Cited by 120Geomagnetism and Paleomagnetism StudiesMicrobial Fuel Cells and BioremediationMetalloenzymes and iron-sulfur proteins

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The Periplasmic Nitrate Reductase Nap Is Required for Anaerobic Growth and Involved in Redox Control of Magnetite Biomineralization in Magnetospirillum gryphiswaldense

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Li, Yingjie, Katzmann, Emanuel, Borg, Sarah, Schüler, Dirk·2012·Journal of Bacteriology

DOI 10.1128/jb.00903-12PMC PMC3430331

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Abstract

The magnetosomes of many magnetotactic bacteria consist of membrane-enveloped magnetite crystals, whose synthesis is favored by a low redox potential. However, the cellular redox processes governing the biomineralization of the mixed-valence iron oxide have remained unknown. Here, we show that in the alphaproteobacterium Magnetospirillum gryphiswaldense, magnetite biomineralization is linked to dissimilatory nitrate reduction. A complete denitrification pathway, including gene functions for nitrate (nap), nitrite (nir), nitric oxide (nor), and nitrous oxide reduction (nos), was identified. Transcriptional gusA fusions as reporters revealed that except for nap, the highest expression of the denitrification genes coincided with conditions permitting maximum magnetite synthesis. Whereas microaerobic denitrification overlapped with oxygen respiration, nitrate was the only electron acceptor supporting growth in the entire absence of oxygen, and only the deletion of nap genes, encoding a periplasmic nitrate reductase, and not deletion of nor or nos genes, abolished anaerobic growth and also delayed aerobic growth in both nitrate and ammonium media. While loss of nosZ or norCB had no or relatively weak effects on magnetosome synthesis, deletion of nap severely impaired magnetite biomineralization and resulted in fewer, smaller, and irregular crystals during denitrification and also microaerobic respiration, probably by disturbing the proper redox balance required for magnetite synthesis. In contrast to the case for the wild type, biomineralization in Δ nap cells was independent of the oxidation state of carbon substrates. Altogether, our data demonstrate that in addition to its essential role in anaerobic respiration, the periplasmic nitrate reductase Nap has a further key function by participating in redox reactions required for magnetite biomineralization.

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Authors: Li, Y., Katzmann, E., Borg, S., & Schüler, D.
Affiliations: Ludwig-Maximilians-Universität München (DE)
ORCID: Li, Yingjie
Borg, Sarah
Schüler, Dirk
Venue: Journal of Bacteriology
Publisher: American Society for Microbiology
Published: 2012-06-22
Volume: 194
Issue: 18
Pages: 4847-4856
ISSN: 0021-9193 (ISSN-L)
1098-5530
DOI: 10.1128/jb.00903-12
PMC: PMC3430331
OpenAlex: W2117447208
Cited by: 117
References: 71
Citations by year: 2026: 8 · 2025: 9 · 2024: 8 · 2023: 7 · 2022: 10 · 2021: 9 · 2020: 13 · 2019: 9 · 2018: 4 · 2017: 5 · 2016: 8 · 2015: 3 · 2014: 8 · 2013: 14 · 2012: 1
FWCI: 3.35
Type: journal article
Language: en
Open access: bronze
doi.org
Locations: Journal of Bacteriology (publishedVersion)
Europe PMC (PubMed Central) (publishedVersion)
PubMed Central (publishedVersion)
PubMed (publishedVersion)
ERef Bayreuth (University of Bayreuth) (submittedVersion)
Funders: China Scholarship Council
Topics: Physical Sciences › Earth and Planetary Sciences › Geophysics › Geomagnetism and Paleomagnetism Studies
Physical Sciences › Environmental Science › Environmental Engineering › Microbial Fuel Cells and Bioremediation
Life Sciences › Biochemistry, Genetics and Molecular Biology › Biochemistry › Metalloenzymes and iron-sulfur proteins
Keywords: periplasmic nitrate reductase, NAP, magnetite biomineralization, magnetosomes, Magnetospirillum gryphiswaldense, denitrification, anaerobic respiration, redox regulation, nitrate reduction, magnetotactic bacteria, nosZ, gene expression regulation
MeSH terms: Quaternary Ammonium Compounds, Anaerobiosis, Culture Media, Nitrates, Oxidation-Reduction, Gene Deletion, Gene Expression Profiling, Magnetospirillum, Nitrate Reductase, Ferrosoferric Oxide, Metabolic Networks and Pathways

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The Periplasmic Nitrate Reductase Nap Is Required for Anaerobic Growth and Involved in Redox Control of Magnetite Biomineralization in Magnetospirillum gryphiswaldense

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