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Article

Effect of CO2 Concentration on the Microbial Activity of Orenia metallireducens (Strain Z6) in Surface Inert Materials

by
Shuyi Li
1,
Wentao Song
1,
Juan Liu
2,
Maxim I. Boyanov
3,4,
Edward J. O’Loughlin
3,
Kenneth M. Kemner
3,
Robert A. Sanford
5,
Hongbo Shao
6,
Qi Feng
1,
Yu He
1,
Yiran Dong
1,7,8,9,10,* and
Liang Shi
1,7,8
1
School of Environmental Studies, China University of Geosciences, Wuhan 430074, China
2
Department of Environmental Engineering, Peking University, Beijing 100871, China
3
Biosciences Division, Argonne National Laboratory, Lemont, IL 60439, USA
4
Institute of Chemical Engineering, Bulgarian Academy of Sciences, 1113 Sofia, Bulgaria
5
Department of Earth Science & Environmental Change, University of Illinois Urbana-Champaign, Champaign, IL 60801, USA
6
Illinois State Geological Survey, Champaign, IL 61820, USA
7
State Environmental Protection Key Laboratory of Source Apportionment and Control of Aquatic Pollution, Ministry of Ecology and Environment, Wuhan 430074, China
8
Hubei Key Laboratory of Yangtze Catchment Environmental Aquatic Science, China University of Geosciences, Wuhan 430074, China
9
Hubei Key Laboratory of Wetland Evolution & Ecological Restoration, China University of Geosciences, Wuhan 430074, China
10
MOE Key Laboratory of Groundwater Quality and Health, School of Environmental Studies, China University of Geosciences, Wuhan 430078, China
*
Author to whom correspondence should be addressed.
Minerals 2025, 15(2), 112; https://doi.org/10.3390/min15020112
Submission received: 11 December 2024 / Revised: 10 January 2025 / Accepted: 20 January 2025 / Published: 24 January 2025
(This article belongs to the Special Issue Redox Reactivity of Iron Minerals in the Geosphere, 2nd Edition)
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Abstract

:
Carbon dioxide (CO2) sequestration has garnered widespread attention as a key strategy for mitigating CO2 emissions and combating the greenhouse effect. However, the mechanisms underlying the interactions between CO2, widespread siliceous minerals and biological processes remain unclear. The present study explored the potential impacts of different CO2 concentrations on microbial activity, environmental conditions and their feedback on the fate of CO2. A total of 20 experimental conditions was created, with the variables including different natural and synthetic siliceous minerals (e.g., quartz sand and a type of commercial glass beads), the presence or absence of the iron-reducing microorganism Orenia metallireducens (strain Z6) and varying CO2 concentrations (0%, 20%, 50%, 100%) in the presence of ferrihydrite and pyruvate. Geochemical, microbial and mineralogical analyses revealed that elevated CO2 concentrations significantly inhibited microbial Fe(III) reduction and pyruvate metabolism. Interestingly, compared to cultures without mineral amendments or those with glass beads alone, the addition of quartz sand enabled strain Z6 to better withstand the environmental stress caused by elevated CO2, promoting pyruvate fermentation and iron reduction. In addition to an increased pH, the formation of siderite, hematite and vivianite was also observed in the bioactive systems. Although both glass beads and quartz sand were primarily composed of silica, differences in the mineral structure, elemental composition and acid neutralization capacity rendered quartz sand more chemically active and unexpectedly led to greater CO2 sequestration.

Graphical Abstract

1. Introduction

Carbon sequestration refers to the process of capturing and storing carbon dioxide (CO2) from the atmosphere through natural processes such as forest carbon fixation and soil carbon storage, or from industrial processes through engineering means including carbon capture, utilization and storage (CCUS) to reduce atmospheric CO2 concentrations and mitigate climate change [1,2,3,4]. The fate of CO2 in subsurface environments involves its interactions with minerals, water and microorganisms, and these have garnered intense attention. Elevated CO2 levels can influence environmental conditions in multiple ways, affecting physical and chemical properties in aquifers and minerals (e.g., pH, salinity, redox potential and mineral stability), potentially promoting complex biogeochemical cycles that govern the distribution of CO2 between solid, aqueous and gaseous phases [5]. Furthermore, microorganisms play vital roles in mediating CO2 transport and transformation, including microbially driven mineralization, carbon fixation and other metabolic processes. Thus, understanding the multi-faceted interactions between CO2, minerals, water and microbes is crucial for predicting the stability and effectiveness of CO2 sequestration, as well as its potential environmental impacts, such as acidification or the mobilization of toxic elements [5,6,7].
Despite significant advances in the understanding of the biogeochemical processes involved in CO2 sequestration, substantial knowledge gaps remain regarding the role of microbe–mineral–CO2–water interactions in shaping the fate of CO2. In terrestrial and marine environments, microbial communities influence mineral dissolution, precipitation and the overall stability of CO2 in environmental systems with elevated CO2 concentrations (e.g., geological storage sites) [8,9,10]. Due to the widespread distribution of iron in natural and engineered environments, the microorganisms involved in iron cycling are ubiquitous and play significant roles in the biogeochemistry of iron and other elements [8]. Furthermore, elevated CO2 concentrations may enhance certain biogeochemical processes. For example, under elevated CO2 concentrations, microbial dissimilatory iron reduction becomes thermodynamically more favorable. Some dissimilatory iron-reducing microorganisms (e.g., Orenia metallireducens and Clostridium acetobutylicum) could catalyze iron reduction to neutralize environmental acidification during the decomposition of organic compounds (e.g., glucose) and create stable pH conditions to support sustained cell growth [8,10,11,12]. However, in our previous work, we found that when the CO2 concentration reaches 100%, the iron-reducing microorganism Orenia metallireducens is unable to create favorable pH conditions through catalytic iron reduction to resist the stress of high CO2 concentration [9].
Silicon (Si) is one of the most abundant elements on Earth, constituting a significant portion of the Earth’s crust in the form of silicate minerals, with silicon dioxide (SiO2) or silica being a primary constituent. In natural environments, silica is most commonly encountered as quartz sand. Due to its chemical stability, SiO2 is widely distributed in natural environments and has been a key component in many geological processes. However, due to its “nominal” chemical inertness, the role of Si and its interactions with other compounds in the environment remains under-investigated, particularly in the context of carbon sequestration.
This study aimed to investigate (1) whether and how quartz sand, a widely distributed and chemically “inert” siliceous mineral, influences microbial activities (e.g., dissimilatory Fe(III) reduction) and biogeochemistry under different CO2 concentrations; and (2) how environmental factors and microbial metabolism, influenced by different CO2 concentrations, mediate the fate of CO2. A series of experimental conditions was created and multidisciplinary approaches were employed to analyze the concurrent processes of CO2 dissolution, microbial metabolism and secondary mineral formation. The potential impact on CO2 sequestration was also evaluated.

2. Methods and Material

2.1. Chemicals and Mineral Preparation and Characterization

All chemicals used in the study were of analytical grade or better and were purchased from Sigma-Aldrich (Shanghai) Co., Ltd. (Shanghai, China), Shanghai Macklin Biochemical Co., Ltd. (Shanghai, China) or Sinopharm Chemical Reagent Co., Ltd. (Shanghai, China). All solutions were prepared using deionized water (≥18 MΩ). The quartz sand was the product of Shanghai Macklin Biochemical Co., Ltd. (Shanghai, China). The high-purity SiO2 glass beads (100 mm in diameter) were bought from BioSpec Product Inc. (BioSpec Products Inc., Bartlesville, OK, USA) [13]. The average particle size and the specific surface area of these two materials are presented in Table 1. Amorphous 2-line ferrihydrite (Feh) was synthesized using the method introduced by Cornell and Schwertmann [14]. The purchased and synthesized minerals were characterized with an Empyrean® NED X-ray Diffractometer (XRD) (Malvern Panalytical, Great Malvern, UK).

2.2. Development of Batch Cultures

Orenia metallireducens strain Z6 (strain Z6) was isolated from briny groundwater from a 2.02 km deep borehole in the Illinois Basin, IL, USA [15]. Previous studies have found that strain Z6 can grow under a broad range of environmental conditions. It can also catalyze iron metabolism and form biominerals during reduction of oxidized iron-containing minerals. The organism was pre-grown in a synthetic groundwater medium (strain Z6) amended with 10 mM glucose [15]. After 34 h, when all the glucose was consumed and the OD600 was ~0.3, the culture was transferred into fresh modified strain Z6 media equilibrated with N2 using sterile syringes at a volume ratio of 1:20. The starting cell concentration was ~1 × 107 cells/mL. In the modified media, the bicarbonate buffer was replaced with 10 mM 4-(2-hydroxyethyl)-1-piperazineethanesulfonic acid (HEPES), and the pH was adjusted to 7.2 using freshly prepared 1 M NaOH [10]. The media (80 mL) were distributed into 100 mL serum bottles and equilibrated with gas or gas mixtures containing different CO2 concentrations (Table 2). The bottles were sealed with butyl rubber stoppers and aluminum seals before being autoclaved at 120 °C for 20 min. Then, 20 mM ferrihydrite and 16.5 mM pyruvate were amended as the electron acceptor and electron donor, respectively. All the amendments were added using sterile and N2-flushed syringes. Details of ferrihydrite, natural minerals and the inoculation conditions are provided in Table 2.
For the batch cultures, four gas conditions were created by purging the modified strain Z6 medium with one of the four gases (e.g., N2, N2:CO2 (80:20, v:v), N2:CO2 (50:50, v:v), and CO2) (Wuhan Iron and Steel Corporation, Wuhan, China), resulting in initial pH values of 7.17 ± 0.01, 6.27 ± 0.04, 5.76 ± 0.04 and 5.46 ± 0.02, respectively (Conditions 1–5, 6–10, 11–15 and 16–20 in Table 2). The intermediate and high CO2 concentrations were selected to simulate natural and anthropogenic “CO2 hotspots”, respectively [16,17]. Under each gas condition, the cultures were divided into five groups: cultivation of strain Z6 in the presence of glass beads or quartz sand (GB/QS + Z6), cultivation of strain Z6 only (Z6) and the abiotic controls containing only glass beads or quartz sand (GB/QS) (Table 2).
The quartz sand and glass beads were initially cleaned with acetone by thoroughly mixing and shaking for 6 h. The liquid was discarded, and the minerals were washed 10 times with ultrapure water. The cleaned mineral was then dried in an oven before being aliquoted, wrapped in aluminum foil, sterilized and moved into an anaerobic chamber (Vigor Technologies (Suzhou) Co., Ltd., Suzhou, China) filled with N2. To develop the systems containing glass beads or quartz sand, the serum bottles with sterile medium were transferred into the anaerobic chamber at least one day before the experimental setup to remove oxygen. The serum bottles were opened and supplemented with one of the sterile minerals (130 mmol/L). After adding the mineral, the bottles were quickly resealed with sterile blue stoppers and aluminum caps, removed from the anaerobic chamber and flushed with the corresponding filter-sterilized gas. These mineral-amended systems were equilibrated for at least 24 h before inoculation. The cultures were incubated static at 37 °C and manually shaken once daily.

2.3. Sample Collection, Pretreatment and Analyses

At each time point, 2.2 mL of thoroughly mixed culture was collected using sterile syringes flushed with nitrogen (N2). Inside an anaerobic chamber, 0.2 mL of the sample was quickly filtered through a 0.45 μm syringe filter (Tianjin Jinteng Laboratory Instruments Co., Ltd., Tianjin, China) and mixed with an equal volume of 1 M HCl for the determination of dissolved Fe(II) [Fe(II)(aq)]. Another 0.2 mL of culture was mixed with an equal volume of 1.0 M HCl to determine 0.5 M acid-extractable Fe(II) [Fe(II)TOT]. Ferrous iron was measured using the ferrozine method and quantified using a UV-Vis spectrophotometer (Thermo Fisher Scientific, Waltham, MA, USA) at 560 nm in wavelength [18]. Additionally, 1 mL of the culture was centrifuged at 4000× g for 5 min, and the supernatant was carefully transferred to a sterile microcentrifuge tube and stored at −20 °C for the determination of soluble organic products. The concentrations of short-chain fatty acids were analyzed using a high-performance liquid chromatography (HPLC) (Shimadzu Corporation, Kyoto, Japan) installed with an Aminex HPLC column (Bio-Rad Laboratories, Inc., Hercules, CA, USA). The column temperature was 50 °C and the mobile phase consisting of 5 mM chromatography-grade sulfuric acid and a flow rate of 0.6 mL/min were employed for the qualification and quantification of the short-chain fatty acids [8,19].
At selected time points, an additional 11 mL of thoroughly mixed culture was collected inside the anaerobic chamber. A total of 1 mL of the culture was used for pH measurement, while the remaining culture was filtered through a 0.22 μm polycarbonate membrane (Tianjin Jinteng Laboratory Instruments Co., Tianjing, Ltd.). The membrane was immediately covered with Kapton tape and placed in a conical tube to minimize the risk of air exposure during transport for Empyrean XRD analysis (Malvern Panalytical, Great Malvern, UK) [20]. The test conditions were as follows: Cu target as the radiation source, Kα radiation, tube voltage of 40 kV, tube current of 30 mA, scanning range of 2θ = 10–70° and scanning speed of 5°/min. The results were analyzed using Jade 6.5 (Materials Data Inc, Livermore, CA, USA). At the end of the experiments, samples were collected for scanning electron microscopy (SEM) (Carl Zeiss AG, Thuringia, Germany) analyses [10]. The aqueous geochemistry and Eh-pH modeling of potential secondary minerals were performed using Geochemist’s Workbench (GWB) (v. 12) (Aqueous Solutions LLC., Champaign, IL, USA).
An additional 5 mL of the sample was centrifuged and dried at 105 °C for 4 h for Fourier-transform infrared spectroscopy (FTIR) analysis (Thermo Fisher Scientific Inc., Waltham, MA, USA). The dried sample was mixed with KBr crystal at a ratio of approximately 1:100, thoroughly ground in an agate mortar and pressed into pellets to obtain transparent particles. The FTIR spectra were recorded in the range of 400–4000 cm−1. Each sample was scanned 16 times at a resolution of 4 cm−1. Each spectrum was corrected using pure KBr and ambient air as the background [21].
The Acid Neutralizing Capacity (ANC) of the glass beads and quartz sand was determined following Gilliam’s method as the indicator of the overall buffering capacity of a solution [22]. Briefly, the glass beads and quartz sand were assigned based on “Fizz” rating before neutralization was quantified according to the corresponding rating [22].

3. Results and Discussion

3.1. Effects of CO2 Concentration on Geochemistry and Microbial Metabolism

The impact of elevated CO2 concentrations on the geochemical conditions and metabolic activity of strain Z6 was investigated. Higher CO2 concentrations increased the total concentration of dissolved carbonate species, including H2CO3, HCO3− and CO32−, leading to environmental acidification and causing potential stress and toxicity to microorganisms [23,24,25]. As the CO2 concentrations increased, the medium shifted from circumneutral to mildly acidic conditions with the pH ranging from 7.10 to 5.46 (Figure 1). Concurrently, the microbial iron-reducing activity decreased and the lag phase was extended (Figure 2). For the cultures incubated with quartz sand (QS + Z6) and equilibrated with 0%–20% CO2, the initial pseudo-zero-order iron-reduction rate constants ranged from 5.18 to 5.63 mM/day. When the CO2 concentrations increased to 50% and 100%, however, the initial reaction rate constants decreased to 4.21 and 2.22 mM/day, respectively (Table 2), consistent with earlier studies [9,10,26]. Meanwhile, the ratios for 0.5 M dissolved Fe(II) divided by total Fe exhibited an initial increase followed by a decline. The exception were the cultures equilibrated with 100% CO2, where the ratio increased after 10 days (Figure 2 and Table 2). At the end of the experiments, approximately 60% of ferrihydrite was reduced in the samples with different CO2 concentrations, but the time to reach the peak value was delayed under the conditions with increased CO2 concentrations due to the longer lag phase.
In the bioactive samples, microbial iron reduction was coupled with fermentation of pyruvate, leading to the production of short-chain fatty acids (e.g., acetate and formate) as the major organic products. At 0% and 20% CO2 concentrations, the concentrations of formate and acetate were nearly identical. The biogenic acetate and formate accounted for 46.0%–49.6% and 9.5%–11.5% of the carbon from the pyruvate. However, at 50% CO2, the pyruvate fermentation rate decreased, and the final acetate concentration was lower than that observed under lower CO2 concentrations. At 100% CO2, an extended lag phase was observed, and the final short-chain fatty acid concentrations were lower than those in the groups exposed to lower CO2 treatments. In addition, in the samples containing 100% CO2, some of the cultures (e.g., Z6 and GB + Z6) were completely inhibited (Figure 3).

3.2. Varied Microbial Activity Between the Cultures Grown with Glass Beads and Quartz Sand

In the systems with low CO2 concentration conditions (0% and 20% CO2), the initial rates and levels of microbial ferrihydrite reduction were barely affected by the type of mineral added. At higher CO2 concentrations, however, the systems amended with quartz sand exhibited the highest initial reaction rates compared with those with glass beads or without any mineral. When the cultures were equilibrated with 100% CO2, only the ones amended with quartz sand exhibited microbial iron-reducing activity (Table 1 and Figure 1d) and the production of pyruvate fermentation products (Figure 3d), while microbial metabolism was completely inhibited under the other conditions. Meanwhile, in all our bioactive samples, significant pH increases were observed (Figure 1). This is consistent with earlier studies, demonstrating that microbial iron reduction could counteract environmental acidification, thereby sustaining microbial metabolism [8,27]. Specifically, microbial metabolism of organic compounds produces H+, which can be neutralized by concurrent Fe(III) reduction that consumes H+. For the quartz sand and glass beads used in this work, the former exhibited an ANC of 518.97 (H2SO4) kg/t, while the glass beads showed a negligible ANC (Table 1). This suggests that the quartz sand may react with high concentrations of CO2, leading to a slight increase in pH and/or reduced CO2 stress. This effect might explain why biological activity was sustained under the 100% CO2 (QS + Z6) condition. Additionally, in the systems with high-concentration CO2 (50%–100% CO2) and quartz sand, the initial pH was observed to be 0.1–0.23 units higher compared to the pure Z6 strain group without quartz sand, supporting the neutralization of the acidity by the quartz sand.
While the primary component of both glass beads and quartz sand used in the present study was SiO2, physicochemical and morphological analyses revealed significant differences in their physiochemical and mineralogical properties. Although similar in particle size, the glass beads and natural quartz sand differed considerably in specific surface areas (Table 1). Scanning electron microscopy (SEM) analysis showed a smooth and spherical surface for the glass beads, whereas the quartz sand displayed a rough and cuboidal shape with fractures (Figure 4a,b). Previous studies have shown that mineral pores provide surface sites that promote the formation of biofilms by microorganisms. Specifically, extracellular polymeric substances (EPSs) act as protective barriers, mitigating environmental stress on microorganisms, for example, by blocking porous media to resist CO2 stress [28,29,30]. Meanwhile, organic molecules in EPSs contain abundant negatively charged functional groups (e.g., carboxyl, hydroxyl and, to a lesser extent, carbonyl groups) that can effectively chelate cations such as Ca2+ and Mg2+, thereby serving as binding sites for carbonate nucleation and growth. These nuclei eventually develop into mineral particles [31]. Furthermore, the calcium content in the quartz sand was approximately four-times higher than that in the glass beads, which may enhance the chelation of EPSs to form secondary mineral binding sites (Figure 4e).
To further investigate whether quartz sand provides binding sites for secondary minerals more effectively, we conducted FTIR spectroscopy. The spectral results revealed characteristic peaks related to Si-O, carbonates, carbonyl groups and hydroxyl groups. The broad peak near 3300 cm−1 corresponds to hydroxyl groups, which may represent the organic portion of iron oxides [32] (Figure 5). The peak around 1620 cm−1 is attributed to the stretching vibration of C=O in organic compounds [33,34]. The characteristic peaks at 1046 and 470 cm−1 are likely attributable to the presence of Si-O [35] (Figure 5). The peak at 1425 cm−1 corresponds to the stretch vibration of carbonate, while the peak at 861 cm−1 is associated with the bending vibration of carbonate [36] (Figure 5). By comparing the presence and absence of strain Z6 under quartz sand conditions, we found that strain Z6 significantly influences the types of functional groups in secondary minerals. In the abiotic control containing only quartz sand, Si-O from quartz sand and possibly C=O from the substrate sodium pyruvate were detected, while in biologically active samples, functional groups such as PO43− (the characteristic peak is observed near 1046 cm−1, while the absorption band near 555 cm−1 corresponds to the vibration of the P-O bond) and C-H (735 cm−1) were additionally observed (Figure 5) [37,38].
In contrast, the biological samples contained a greater variety of characteristic peaks. Additionally, the difference between adding quartz sand or glass beads in the biological samples also influenced the FTIR spectra. Under the 100% CO2 (QS + Z6) condition, characteristic peaks related to Si-O, carbonates, carbonyl groups and hydroxyl groups were observed (Figure 5). This suggests that these functional groups may chelate Ca2+ to serve as nucleation sites for minerals under these conditions.

3.3. Secondary Mineral Characterization

XRD analysis indicated that in the bioactive samples, siderite, vivianite and hematite were formed as the major secondary minerals, while no distinct peaks were observed in the abiotic controls (Figure 6). Under 100% CO2 conditions, the intensity of the XRD peaks for siderite was weaker in the quartz sand-containing system. This may be related to the effects of pH and Eh. On the one hand, varying the concentrations of CO2 influenced the pH, which may result in siderite with different morphologies and degrees of crystallinity. At lower pH conditions, the crystallinity of siderite becomes weaker [9]. On the other hand, although studies suggest that higher concentrations of CO2 favor siderite formation, microbes are more likely to produce magnetite during iron reduction under relatively high Eh conditions [39]. Under such conditions, iron-reduction activity is significantly lower than under other gas conditions. The Eh-pH diagram based on geochemical modeling showed that in the glass bead-containing cultures, the feasible pH range for siderite formation was higher compared to that in the samples with quartz sand (Figure 7), aligning with the lower peak intensity observed in the glass bead-containing bioreactions equilibrated with 50% CO2 (Figure 4d and Figure 6a).
The morphologies of the secondary minerals based on SEM observation supported the results of the XRD analysis (Figure 4 and Figure 6). The siderite varied depending on the experimental conditions. For example, spindle-shaped crystals with diameters of 1–2.5 µm siderite were observed in 0% CO2 GB + Z6, and spherical siderite with the diameter of 3–5 µm formed in 20% and 50% GB + Z6 (Figure 4c–f). This is consistent with earlier studies on the Z6 strain, in which ferrihydrite was reduced to form vivianite [8,9,10]. Similarly, under all the bioactive conditions, vivianite with distinct monoclinic prismatic crystals was observed (Figure 4a).

4. Conclusions

This study demonstrated that under different CO2 conditions, the Si-rich quartz sand and glass beads exhibited different impacts on microbial activity, despite their similarity in having silica as the major constituent. In comparison, glass beads are chemically inert, and their presence does not significantly influence microbial metabolism. By contrast, the quartz sand can facilitate microbial survival to a certain extent under elevated CO2 concentrations. The possible reasons include (1) the larger specific surface area of quartz sands may favor microbial colonization, helping to resist environmental stress; (2) the higher Ca content in quartz sands may bind anions or functional groups, providing nucleation sites for secondary mineral formation; and (3) the stronger acid-neutralizing capacity of quartz sands may partially alleviate CO2 stress for microorganisms. For iron-reducing organisms, the pH increase during the reaction can favor the conversion of carbonate species to the more stable dissolved bicarbonate and carbonate species, while higher CO2 concentrations are favorable for the formation of Fe-containing carbonate minerals (e.g., siderite and carbonate green rust) [10]. Thus, protected microbial iron reduction may favor the stability of CO2, preventing its release into the atmosphere. In summary, the “nominally inert” quartz sand may support microbial survival and activity under high CO2 stress and facilitate the maintenance of biogeochemical processes in challenging environments. Considering the essential roles of microorganisms in the transport and transformation of CO2, our observations may be instructive to better assess their direct and indirect influences on the fate of CO2 in the scenarios associated with CO2-rich environments (e.g., CO2 sequestration).

Author Contributions

Methodology, S.L., W.S. and Q.F.; Formal analysis, S.L., M.I.B., E.J.O. and K.M.K.; Data curation, W.S. and Y.H.; Writing—original draft, S.L.; Writing—review & editing, J.L., R.A.S., H.S., Y.D. and L.S.; Funding acquisition, Y.D. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by National Natural Science Foundation of China: grant no. 41877321, 92051111 and 42272353. Fundamental Research Funds for the Chinese Central Government via China University of Geosciences (Wuhan) under contract 122-G1323522144. MIB, EJO, and KMK were supported in part by the Wetland Hydrobiogeochemistry Science Focus Area (SFA) at Argonne National Laboratory funded by the Environmental Systems Science Research Program, Office of the Biological and Environmental Research, Office of Science, U.S. Department of Energy (DOE), under contract DE-AC02-06CH11357. The APC was funded by Minerals Journal and University of Illinois at Urbana-Champaign IOAP discount.

Data Availability Statement

Due to privacy reasons, the datasets generated or analyzed during this study may not be publicly available. Requests for access can be made by contacting the corresponding author.

Conflicts of Interest

The authors declare no conflict of interest.

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Minerals 15 00112 g001
Figure 1. Changes in pH at 0, 2.5, 12.5 and 45 days of incubation under different experimental conditions. The systems shown in (a–d) were amended with 20 mM ferrihydrite. GB: glass beads-amended only with no cells inoculated; GB + Z6: strain Z6 was incubated in the presence of glass beads; Z6: only strain Z6 was incubated; QS + Z6: strain Z6 was incubated in the presence of quartz sand; QS: quartz sand-amended only and no cells were inoculated. The solid and open histograms indicate active and no microbial iron reduction observed at the designated time points, respectively. The red dashed lines indicate the initial pH of the media before all the amendments were added.
Figure 1. Changes in pH at 0, 2.5, 12.5 and 45 days of incubation under different experimental conditions. The systems shown in (a–d) were amended with 20 mM ferrihydrite. GB: glass beads-amended only with no cells inoculated; GB + Z6: strain Z6 was incubated in the presence of glass beads; Z6: only strain Z6 was incubated; QS + Z6: strain Z6 was incubated in the presence of quartz sand; QS: quartz sand-amended only and no cells were inoculated. The solid and open histograms indicate active and no microbial iron reduction observed at the designated time points, respectively. The red dashed lines indicate the initial pH of the media before all the amendments were added.
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Figure 2. Microbial iron reduction by strain Z6 and Si-containing solids under different CO2 concentrations ((a): 0, (b): 20, (c): 50 and (d): 100%, v:v). The solid lines and the dashed lines indicate 0.5 M HCl-extractable Fe(II) (Fe(II)T) and dissolved Fe(II) (Fe(II)aq), respectively. The plots show the average of triplicates and the error bars indicate the standard deviation of the replicates.
Figure 2. Microbial iron reduction by strain Z6 and Si-containing solids under different CO2 concentrations ((a): 0, (b): 20, (c): 50 and (d): 100%, v:v). The solid lines and the dashed lines indicate 0.5 M HCl-extractable Fe(II) (Fe(II)T) and dissolved Fe(II) (Fe(II)aq), respectively. The plots show the average of triplicates and the error bars indicate the standard deviation of the replicates.
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Figure 3. The major short-chain fatty acids formate and acetate produced during pyruvate fermentation in the samples amended with 20 mM ferrihydrite (a–d). All the samples were prepared in triplicate and the error bars indicate the standard deviation of replicates. In the abiotic controls prepared under the corresponding conditions except for no cell inoculation, no increase in formate and acetate was detected and, thus, are not shown. The dashed line (-F) and the solid line (-A) represent the carbon atom ratios of formate and acetate, respectively, to the consumed pyruvate.
Figure 3. The major short-chain fatty acids formate and acetate produced during pyruvate fermentation in the samples amended with 20 mM ferrihydrite (a–d). All the samples were prepared in triplicate and the error bars indicate the standard deviation of replicates. In the abiotic controls prepared under the corresponding conditions except for no cell inoculation, no increase in formate and acetate was detected and, thus, are not shown. The dashed line (-F) and the solid line (-A) represent the carbon atom ratios of formate and acetate, respectively, to the consumed pyruvate.
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Figure 4. Morphologies of the secondary minerals formed under the designed conditions were characterized using scanning electron microscopy (SEM) and EDS. Panels (a,b) show the SEM characterization of quartz sand and glass beads used in the experiments, respectively. Blue arrows indicate vivianite (Viv), while yellow arrows denote siderite (Sid). Panels (c–f) represent the cultivation conditions with glass beads and strain Z6 under different gas atmospheres.
Figure 4. Morphologies of the secondary minerals formed under the designed conditions were characterized using scanning electron microscopy (SEM) and EDS. Panels (a,b) show the SEM characterization of quartz sand and glass beads used in the experiments, respectively. Blue arrows indicate vivianite (Viv), while yellow arrows denote siderite (Sid). Panels (c–f) represent the cultivation conditions with glass beads and strain Z6 under different gas atmospheres.
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Figure 5. The FTIR spectra under various conditions are shown, with gray translucent rectangles highlighting the characteristic peaks of relevant functional groups.
Figure 5. The FTIR spectra under various conditions are shown, with gray translucent rectangles highlighting the characteristic peaks of relevant functional groups.
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Figure 6. XRD characterization analysis of the secondary minerals. (a) GB + Z6: the strain Z6 culture in the presence of glass beads; (b) Z6: the strain Z6 culture; and (c) QS + Z6: the strain Z6 culture in the presence of quartz sand. In (a), no specific XRD peak was evident since glass beads are amorphous. In (c), as quartz sand with the diameter 0.5–1 mm could not be retrieved using the syringe during sampling, no characteristic peaks for it were detected during XRD characterization.
Figure 6. XRD characterization analysis of the secondary minerals. (a) GB + Z6: the strain Z6 culture in the presence of glass beads; (b) Z6: the strain Z6 culture; and (c) QS + Z6: the strain Z6 culture in the presence of quartz sand. In (a), no specific XRD peak was evident since glass beads are amorphous. In (c), as quartz sand with the diameter 0.5–1 mm could not be retrieved using the syringe during sampling, no characteristic peaks for it were detected during XRD characterization.
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Figure 7. Modeling of pH-Eh under the experimental conditions for secondary mineral formation with the Geochemist’s Workbench (GWB). The medium conditions and the measured biogenic Fe(II) concentrations were applied for modeling.
Figure 7. Modeling of pH-Eh under the experimental conditions for secondary mineral formation with the Geochemist’s Workbench (GWB). The medium conditions and the measured biogenic Fe(II) concentrations were applied for modeling.
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Table 1. The properties of the glass beads and quartz sand used in the experiments.
Table 1. The properties of the glass beads and quartz sand used in the experiments.
MineralsBET a (m2/g)APS b (µm)ANC c (kg/t)Ca (mg/kg)Fe (mg/kg)
Glass Beads0.1903 ± 0.0041457.950.5780,019.31369.34
Quartz Sand1.083 ± 0.0851231.07518.97330,960.13201.04
a BET: the specific surface area of the minerals; b APS: average particle size; c ANC: acid neutralization capacity of the minerals.
Table 2. The experimental conditions developed in the present study, iron-reducing activity and secondary minerals formed a.
Table 2. The experimental conditions developed in the present study, iron-reducing activity and secondary minerals formed a.
IDConditions bGasMineral (mmol/L)Cell Inoculation ckint (mM/day)Maxium Fe(II)aq:Fe(II)TOT (Time, day) dFinal Fe(II)aq:Fe(II)TOTSecondary Minerals e
XRD
1Z6 (0% CO2)N2-Y5.39 0.44 (8)0.27sid, viv, hem
2GB (0% CO2)N2130N----
3GB + Z6 (0% CO2)N2130Y5.44 0.39 (8)0.12sid, viv, hem
4QS (0% CO2)N2130N----
5QS + Z6 (0% CO2)N2130Y5.18 0.44 (8)0.15sid, viv, hem
6Z6 (20% CO2)N2:CO2
(80:20, v:v)		-Y5.14 0.78 (10)0.35sid, viv, hem
7GB (20% CO2)N2:CO2
(80:20, v:v) 		130N----
8GB + Z6 (20% CO2)N2:CO2
(80:20, v:v)		130Y6.34 0.71 (6)0.29sid, viv, hem
9QS (20% CO2)N2:CO2
(80:20, v:v)		130N----
10QS + Z6 (20% CO2)N2:CO2
(80:20, v:v)		130Y5.63 0.59 (6)0.24sid, viv, hem
11Z6 (50% CO2)N2:CO2
(50:50, v:v) 		-Y0.00 0.84 (10)0.39sid, viv, hem
12GB (50% CO2)N2:CO2
(50:50, v:v) 		130N----
13GB + Z6 (50% CO2)N2:CO2
(50:50, v:v) 		130Y0.23 0.82 (10)0.52sid, viv, hem
14QS (50% CO2)N2:CO2
(50:50, v:v) 		130N----
15QS + Z6 (50% CO2)N2:CO2
(50:50, v:v) 		130Y4.21 0.82 (10)0.33sid, viv, hem
16Z6 (100% CO2)CO2-N0.16---
17GB (100% CO2)CO2130N----
18GB + Z6 (100% CO2)CO2130N0.03---
19QS (100% CO2)CO2130N----
20QS + Z6 (100% CO2)CO2130Y2.230.79 (10)0.84sid, viv, hem
a Under all the experimental conditions, the media contained 20 mM ferrihydrite as the electron acceptor and 16.5 mM pyruvate as the electron donor; abiotic controls were prepared in the same manner except for without cell inoculation. b Abbreviations: GB: glass beads; Z6: strain Z6; QS: quartz sand; c Y: with cell inoculation, N: cells were not inoculated. d The highest ratio for aqueous Fe(II) and total acid extractable Fe(II) and the time for the turning point when the trend of the ratios started to decrease. e Abbreviations: sid: siderite; hem: hematite; viv: vivianite.
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Li, S.; Song, W.; Liu, J.; Boyanov, M.I.; O’Loughlin, E.J.; Kemner, K.M.; Sanford, R.A.; Shao, H.; Feng, Q.; He, Y.; et al. Effect of CO2 Concentration on the Microbial Activity of Orenia metallireducens (Strain Z6) in Surface Inert Materials. Minerals 2025, 15, 112. https://doi.org/10.3390/min15020112

AMA Style

Li S, Song W, Liu J, Boyanov MI, O’Loughlin EJ, Kemner KM, Sanford RA, Shao H, Feng Q, He Y, et al. Effect of CO2 Concentration on the Microbial Activity of Orenia metallireducens (Strain Z6) in Surface Inert Materials. Minerals. 2025; 15(2):112. https://doi.org/10.3390/min15020112

Chicago/Turabian Style

Li, Shuyi, Wentao Song, Juan Liu, Maxim I. Boyanov, Edward J. O’Loughlin, Kenneth M. Kemner, Robert A. Sanford, Hongbo Shao, Qi Feng, Yu He, and et al. 2025. "Effect of CO2 Concentration on the Microbial Activity of Orenia metallireducens (Strain Z6) in Surface Inert Materials" Minerals 15, no. 2: 112. https://doi.org/10.3390/min15020112

APA Style

Li, S., Song, W., Liu, J., Boyanov, M. I., O’Loughlin, E. J., Kemner, K. M., Sanford, R. A., Shao, H., Feng, Q., He, Y., Dong, Y., & Shi, L. (2025). Effect of CO2 Concentration on the Microbial Activity of Orenia metallireducens (Strain Z6) in Surface Inert Materials. Minerals, 15(2), 112. https://doi.org/10.3390/min15020112

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