Through Analysis of Cell-Mineral Associations, Cell Encrustation, and Mineralogy in the Chemolithoautotrophic Enrichment Culture KS. Appl Environ Microbiol. 2017 07 1;83(13) PubMed PMID: 28455336.
* Article titles in AMA citation format should be in sentence-case
TY - JOUR T1 - Insights into Nitrate-Reducing Fe(II) Oxidation Mechanisms through Analysis of Cell-Mineral Associations, Cell Encrustation, and Mineralogy in the Chemolithoautotrophic Enrichment Culture KS. AU - Nordhoff,M, AU - Tominski,C, AU - Halama,M, AU - Byrne,J M, AU - Obst,M, AU - Kleindienst,S, AU - Behrens,S, AU - Kappler,A, Y1 - 2017/06/16/ PY - 2017/03/30/received PY - 2017/04/25/accepted PY - 2017/4/30/pubmed PY - 2017/12/26/medline PY - 2017/4/30/entrez KW - cell-mineral aggregates KW - green rust KW - nitrate-dependent Fe(II) oxidation JF - Applied and environmental microbiology JO - Appl. Environ. Microbiol. VL - 83 IS - 13 N2 - 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 Gallionella and Sideroxydans) 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 (Nocardioides and Rhodanobacter) 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.IMPORTANCE 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. SN - 1098-5336 UR - https://www.unboundmedicine.com/medline/citation/28455336/Insights_into_Nitrate_Reducing_Fe_II__Oxidation_Mechanisms_through_Analysis_of_Cell_Mineral_Associations_Cell_Encrustation_and_Mineralogy_in_the_Chemolithoautotrophic_Enrichment_Culture_KS_ L2 - http://aem.asm.org/cgi/pmidlookup?view=long&pmid=28455336 DB - PRIME DP - Unbound Medicine ER -