Coupled anaerobic and aerobic microbial processes for Mn-carbonate precipitation: A realistic model of inorganic carbon pool formation
Introduction
Carbonate minerals represent the most significant form of geological carbon storage. MnII carbonate, such as rhodochrosite, is a common carbon sink product in natural systems and is found to be widely distributed in neutral to alkaline environments (Sternbeck and Sohlenius, 1997, Lebron and Suarez, 1999), in arid regions to humid soils (Kahle, 1984, Bhattacharya et al., 2009) and in oxic to anoxic sediments (Huckriede and Meischner, 1996, Lenz et al., 2014).
The deposition of MnII carbonate is generally an anaerobic process of MnIV oxide reduction that is strongly linked to organics degradation. It has been indicated by many reported examples, such as both MnII carbonates and organics being enriched in the same sedimentary environments (Huckriede and Meischner, 1996, Jakobsen and Postma, 1989); the reduction of Mn oxides being controlled by organics oxidation (Aller, 1990, Johnson et al., 2013); and the MnII carbonates having a fairly negative δ13C value in carbon isotopic characteristics (Okita et al., 1988, Matsumoto, 1992, Tsikos et al., 2003). Among those studies, the microbial MnIV reduction is known as a most important pathway causing MnII carbonates deposition.
Regarding the redox environments for MnII carbonate precipitation, although some scholars have proposed it preferentially occurring in anoxic sulfidic environments (Berner et al., 1970), the exceptional case from Huckriede and Meischner (1996) found that rhodochrosite layers could develop in a suboxic environment that is only associated with traces of sulfides. In fact, the precipitation of MnII carbonate has been found in a variety of environmental settings, including the deep sea (Pedersen and Price, 1982), near coastal (Holdren and Bricker, 1975) and freshwater sediments (Robbins and Callender, 1975), and from post-oxic to sulfidic and methanic environments (Berner, 1981). In some other cases, black shales, which are rich in both organic carbon and rhodochrosite ore, were found at the margins of black-shale basins (Bolton and Frakes, 1985, Fan et al., 1992, Okita, 1992, Roy, 1992), where the exchange and mixing of anoxic water with shallower, oxygen-bearing water are present (Force and Cannon, 1988). All of these examples suggest that MnII carbonate could precipitate in anoxic, suboxic and even oxic-anoxic boundary or transition zones.
The reduction of MnIV oxides has also been found to occur in a wide range of redox environments, including anoxic conditions (Canfield et al., 1993, Hulth et al., 1999, Konovalov et al., 2004), suboxic zones (Morrison et al., 1999, Lam et al., 2007, Karstensen et al., 2008), oxic-anoxic interfaces (Jakobsen and Postma, 1989, Yakushev et al., 2007), and even an oxic environment (Canfield et al., 1995, Cline and Richards, 1972, Devol, 1978).
A laboratory simulation of the bioreduction of MnIV oxides coupled with organic carbon oxidation was first demonstrated with Alteromonas putrefaciens MR-1 (Myers and Nealson, 1988), and then the dissimilatory MnIV reduction by obligate and facultative anaerobic organisms was extensively conducted and reported elsewhere (Lovley and Phillips, 1988, Fischer et al., 2008, Lin et al., 2012, Kim et al., 2014). However, most laboratory simulated studies have focused on the bioreduction of Mn oxides under anaerobic conditions, where dissimilatory metal-reducing bacteria (DMRB) such as Geobacter sp. (Mehta et al., 2005), Shewanella sp. (Myers and Nealson, 1990), or sulfate-reducing bacteria such as Pseudomonas spp. and Bacillus spp. (Nealson and Myers, 1992, Gounot, 1994) were widely used. The mechanisms of Mn bioreduction and MnII carbonate formation under aerobic environments are less studied and, thus, deserve exploration.
In this study, a combined process of aerobic respiration and birnessite reduction by a facultatively anaerobic bacterium Dietzia strain DQ12-45-1b (45-1b) was investigated, which may account for the deposition of Mn carbonate in O2-containing environments. Additionally, isotope tracer experiments were conducted to trace the carbon source in Mn carbonates. Furthermore, the prerequisites for birnessite bioreduction and rhodochrosite precipitation under aerobic environments are explored and discussed. Our goal is to reveal the Mn carbonate deposition mechanism at oxic-suboxic/anoxic interfaces, which may also suggest a new model of carbon conversion and storage in soil or sedimentary environments.
Section snippets
Birnessite synthesis
Birnessite used in this study was synthesized by using a chemical method proposed by McKenzie (1971). The 30 mL of concentrated HCl (analytical reagent, A.R.) was added dropwise into a boiling and stirring solution containing 0.2 mol KMnO4 (A.R.) dissolved in 350 mL of deionized water. Then, the suspension was boiled for 30 min longer for a thorough reaction. The suspension was filtered, and the precipitate was washed 15 times with deionized water to remove K+ and Cl− possibly adsorbed on
Bacterial growth coupled with chemical changes in the solution
With the inoculation of 45-1b, the living cell number of the bio + bir (aerobic) group gradually increased from (4.5 ± 0.4) × 109 to (5.7 ± 0.4) × 109 cells mL−1 during the 0–72 h incubation (Fig. 2a). After peaking at 72 h, the living cell number decreased, which indicated a decline phase of microbial growth. While in the bio + bir (anaerobic) group, it experienced an initial drop to (4.1 ± 0.1) × 109 cells mL−1 within 24 h and then increased slowly to (4.6 ± 0.1) × 109 cells mL−1 during
Bacterial growth coupled with competing aerobic and anaerobic respiration
As was observed from the growth curves, 45-1b could survive in both aerobic and anaerobic conditions, even though 45-1b grew better and consumed more acetate under aerobic conditions (Fig. 2a and b). However, the main questions lie in (1) whether aerobic and anaerobic respirations co-occurred in the bio + bir aerobic group and (2) what was the individual contribution of competing aerobic and anaerobic respiration to organics consumption.
As shown in Fig. 3a, the bioreduction of birnessite mainly
Conclusions
By comparing the changes of suspensions and minerals in aerobic and anaerobic conditions, we studied the coupled anaerobic and aerobic microbial processes in birnessite bioreduction. Based on the experiments of 45-1b interaction with birnessite in aerobic and anaerobic conditions, we found that 45-1b grew better under an aerobic environment, which was coupled with the more rapid oxidation of acetate to raise the alkalinity and consumption of oxygen to create a locally anaerobic environment.
Acknowledgments
This work was supported by the Natural Science Foundation of China [Grant Nos. 91851208, 41820104003, 41872042, 41522201 and 41230103].
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