Fe(III) (oxyhydr)oxide reduction by the thermophilic iron-reducing bacterium Desulfovulcanus ferrireducens

Elizabeth C Sklute; Deborah A Leopo; Kaylee A Neat; Kenneth J T Livi; M Darby Dyar; James F Holden

doi:10.3389/fmicb.2023.1272245

Fe(III) (oxyhydr)oxide reduction by the thermophilic iron-reducing bacterium Desulfovulcanus ferrireducens

Front Microbiol. 2023 Oct 20:14:1272245. doi: 10.3389/fmicb.2023.1272245. eCollection 2023.

Authors

Elizabeth C Sklute^{1

2}, Deborah A Leopo³, Kaylee A Neat⁴, Kenneth J T Livi⁵, M Darby Dyar^{1

4}, James F Holden³

Affiliations

¹ Planetary Science Institute, Tucson, AZ, United States.
² Los Alamos National Laboratory, Los Alamos, NM, United States.
³ Department of Microbiology, University of Massachusetts, Amherst, MA, United States.
⁴ Department of Astronomy, Mount Holyoke College, South Hadley, MA, United States.
⁵ Department of Materials Science and Engineering, Johns Hopkins University, Baltimore, MD, United States.

Abstract

Some thermophilic bacteria from deep-sea hydrothermal vents grow by dissimilatory iron reduction, but our understanding of their biogenic mineral transformations is nascent. Mineral transformations catalyzed by the thermophilic iron-reducing bacterium Desulfovulcanus ferrireducens during growth at 55°C were examined using synthetic nanophase ferrihydrite, akaganeite, and lepidocrocite separately as terminal electron acceptors. Spectral analyses using visible-near infrared (VNIR), Fourier-transform infrared attenuated total reflectance (FTIR-ATR), and Mössbauer spectroscopies were complemented with x-ray diffraction (XRD) and transmission electron microscopy (TEM) using selected area electron diffraction (SAED) and energy dispersive X-ray (EDX) analyses. The most extensive biogenic mineral transformation occurred with ferrihydrite, which produced a magnetic, visibly dark mineral with spectral features matching cation-deficient magnetite. Desulfovulcanus ferrireducens also grew on akaganeite and lepidocrocite and produced non-magnetic, visibly dark minerals that were poorly soluble in the oxalate solution. Bioreduced mineral products from akaganeite and lepidocrocite reduction were almost entirely absorbed in the VNIR spectroscopy in contrast to both parent minerals and the abiotic controls. However, FTIR-ATR and Mössbauer spectra and XRD analyses of both biogenic minerals were almost identical to the parent and control minerals. The TEM of these biogenic minerals showed the presence of poorly crystalline iron nanospheres (50-200 nm in diameter) of unknown mineralogy that were likely coating the larger parent minerals and were absent from the controls. The study demonstrated that thermophilic bacteria transform different types of Fe(III) (oxyhydr)oxide minerals for growth with varying mineral products. These mineral products are likely formed through dissolution-reprecipitation reactions but are not easily predictable through chemical equilibrium reactions alone.

Keywords: Mössbauer spectroscopy; akaganeite; ferrihydrite; iron reduction; lepidocrocite; magnetite; reflectance spectroscopy; thermophile.

Grants and funding

The author(s) declare financial support was received for the research, authorship, and/or publication of this article. This study was supported by a grant from the NASA Exobiology Program (80NSSC18K1296).