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bioRxiv · 10.1101/2023.09.04.556225

"Candidatus Siderophilus nitratireducens": a psychrophilic, nap-dependent nitrate-reducing iron oxidizer within the new order Siderophiliales

Corbera-Rubio, F.·Stouten, G. R.·Bruins, J.·Dost, S. F.·Merkel, A. Y.·Muller, S.·van Loosdrecht, M. C. M.·van Halem, D.·Laureni, M.
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Abstract

Nitrate leaching from agricultural soils is increasingly found in groundwater, a primary source of drinking water worldwide. This nitrate influx can potentially stimulate the biological oxidation of iron in anoxic groundwater reservoirs. Nitrate-reducing iron-oxidizing (NRFO) bacteria have been extensively studied in laboratory settings, yet their ecophysiology in natural environments remains largely unknown. To this end, we established a pilot-scale filter on nitrate-rich groundwater to elucidate the structure and metabolism of nitrate-reducing iron-oxidizing microbiomes under oligotrophic conditions mimicking natural groundwaters. The enriched community stoichiometrically removed iron and nitrate consistently with NRFO metabolism. Genome-resolved metagenomics revealed the underlying metabolic network between the dominant iron-dependent denitrifying autotrophs and the less abundant organoheterotrophs. The most abundant genome belonged to a new Candidate order, named Siderophiliales. This new species, "Candidatus Siderophilus nitratireducens", carries central genes to iron oxidation (cytochrome c cyc2), carbon fixation (rbc), and for the sole periplasmic nitrate reductase (nap). To our knowledge, this is the first report of nap-based lithoautotrophic growth, and we demonstrate that iron oxidation coupled to dissimilatory reduction of nitrate to nitrite is thermodynamically favourable under realistic Fe3+/Fe2+ and [Formula] concentration ratios. Ultimately, by bridging the gap between laboratory investigations and real-world conditions, this study provides insights into the intricate interplay between nitrate and iron in groundwater ecosystems, and expands our understanding of NRFOs taxonomic diversity and ecological role.

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Corbera-Rubio, F., Stouten, G. R., Bruins, J., Dost, S. F., Merkel, A. Y., Muller, S., van Loosdrecht, M. C. M., van Halem, D., Laureni, M.. 2023-09-04. "Candidatus Siderophilus nitratireducens": a psychrophilic, nap-dependent nitrate-reducing iron oxidizer within the new order Siderophiliales. https://doi.org/10.1101/2023.09.04.556225

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