Microbe-clay mineral interactions Dong Hailiang, Dong Hailiang; Jaisi, Deb P; Kim, Jinwook ...
The American mineralogist,
11/2009, Volume:
94, Issue:
11-12
Journal Article
Peer reviewed
Clays and clay minerals are common components in soils, sediments, and sedimentary rocks, and they play an important role in many environmental processes. Iron is ubiquitous in clays and clay ...minerals and its oxidation state, in part, controls the physical and chemical properties of these fine-grained minerals. The structural ferric iron in clay minerals can be reduced either chemically or biologically. Biological reductants include mesophilic and thermophilic microorganisms from diverse environments such as soils, sediments, sedimentary rocks, and hydrothermal hot springs. Multiple clay minerals have been used for microbial reduction studies, including dioctahedral smectite-illite series, palygorskite, chlorite, and their various mixtures in natural soils and sediments. All of these clay minerals are reducible by microorganisms under various conditions with smectite (nontronite) being the most reducible and illite the least. The rate and extent of bioreduction depends on many experimental factors, such as the type of microorganisms and clay minerals, solution chemistry, and temperature. Despite significant efforts, current understanding of the mechanisms of microbial reduction of ferric iron in clay minerals is still limited. Whereas some studies have presented evidence for a solid-state reduction mechanism, others argue that the clay mineral structure partially dissolves when the extent of reduction is high. This inconsistency may be related to several experimental conditions, and their specific effects are discussed in this paper. Whereas past experiments have been largely conducted in well-controlled laboratory systems, recent efforts have attempted to transfer knowledge to the field to improve our understanding of more complex soil systems for better agricultural practices. Biologically reduced clay minerals are also important agents in remediating inorganic and organic contaminants in soil and groundwater systems. This paper reviews the most recent developments and suggests some directions for future research.
Organic matter and reduced sulfur compounds commonly coexist in groundwater aquifers and their respective roles in Cr(VI) bio-reduction have been well established, but Cr(VI) bio-reduction under ...mixotrophic condition, where organics and elemental sulfur simultaneously occur as co-donors of electrons, remains largely unknown. Herein a sulfur-based mixotrophic bio-reduction process is demonstrated to be effective to detoxify Cr(VI), with a removal efficiency of 95.5 ± 0.74% within 48 h at an initial concentration of 50 mg/L. In addition to direct reduction by heterotrophic Cr(VI) reducers such as Desulfovibrio and Desulfuromonas, volatile fatty acids (VFAs) produced from autotrophic sulfur oxidation served as electron donors for heterotrophic Cr(VI) reducers. Part of VFAs was also assimilated and accumulated as glycogen within cells, which enhanced their Cr(VI) removal capacity. Metabolic pathway analysis suggested that Cr(VI) was reduced to insoluble Cr(III) both extracellularly by cytochrome c and intracellularly by nicotinamide adenine dinucleotide in the presence of upregulated chrA gene. Constituents of extracellular polymeric substances (EPS) also contributed to Cr(VI) reduction enzymatically, through binding of toxic Cr(VI) by carboxyl and hydroxyl groups. Results from this study have important implications for understanding the biogeochemical behavior and environmental remediation of Cr(VI) in groundwater aquifers and sediments/soils.
It is generally believed that clay minerals can protect organic matter from degradation in redox active environments, but both biotic and abiotic factors can influence the redox process and thus ...potentially change the clay-organic association. However, the specific mechanisms involved in this process remain poorly understood. In this study, model organic compound 12-Aminolauric acid (ALA) was selected to intercalate into the structural interlayer of nontronite (an iron-rich smectite, NAu-2) to form an ALA-intercalated NAu-2 composite (ALA-NAu-2). Shawanella putrefaciens CN32 and sodium dithionite were used to reduce structural Fe(III) to Fe(II) in NAu-2 and ALA-NAu-2. The bioreduced ALA-NAu-2 was subsequently re-oxidized by air. The rates and extents of bioreduction and air re-oxidation were determined with wet chemistry methods. ALA release from ALA-NAu-2 via the redox process was monitored. Mineralogical changes after iron redox cycle were investigated with X-ray diffraction, infrared spectroscopy, and scanning and transmission electron microscopy. At the beginning stage of bioreduction, S. putrefaciens CN32 reductively dissolved small and poorly crystalline particles and released intercalated ALA, resulting a positive correlation between ALA release and iron reduction extent (<12%). The subsequent bioreduction (reduction extent from 12-30%) and complete air re-oxidation showed no effect on ALA release. These results suggest that released ALA was largely from small and poorly crystalline NAu-2 particles. In contrast to bioreduction, chemical reduction did not exhibit any selectivity in reducing ALA-NAu-2 particles, and a considerable amount of reductive dissolution was responsible for a large amount of ALA release (>80%). Because bacteria are the principal agent for mediating redox process in natural environments, our results demonstrated that the structural interlayer of smectite can serve as a potential shelter to protect organic matter from oxidation.
Oxygenation of reduced iron-bearing clay minerals produces highly reactive oxidants that are capable of transforming a range of organic compounds, which is of great environmental importance, but the ...effect of Fe-chelating ligands on this process has not been studied. In this work, oxidant production from oxygenation of reduced nontronite was investigated in the presence of four common ligands. Addition of phosphate, tripolyphosphate (TPP), nitrilotriacetic acid (NTA) and ethylene diaminetetraacetic acid (EDTA) all significantly increased the oxidant yields, but the specific mechanisms varied, depending on the ligand types. NTA and EDTA addition promoted dissolution of structural Fe, forming aqueous NTA-Fe2+ and EDTA-Fe2+ complexes. Upon exposure to air, these complexed species rapidly oxidized through homogeneous Fenton reaction, forming chelated soluble Fe3+ species, which were rapidly reduced back to Fe2+ by electrons transferred from structural Fe(II) in reduced nontronite. With increasing NTA and EDTA loadings, homogeneous Fenton reaction gradually dominated over heterogeneous oxidation of structural Fe(II). Because of rapid air oxidation of NTA-Fe2+ and EDTA-Fe2+ complexes, these species were maintained at low levels in aqueous solution, thus minimizing the quenching effect of oxidants by excess Fe2+and the probability of non-oxidant generation pathway, both of which contributed to the observed increase of the oxidant yields. In contrast, phosphate increased the oxidant yield through sorption to the surface of reduced NAu-2 and a subsequent shift of weak oxidant possibly Fe(IV) to strongly reactive hydroxyl radicals (HO). TPP played a dual role by both changing the surface catalytic properties of nontronite through sorption and enhancing homogeneous Fenton reaction by chelating with aqueous Fe2+ and Fe3+. These results shed lights on how commonly present natural and synthetic ligands affect the oxidation process of reduced iron-bearing clay minerals and oxidant production, hence providing a theoretical basis for understanding oxidant-promoted transformation mechanisms of organic matter in either natural or engineered systems.
Microbial vanadate V(V) reduction is the key process of vanadium geochemical cycling, while the identified functional microbes are rather limited. Considering the structural similarity of ...metavanadate and nitrate, widespread denitrifying bacteria are expected to be able to mediate V(V) reduction, but this process has not been fully understood. This study confirmed the effectiveness of two denitrifying bacteria, i.e., Acidovorax sp. strain BoFeN1 and Pseudogulbenkiania sp. strain 2002, in reducing V(V). During 120-h incubation, the V(V) removal efficiency was 89.0 ± 1.83% and 96.0 ± 1.43% by strain BoFeN1 and strain 2002, respectively. V(V) was reduced to tetravalent vanadium V(IV) both intracellularly and extracellularly. Use of inhibitors and metabolomic analysis revealed enzyme catalysis and electron transfer pathways for V(V) reduction. Enzyme catalysis was identified by analyses of gene abundance, transcript abundance, and enzymatic activity. Electron transfer was verified through quantifying electron transporters, monitoring electron transport system activity, and performing cyclic voltammetry analysis. For strain BoFeN1, nitrite and nitrous oxide reductases played vital roles in V(V) reduction, together with cytochrome c (Cyt c) and nicotinamide adenine dinucleotide (NADH) mediated electron transfer. Differentially expressed riboflavin produced by strain BoFeN1 also promoted electron transfer. Strain 2002 mainly utilized periplasmic nitrate reductase to reduce V(V). Aquifer sediment bioaugmented with these strains enhanced V(V) reduction by 10.5%−51.1%. They well colonized and collaborated with indigenous microorganisms to reduce V(V) to V(IV). This study advances understanding of environmental biogeochemistry of vanadium and provides molecular insights into V(V) bio-reduction as a sustainable bioremediation strategy.
Electrons can be transferred from microorganisms to multivalent metal ions that are associated with minerals and vice versa. As the microbial cell envelope is neither physically permeable to minerals ...nor electrically conductive, microorganisms have evolved strategies to exchange electrons with extracellular minerals. In this Review, we discuss the molecular mechanisms that underlie the ability of microorganisms to exchange electrons, such as c-type cytochromes and microbial nanowires, with extracellular minerals and with microorganisms of the same or different species. Microorganisms that have extracellular electron transfer capability can be used for biotechnological applications, including bioremediation, biomining and the production of biofuels and nanomaterials.
Although biodiversity and ecosystem functions are strongly shaped by contemporary environments, such as climate and local biotic and abiotic attributes, relatively little is known about how they ...depend on long-term geological processes. Here, along a 3000-m elevational gradient with tectonic faults on the Tibetan Plateau (that is, Galongla Mountain in Medog County, China), we study the joint effects of geological and contemporary environments on biological communities, such as the diversity and community composition of plants and soil bacteria, and ecosystem functions. We find that these biological communities and ecosystem functions generally show consistent elevational breakpoints at 2000-2800 m, which coincide with Indus-Yalu suture zone fault and are similar to the elevational breakpoints of soil bacteria on another mountain range 1000 km away. Mean annual temperature, soil pH and moisture are the primary contemporary determinants of biodiversity and ecosystem functions, which support previous findings. However, compared with the models excluding geological processes, inclusion of geological effects, such as parent rock and weathering, increases 67.9 and 35.9% of the explained variations in plant and bacterial communities, respectively. Such inclusion increases 27.6% of the explained variations in ecosystem functions. The geological processes thus provide additional links to ecosystem properties, which are prominent but show divergent effects on biodiversity and ecosystem functions: parent rock and weathering exert considerable direct effects on biodiversity, whereas indirectly influence ecosystem functions via interactions with biodiversity and contemporary environments. Thus, the integration of geological processes with environmental gradients could enhance our understanding of biodiversity and, ultimately, ecosystem functioning across different climatic zones.
Investigating microbial response to environmental variables is of great importance for understanding of microbial acclimatization and evolution in natural environments. However, little is known about ...how microbial communities responded to environmental factors (e.g. salinity, geographic distance) in lake surface sediments of the Qinghai-Tibetan Plateau (QTP). In this study, microbial diversity and community structure in the surface sediments of nine lakes on the QTP were investigated by using the Illumina Miseq sequencing technique and the resulting microbial data were statistically analyzed in combination with environmental variables. The results showed total microbial community of the studied lakes was significantly correlated (r = 0.631, P < 0.001) with lake salinity instead of geographic distance. This suggests that lake salinity is more important than geographic distance in shaping the microbial diversity and community structure in the studied samples. In addition, the abundant and rare taxa (OTUs with relative abundance higher than 1% and lower than 0.01% within one sample, respectively) were significantly (P < 0.05) correlated (r = 0.427 and 0.783, respectively) with salinity, suggesting rare taxa might be more sensitive to salinity than their abundant counterparts, thus cautions should be taken in future when evaluating microbial response (abundant vs. rare sub-communities) to environmental conditions.
Biochar naturally occurs in soils and sediments as a result of wildfire, but its role in Fe redox cycling is poorly known. In this study, bioreduction experiments were conducted with lactate as the ...electron donor, Fe(III) in nontronite (NAu-2) or ferric citrate as the electron acceptor, and Shewanella putrefaciens CN32 as the Fe(III)-reducing bacterium in the absence and presence of biochar. High biochar concentrations increased but low concentrations decreased the reduction rate and extent. When NAu-2 was replaced with ferric citrate aqueous Fe(III)-citrate complex, while the rate was enhanced, the extent of bioreduction remained unchanged at low biochar concentration but declined at high biochar concentration. These different redox behaviors of biochar can be explained by the interplay among four factors: (1) the electron shuttling role of biochar; (2) the electron buffering capacity of biochar; (3) the effect of biochar surface on cell distribution; (4) the effect of biochar on cell attachment and growth. In the absence of biochar, the electron transfer pathway is from cells directly to Fe(III) (Pathway 1). However, in the presence of biochar, there is a second pathway (Pathway 2), i.e., from attached cells to biochar and from biochar to Fe(III). At low biochar concentrations, the presence of biochar decreases the efficiency of Pathway 1 because some cells are diverted to biochar surface, but this deficiency is not made up by Pathway 2 because of physical separation between negatively-charged biochar and NAu-2 particles. Therefore, even though biochar particles receive electrons from attached cells, they are not able to transfer them to NAu-2, thus retaining a proportion of electrons. Possible cell clumping on biochar surface may decrease effective cell concentration and thus pose additional inhibition of NAu-2 bioreduction. However, in the treatment of soluble Fe(III)-citrate complex, Pathway 2 is still effective, because there is no physical barrier between biochar and soluble Fe(III). The electron shuttling role of biochar actually increases the rate of Fe(III) bioreduction.
As biochar concentration increases, large surface area of biochar spreads out cells and increases the probability of encounter between cells and NAu-2 particles. In this case, both pathways are effective. Increasing biochar concentrations result in fewer electron retention per gram of biochar. Possible cell growth on biochar surface would further enhance Pathway 2. Therefore, the overall result is the enhanced rate and extent of Fe(III) bioreduction in NAu-2. However, for soluble Fe(III)-citrate complex, both pathways may be impaired because high concentration of biochar would accumulate toxic substances and decrease concentration of cells, which would inhibit Fe(III) bioreduction. As biochar accumulates in soils, the role of biochar is expected to greatly impact Fe redox reactions and other environmental processes.
Hexavalent chromium Cr(VI) is one of the common heavy-metal contaminants in groundwater, and the availability of electron donors is considered to be a key parameter for Cr(VI) biotransformation. ...During the autotrophic remediation process, however, much remains to be illuminated about how complex syntrophic microbial communities couple Cr(VI) reduction with other elemental cycles. Two series of Cr(VI)-reducing groundwater bioreactors were independently amended by elemental sulfur and iron and inoculated with the same inoculum. After 160 days of incubation, both bioreactors showed similar archaea-dominating microbiota compositions, whereas a higher Cr(VI)-reducing rate and more methane production were detected in the Fe0-driven one. Metabolic reconstruction of 23 retrieved genomes revealed complex symbiotic relationships driving distinct elemental cycles coupled with Cr(VI) reduction in bioreactors. In both bioreactors, these Cr(VI) reducers were assumed to live in syntrophy with oxidizers of sulfur, iron, hydrogen, and volatile fatty acids and methane produced by carbon fixers and multitrophic methanogens, respectively. The significant difference in methane production was mainly due to the fact that the yielded sulfate greatly retarded acetoclastic methanogenesis in the S-bioreactor. These findings provide insights into mutualistic symbioses of carbon, sulfur, iron, and chromium metabolisms in groundwater systems and have implications for bioremediation of Cr(VI)-contaminated groundwater.
PDF
