Abstract
BackgroundMagnetotactic bacteria are capable of synthesizing magnetosomes only under oxygen-limited conditions. However, the mechanism of the aerobic repression on magnetite biomineralization has remained unknown. In Escherichia coli and other bacteria, Fnr (fumarate and nitrate reduction regulator) proteins are known to be involved in controlling the switch between microaerobic and aerobic metabolism. Here, we report on an Fnr-like protein (MgFnr) and its role in growth metabolism and magnetite biomineralization in the alphaproteobacterium Magnetospirillum gryphiswaldense.ResultsDeletion of Mgfnr not only resulted in decreased N2 production due to reduced N2O reductase activity, but also impaired magnetite biomineralization under microaerobic conditions in the presence of nitrate. Overexpression of MgFnr in the WT also caused the synthesis of smaller magnetite particles under anaerobic and microaerobic conditions in the presence of nitrate. These data suggest that proper expression of MgFnr is required for WT-like magnetosome synthesis, which is regulated by oxygen. Analyses of transcriptional gusA reporter fusions revealed that besides showing similar properties to Fnr proteins reported in other bacteria, MgFnr is involved in the repression of the expression of denitrification genes nor and nosZ under aerobic conditions, possibly owing to several unique amino acid residues specific to MTB-Fnr.ConclusionsWe have identified and thoroughly characterized the first regulatory protein mediating denitrification growth and magnetite biomineralization in response to different oxygen conditions in a magnetotactic bacterium. Our findings reveal that the global oxygen regulator MgFnr is a genuine O2 sensor. It is involved in controlling expression of denitrification genes and thereby plays an indirect role in maintaining proper redox conditions required for magnetite biomineralization.
Highlights
Magnetotactic bacteria are capable of synthesizing magnetosomes only under oxygen-limited conditions
Sharing similar characteristics with Fnr of other bacteria, MgFnr is able to repress the transcription of denitrification genes under aerobic conditions, possibly owing to several unique amino acid residues specific to Magnetotactic bacteria (MTB)-Fnr
WT overexpressing Mgfnr (WT + pLYJ110) produced smaller magnetite particles under anaerobic conditions (30.3 ± 15.1 nm, which was similar to that of WT in microaerobic nitrate medium) (Table 1, Additional file 1) and under microaerobic conditions in the presence of nitrate (23.5 ± 13.8 nm versus 30.5 ± 12.4 in WT). This indicated that MgFnr is involved in magnetosome formation during nitrate reduction, and that the expression level of MgFnr is crucial for proper magnetite biomineralization
Summary
Magnetotactic bacteria are capable of synthesizing magnetosomes only under oxygen-limited conditions. Whereas aerobic conditions completely inhibit magnetite biomineralization [5,10] It is unknown whether this aerobic repression is controlled by biological regulation, or alternatively, directly caused by chemical oxidation of iron ions within the cells. Deletion of nap genes encoding a periplasmic nitrate reductase abolished anaerobic growth and delayed aerobic growth in both nitrate and ammonium medium, and severely impaired magnetite biomineralization and resulted in biosynthesis of fewer, smaller and irregular crystals during denitrification and microaerobic respiration [5]. Loss of the nitrite reductase gene nirS led to defective growth of cells, which synthesized fewer, smaller and irregular crystals during nitrate reduction [6]. Transcriptional gusA fusions revealed that expression of nap is upregulated by oxygen, whereas other denitrification genes including nirS, nor, and nosZ display the highest expression under microaerobic conditions in the presence of nitrate [5]
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