Abstract
Microorganisms capable of anaerobic nitrate-dependent Fe(II) (ferrous iron) oxidation (ANDFO) contribute significantly to iron and nitrogen cycling in various environments. However, lab efforts in continuous cultivation of ANDFO strains suffer from loss of activity when ferrous iron is used as sole electron donor. Here, we used a novel strain of nitrate-dependent Fe(II)-oxidizing bacterium Bacillus ferroxidians as a model and focused on the physiological activity of cells during ANDFO. It was shown that B. ferrooxidans entered a metabolically inactive state during ANDFO. B. ferrooxidans exhibited nitrate reduction coupled with Fe(II) oxidation, and the activity gradually declined and was hardly detected after 48-h incubation. Propidium monoazide (PMA) assisted 16S rRNA gene real-time PCR suggested that a large number of B. ferrooxidans cells were alive during incubation. However, 2H(D)-isotope based Raman analysis indicated that the cells were metabolically inactive after 120-h of ANDFO. These inactive cells re-awakened in R2A medium and were capable of growth and reproduction, which was consistent with results in Raman analysis. Scanning electron microscopy (SEM) observation and x-ray diffraction (XRD) revealed the formation of Fe minerals in close proximity of cells in the Fe(II)-oxidizing medium after Fe(II) oxidation. Overall, our results demonstrated that continued ANDFO can induce a metabolically inactive state in B. ferrooxidans, which was responsible for the loss of activity during ANDFO. This study provides an insight into the ANDFO process and its contribution to iron and nitrogen cycling in the environments.
Highlights
An important nitrogen turnover process of nitrate reduction is closely linked to Fe(II)-oxidation under anoxic conditions, contributing greatly to nitrogen and iron cycling in the environment (Weber et al, 2006; Borch et al, 2010; Melton et al, 2014)
The strain of B. ferrooxidans was isolated from a paddy soil collected in Yingtan, China (116◦82 E, 28◦2 N) (Zhou et al, 2016, 2018)
We found that the iron oxidation capacity of the strain B. ferrooxidans decreased with increasing numbers of transfers, and almost no growth was observed in the Fe(II)-oxidizing medium (FeOM)
Summary
An important nitrogen turnover process of nitrate reduction is closely linked to Fe(II)-oxidation under anoxic conditions, contributing greatly to nitrogen and iron cycling in the environment (Weber et al, 2006; Borch et al, 2010; Melton et al, 2014). Inactivity and Re-awakening of Bacillus ferrooxidans nitrate reduction (including NO2−, NO, and N2O) as electron acceptors with the iron (II) as electron donor (Weber et al, 2006). Most of the isolated ANDFO strains grow mixotrophically, including Acidovorax sp. Continuous cultivation with ferrous iron as sole electron donor is impossible for most of these ANDFO bacteria (Kappler, 2005). These strains cannot oxidize ferrous iron in absence of an organic substrate. Little is known about this phenomenon; e.g., the physiological activity of the cells during ANDFO has not been described and it is not known whether iron oxidation may induce a metabolically inactive state
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