Controls on Iron Reduction and Biomineralization over Broad Environmental Conditions as Suggested by the FirmicutesOrenia metallireducensStrain Z6

Abstract

Microbial iron reduction is a ubiquitous biogeochemical process driven by diverse microorganisms in a variety of environments. However, it is often difficult to separate the biological from the geochemical controls on bioreduction of Fe­(III) oxides. Here, we investigated the primary driving factor(s) that mediate secondary iron mineral formation over a broad range of environmental conditions using a single dissimilatory iron reducer, Orenia metallireducens strain Z6. A total of 17 distinct geochemical conditions were tested with differing pH (6.5–8.5), temperature (22–50 °C), salinity (2–20% NaCl), anions (phosphate and sulfate), electron shuttle (anthraquinone-2,6-disulfonate), and Fe­(III) oxide mineralogy (ferrihydrite, lepidocrocite, goethite, hematite, and magnetite). The observed rates and extent of iron reduction differed significantly with k int between 0.186 and 1.702 mmol L–1 day–1 and Fe­(II) production ranging from 6.3% to 83.7% of the initial Fe­(III). Using X-ray absorption and scattering techniques (EXAFS and XRD), we identified and assessed the relationship between secondary minerals and the specific environmental conditions. It was inferred that the observed bifurcation of the mineralization pathways may be mediated by differing extents of Fe­(II) sorption on the remaining Fe­(III) minerals. These results expand our understanding of the controls on biomineralization during microbial iron reduction and aid the development of practical applications.

Effects of Fe(III) Oxide Mineralogy and Phosphate on Fe(II) Secondary Mineral Formation during Microbial Iron Reduction

“…In addition to the presence/concentration of phosphate, other factors have been proposed to contribute to the formation of green rusts during Fe(III) oxide bioreduction, including the presence of other oxyanions (arsenate, silicate, molybdate, tungstate, etc.) [31,41]; the presence and nature of dissolved organic carbon (including humic substances and microbially produced extracellular polymeric materials) [31,33,38]; the species and population size of IRB [31][32][33]; the type and concentration of the electron donor [18,36,37]; the rate and extent of Fe(II) production [17,19,125]; the presence of electron shuttles [17]; the sorption of Fe(II) to the parent Fe(III) oxide [25]; the extent of aggregation of Fe(III) oxide particles [27]; Fe(III) oxide mineralogy (this study). Despite over 20 years of investigation, a definitive and comprehensive understanding of the key factor(s) and mechanisms of green rust formation during microbial Fe(III) oxide reduction remains elusive.…”

“…These phylogenetically diverse microorganisms couple the oxidation of an electron donor (organic compounds or molecular hydrogen, H 2 ) to the reduction of Fe(III) to Fe(II) [1][2][3][4][5][6][7][8][9][10][11][12][13][14][15]. The Fe(II), resulting from the microbial reduction of Fe(III) oxides, can be present as a broad range of Fe(II) species, including soluble and adsorbed Fe(II) and mineral phases containing structural Fe(II) (e.g., magnetite (Fe 3 O 4 ), siderite (FeCO 3 ), vivianite [Fe 3 (PO 4 ) 2 •8H 2 O], green rust, chukanovite [Fe 2 (OH) 2 CO 3 ], and Fe(II)-bearing clays) [16][17][18][19][20][21][22][23][24][25].…”

“…Many factors have been identified as contributing to the formation of specific Fe(II)bearing secondary minerals during the microbial reduction of Fe(III) oxides, including Fe(III) oxide mineralogy [19,25,26]; Fe(III) oxide particle aggregation [27]; the presence of electron shuttles [17]; the rate and extent of Fe(II) production [17,19,[28][29][30]; the extent of Fe(II) sorption on the parent Fe(III) oxide [25]; the species of IRB and the number of cells present [31][32][33]; the concentration and type of electron donor [34][35][36][37]; the type of organic matter present (including humic substances and microbially-produced extracellular polymeric materials) [31,33,38]; and the presence of phosphate and other oxyanions (silicate, molybdate, arsenate, etc.) [17,31,[39][40][41].…”

Elucidating Heterogeneous Iron Biomineralization Patterns in a Denitrifying As(III)-Oxidizing Bacterium: Implications for Arsenic Immobilization

“…Moreover, as absorption correction is not included in the STEM-EDS quantification, this analysis is likely to overestimate the Fe content, since higher energy Fe X-rays will be absorbed less strongly than the lower energy oxygen. Goethite and particularly lepidocrocite, can be susceptible to bioreduction 64, 65 , potentially remobilizing As. However, the crystalline “flakes” (developed after a longer incubation) were As deficient, in contrast to the amorphous spherical NPs, which retained more As, as shown by STEM-EDS analysis.…”

Reduction of Vanadium(V) by Iron(II)-Bearing Minerals

“…Microbial reduction of V(V) typically leads to the formation of V(IV) species (i.e., soluble complexes and various precipitates); however, reduction to V(III) has been reported [18,22,28]. In addition to direct microbial reduction of V(V), microbes can indirectly impact V speciation/mobility by altering the geochemical conditions of their environment, particularly microbes involved in the biogeochemical cycling of Fe and S. Microbial reduction of ferric iron (Fe(III)) can result in the formation of a broad range of Fe(II) species including mineral phases containing structural Fe(II) (e.g., magnetite (Fe 3 O 4 ) , siderite (FeCO 3 ), vivianite [Fe 3 (PO 4 ) 2 •8H 2 0], green rust (a mixed Fe(II)/Fe(III) layered double hydroxide), and chukanovite [Fe 2 (OH) 2 CO 3 ]) [41][42][43][44][45][46][47][48][49][50][51]. Likewise, microbial reduction of oxidized S species such as sulfate, sulfite, and thiosulfate, and S(0), results in the production of sulfide, and its subsequent reaction with Fe(II) leads to the formation of insoluble ferrous sulfides such as mackinawite (FeS), greigite (Fe 3 S 4 ), pyrite (FeS 2 ), and pyrrhotite (Fe (1-x) S (x = 0 to 0.2)) [52][53][54][55][56][57][58].…”