Microbial Iron Cycling Research Articles

Intensive cryptic microbial iron cycling in the low iron water column of the meromictic Lake Cadagno.

Iron redox reactions play an important role in carbon remineralization, supporting large microbial communities in iron-rich terrestrial and aquatic sediments. Stratified water columns with comparably low iron concentrations are globally widespread, but microbial iron cycling in these systems has largely been ignored. We found evidence for unexpectedly high iron turnover rates in the low (1-2 µmol·l-1 ) iron waters of Lake Cadagno. Light-dependent, biological iron oxidation rates (1.4-13.8 µmol·l-1 ·d-1 ) were even higher than in ferruginous lakes with well-studied microbial iron cycles. This photoferrotrophic iron oxidation may account for up to 10% of total primary production in the chemocline. Iron oxides could not be detected and were presumably reduced immediately by iron-reducing microorganisms. Sequences of putative iron oxidizers and reducers were retrieved from in situ 16S rRNA gene amplicon libraries and some of these bacteria were identified in our enrichment cultures supplemented with Fe(II) and FeS. Based on our results, we propose a model in which iron is oxidized by photoferrotrophs and microaerophiles, and iron oxides are immediately reduced by heterotrophic iron reducers, resulting in a cryptic iron cycle. We hypothesize that microbial iron cycling may be more prevalent in water column redoxclines, especially those within the photic zone, than previously believed.

The Irony of Iron - Biogenic Iron Oxides as an Iron Source to the Ocean.

Primary productivity in at least a third of the sunlit open ocean is thought to be iron-limited. Primary sources of dissolved iron (dFe) to the ocean are hydrothermal venting, flux from the sediments along continental margins, and airborne dust. This article provides a general review of sources of hydrothermal and sedimentary iron to the ocean, and speculates upon the role that iron-cycling microbes play in controlling iron dynamics from these sources. Special attention is paid to iron-oxidizing bacteria (FeOB) that live by oxidizing iron and producing biogenic iron oxides as waste products. The presence and ubiquity of FeOB both at hydrothermal systems and in sediments is only beginning to be appreciated. The biogenic oxides they produce have unique properties that could contribute significantly to the dynamics of dFe in the ocean. Changes in the physical and chemical characteristics of the ocean due to climate change and ocean acidification will undoubtedly impact the microbial iron cycle. A better understanding of the contemporary role of microbes in the iron cycle will help in predicting how these changes could ultimately influence marine primary productivity.

Biogeochemical implications from dissolved rare earth element and Nd isotope distributions in the Gulf of Alaska

Dissolved rare earth element (REE) concentrations and Nd isotope compositions were measured for surface waters and full water column profiles of the Gulf of Alaska (GoA), and compared to water mass properties and circulation in order to better understand the mechanisms controlling the input and transport of REEs in the ocean. The REEs display a typical open-ocean range of concentrations (i.e., La: 12–66pM; Lu: 0.2–2.5pM) and depth distributions (i.e., surface ocean depletion and enrichment with water depth). Nd isotope signatures are highly radiogenic, as expected for the North Pacific margin (ranging from −3.8 to +0.2εNd). The most radiogenic values were found in the coastal waters but also in the cores of eddies, indicating efficient export of REEs from the margins and across the mixed layer. This is the first time that distinct Nd isotope distributions in near surface waters can be directly assigned to offshore eddy transport. A distinct mid-depth (∼2200m) Nd isotope signal was found that most likely reflects advection of a water mass that formed through past down-welling in the Northern Pacific. Subsurface Nd isotope compositions appear to behave conservatively and can be explained through a REE distribution model proposed here. This model is based on multivariate analysis of the REEs and invokes two distinct “pools” of dissolved REEs: a “passive pool” complexed by carbonate ions, and a “bio-reactive pool” that is microbially manipulated. The latter “pool” is only significant in the upper water column and most likely reflects the indirect effects of microbial cycling of iron. Our model of the open ocean REE distribution contributes to explaining the conservative nature of Nd isotopes and provides a mechanism linking surface ocean and pore water REE dynamics.

Limitations to a microbial iron cycle on Mars

Anaerobic microbial metabolisms found on the Earth are the most plausible candidates for understanding potentially analogous energy gathering metabolisms on Mars. The iron-rich nature of Mars raises questions on whether the planet could support energy acquisition by iron-cycling microorganisms. This review paper addresses what is known about the redox couples that support microbial iron cycling on Earth, and evaluates evidence to date of the presence or absence of relevant redox constituents on Mars. We give particular focus to iron reduction. These constituents include the presence and prevalence of ferric iron-bearing minerals that may serve as terminal electron acceptors, and the likelihood of organic compounds (exogenous and endogenous) or hydrogen residing in the near- or sub-surface as a source of electron donors. Whilst it is feasible that redox couples for iron cycling may exist, or have existed in the past, current knowledge suggests that for chemolithotrophs (iron oxidation) Mars may be an electron acceptor limited world and that for chemoorganotrophs (iron reduction) Mars may be limited in widespread, readily available electron donors, particularly in its subsurface. There are several major limitations in this assessment due to lack of experimental data on Earth, and lack of measurements on Mars. We outline a series of high priority in-situ measurements that are necessary to fully evaluate the potential for a Martian biological iron cycle. Our conclusions also apply to the search for a Martian biological sulphur cycle.

Abundance, Distribution, and Activity of Fe(II)-Oxidizing and Fe(III)-Reducing Microorganisms in Hypersaline Sediments of Lake Kasin, Southern Russia

The extreme osmotic conditions prevailing in hypersaline environments result in decreasing metabolic diversity with increasing salinity. Various microbial metabolisms have been shown to occur even at high salinity, including photosynthesis as well as sulfate and nitrate reduction. However, information about anaerobic microbial iron metabolism in hypersaline environments is scarce. We studied the phylogenetic diversity, distribution, and metabolic activity of iron(II)-oxidizing and iron(III)-reducing Bacteria and Archaea in pH-neutral, iron-rich salt lake sediments (Lake Kasin, southern Russia; salinity, 348.6 g liter(-1)) using a combination of culture-dependent and -independent techniques. 16S rRNA gene clone libraries for Bacteria and Archaea revealed a microbial community composition typical for hypersaline sediments. Most-probable-number counts confirmed the presence of 4.26 × 10(2) to 8.32 × 10(3) iron(II)-oxidizing Bacteria and 4.16 × 10(2) to 2.13 × 10(3) iron(III)-reducing microorganisms per gram dry sediment. Microbial iron(III) reduction was detected in the presence of 5 M NaCl, extending the natural habitat boundaries for this important microbial process. Quantitative real-time PCR showed that 16S rRNA gene copy numbers of total Bacteria, total Archaea, and species dominating the iron(III)-reducing enrichment cultures (relatives of Halobaculum gomorrense, Desulfosporosinus lacus, and members of the Bacilli) were highest in an iron oxide-rich sediment layer. Combined with the presented geochemical and mineralogical data, our findings suggest the presence of an active microbial iron cycle at salt concentrations close to the solubility limit of NaCl.

Magnetic signature of hydrocarbon-contaminated soils and sediments at the former oil field Hänigsen, Germany

Magnetic properties of hydrocarbon (HC) containing soils and sediments from two sites (Site A and B) of the former oil-field Hanigsen were analyzed in order to determine whether magnetic methods can be employed to delineate HC contamination of soils and sediments. Magnetic parameters such as magnetic susceptibility and induced isothermal remanent magnetizations, as well as soil and sediment properties such as pH, iron content and water content, HC content and most probable number counts of iron-metabolizing microorganisms were determined. The magnetic concentration-dependent parameters for HC contaminated samples were 25 times higher in soils from Site A than in sediment samples from Site B. However, at Site B the magnetic susceptibility was still four times higher in comparison to lithologically similar non-contaminated sediment samples from a third Site C. Newly formed magnetite containing mainly single domain particles was responsible for the magnetic enhancement, whereas superparamagnetic grains represented only a minor component. Site A had an acidic pH compared to neutral pH at Site B, and a higher crystalline and bioavailable total iron content. Nevertheless, Site B samples contained significant numbers of both iron(II)-oxidizing and iron(III)-reducing microorganisms indicating that microbial iron cycling might have taken place at this site and potentially played a role for iron mineral transformation, including magnetite (trans)formation. The content of total non-polar hydrocarbons (TNPH) at Site A was one order of magnitude higher than at Site B. Only at Site A magnetic susceptibility correlated well with TNPH. Our results demonstrate that HC contaminated samples had an enhanced magnetite content compared to non-contaminated soils and sediments. Therefore, magnetic methods may provide a quick and cost-effective way to assess HC contamination in soils and sediments. However, more field sites and laboratory investigations are needed to reveal the complex nature of the processes involved.

Seasonal Changes In Mineralogy, Geochemistry and Microbial Community of Bacteriogenic Iron Oxides (BIOS) Deposited in a Circumneutral Wetland

Changes in the mineralogy, microbial community structure and aquatic geochemistry of bacteriogenic iron oxides (BIOS) deposited at a circumneutral groundwater seep were recorded seasonally. X-ray diffraction and X-ray absorption spectroscopy demonstrated that 2-line ferrihydrite dominated the iron-bearing mineralogy of the BIOS (>60%). Minor proportions of the more crystalline lepidocrocite were also detected in BIOS collected throughout the year (<30%), but goethite (<15%) was only identified in sediments collected during the spring, summer and fall months. Subsurface porewater profiles generally showed an increase in dissolved equilibrium concentrations of Fe(II), indicative of microbial Fe(III) reduction, and the depth at which appreciable levels of dissolved Fe(II) (and to a lesser extent manganese) arose, and sulfate concentrations declined, become shallower as the seasons progressed from spring to fall. Clone libraries constructed from 16S rRNA gene sequence analysis of surficial BIOS showed the presence of sequences closely affiliated to known Fe(II)-oxidizing and Fe(III)-reducing prokaryotes, pointing towards a tightly coupled microbial iron cycle. Clones that showed closest identity to Fe(II)-oxidizing bacteria in culture, including Gallionella spp. and Sideroxydans spp., made up a significant portion of the clone library, but their relative proportion declined through the winter (73%), spring (26%) and summer (9%). The dominance of the putative microaerophilic Fe(II)-oxidizing chemolithoautotrophs in the winter clone library may be partly due to the lower temperature and dissolved organic carbon concentrations observed during this season, conditions that could have limited mixotrophic or organotrophic growth by mesophilic bacteria. Supplemental materials are available for this article. Go to the publisher's online edition of Geomicrobiology Journal to view the free supplemental file.

Microbial Iron Cycling in Acidic Geothermal Springs of Yellowstone National Park: Integrating Molecular Surveys, Geochemical Processes, and Isolation of Novel Fe-Active Microorganisms

Geochemical, molecular, and physiological analyses of microbial isolates were combined to study the geomicrobiology of acidic iron oxide mats in Yellowstone National Park. Nineteen sampling locations from 11 geothermal springs were studied ranging in temperature from 53 to 88°C and pH 2.4 to 3.6. All iron oxide mats exhibited high diversity of crenarchaeal sequences from the Sulfolobales, Thermoproteales, and Desulfurococcales. The predominant Sulfolobales sequences were highly similar to Metallosphaera yellowstonensis str. MK1, previously isolated from one of these sites. Other groups of archaea were consistently associated with different types of iron oxide mats, including undescribed members of the phyla Thaumarchaeota and Euryarchaeota. Bacterial sequences were dominated by relatives of Hydrogenobaculum spp. above 65–70°C, but increased in diversity below 60°C. Cultivation of relevant iron-oxidizing and iron-reducing microbial isolates included Sulfolobus str. MK3, Sulfobacillus str. MK2, Acidicaldus str. MK6, and a new candidate genus in the Sulfolobales referred to as Sulfolobales str. MK5. Strains MK3 and MK5 are capable of oxidizing ferrous iron autotrophically, while strain MK2 oxidizes iron mixotrophically. Similar rates of iron oxidation were measured for M. yellowstonensis str. MK1 and Sulfolobales str. MK5. Biomineralized phases of ferric iron varied among cultures and field sites, and included ferric oxyhydroxides, K-jarosite, goethite, hematite, and scorodite depending on geochemical conditions. Strains MK5 and MK6 are capable of reducing ferric iron under anaerobic conditions with complex carbon sources. The combination of geochemical and molecular data as well as physiological observations of isolates suggests that the community structure of acidic Fe mats is linked with Fe cycling across temperatures ranging from 53 to 88°C.

Anoxic Iron Cycling Bacteria from an Iron Sulfide- and Nitrate-Rich Freshwater Environment

In this study, both culture-dependent and culture-independent methods were used to determine whether the iron sulfide mineral- and nitrate-rich freshwater nature reserve Het Zwart Water accommodates anoxic microbial iron cycling. Molecular analyses (16S rRNA gene clone library and fluorescence in situ hybridization, FISH) showed that sulfur-oxidizing denitrifiers dominated the microbial population. In addition, bacteria resembling the iron-oxidizing, nitrate-reducing Acidovorax strain BrG1 accounted for a major part of the microbial community in the groundwater of this ecosystem. Despite the apparent abundance of strain BrG1-like bacteria, iron-oxidizing nitrate reducers could not be isolated, likely due to the strictly autotrophic cultivation conditions adopted in our study. In contrast an iron-reducing Geobacter sp. was isolated from this environment while FISH and 16S rRNA gene clone library analyses did not reveal any Geobacter sp.-related sequences in the groundwater. Our findings indicate that iron-oxidizing nitrate reducers may be of importance to the redox cycling of iron in the groundwater of our study site and illustrate the necessity of employing both culture-dependent and independent methods in studies on microbial processes.

Acid‐tolerant microaerophilic Fe(II)‐oxidizing bacteria promote Fe(III)‐accumulation in a fen

The ecological importance of Fe(II)-oxidizing bacteria (FeOB) at circumneutral pH is often masked in the presence of O(2) where rapid chemical oxidation of Fe(II) predominates. This study addresses the abundance, diversity and activity of microaerophilic FeOB in an acidic fen (pH ∼ 5) located in northern Bavaria, Germany. Mean O(2) penetration depth reached 16 cm where the highest dissolved Fe(II) concentrations (up to 140 µM) were present in soil water. Acid-tolerant FeOB cultivated in gradient tubes were most abundant (10(6) cells g(-1) peat) at the 10-20 cm depth interval. A stable enrichment culture was active at up to 29% O(2) saturation and Fe(III) accumulated 1.6 times faster than in abiotic controls. An acid-tolerant, microaerophilic isolate (strain CL21) was obtained which was closely related to the neutrophilic, lithoautotrophic FeOB Sideroxydans lithotrophicus strain LD-1. CL21 oxidized Fe(II) between pH 4 and 6.0, and produced nanoscale-goethites with a clearly lower mean coherence length (7 nm) perpendicular to the (110) plane than those formed abiotically (10 nm). Our results suggest that an acid-tolerant population of FeOB is thriving at redox interfaces formed by diffusion-limited O(2) transport in acidic peatlands. Furthermore, this well-adapted population is successfully competing with chemical oxidation and thereby playing an important role in the microbial iron cycle.

Functional diversity of bacteria in a ferruginous hydrothermal sediment

A microbial community showing diverse respiratory processes was identified within an arsenic-rich, ferruginous shallow marine hydrothermal sediment (20-40 degrees C, pH 6.0-6.3) in Santorini, Greece. Analyses showed that ferric iron reduction with depth was broadly accompanied by manganese and arsenic reduction and FeS accumulation. Clone library analyses indicated the suboxic-anoxic transition zone sediment contained abundant Fe(III)- and sulfate-reducing Deltaproteobacteria, whereas the overlying surface sediment was dominated by clones related to the Fe(II)-oxidizing zetaproteobacterium, Mariprofundus ferroxydans. Cultures obtained from the transition zone were enriched in bacteria that reduced Fe(III), nitrate, sulfate and As(V) using acetate or lactate as electron donors. In the absence of added organic carbon, bacteria were enriched that oxidized Fe(II) anaerobically or microaerobically, sulfide microaerobically and aerobically and As(III) aerobically. According to 16S rRNA gene analyses, enriched bacteria represented a phylogenetically wide distribution. Most probable number counts indicated an abundance of nitrate-, As(V)- and Fe(III)((s,aq))-reducers, and dissolved sulfide-oxidizers over sulfate-reducers, and FeS-, As(III)- and nitrate-dependent Fe(II)-oxidisers in the transition zone. It is noteworthy that the combined community and geochemical data imply near-surface microbial iron and arsenic redox cycling were dominant biogeochemical processes.

Fe(III) mineral formation and cell encrustation by the nitrate‐dependent Fe(II)‐oxidizer strain BoFeN1

ABSTRACTUnderstanding the mechanisms of anaerobic microbial iron cycling is necessary for a full appreciation of present‐day biogeochemical cycling of iron and carbon and for drawing conclusions about these cycles on the ancient Earth. Towards that end, we isolated and characterized an anaerobic nitrate‐dependent Fe(II)‐oxidizing bacterium from a freshwater sediment. The 16SrRNA gene sequence of the isolated bacterium (strain BoFeN1) places it within the β‐Proteobacteria, with Acidovorax sp. strain G8B1 as the closest known relative. During mixotrophic growth with acetate plus Fe(II) and nitrate as electron acceptor, strain BoFeN1 forms Fe(III) mineral crusts around the cells. The amount of the organic cosubstrate acetate present seems to control the rate and extent of Fe(II) oxidation and the viability of the cells. The crystallinity of the mineral products is influenced by nucleation by Fe minerals that are already present in the inoculum.

Bacterial Iron Oxidation in Circumneutral Freshwater Habitats: Findings from the Field and the Laboratory

Lithotrophic Fe-oxidation at neutral pH is becoming recognized as an important microbial process. An overview of the microbial iron cycle is presented with an emphasis on the role of microbes that grow under microaerobic conditions at oxic-anoxic transition zones where Fe(II) is abundant. Examples of these environments from freshwater are considered. Contrary Creek is a spring-fed wetland in Virginia. Measurements over the course of a year showed that it had a consistent pH around 6, and Fe(II) concentrations ranged from 25 to 300 μ M, with the highest concentrations in the summer months. At all times abundant flocs of Fe-oxides composed principally of Lepthothrix ochracea sheaths were present. Based on observations at this site, and other sites, a model for microbial Fe mat formation is presented. A thermal site in Yellowstone National Park that had consistent circumneutral pH and high Fe(II) concentrations was also studied. This site did not have evidence for Fe-oxidizing bacteria, but was, instead, dominated by a cyanobacterial photosynthetic mat. Consideration is given to growth conditions for pure cultures of Fe-oxidizing bacteria (FeOB) in the laboratory. A novel method of growing FeOB on gradient plates was developed. This led to an increase of cell yields to 2 × 108 cells/ml, which is nearly an order of magnitude greater than previous methods have yielded. Finally, speculation is made as to the potential for conditions on Mars that might have been conducive for microbial Fe-oxidation.

Microbial cycling of iron and sulfur in sediments of acidic and pH-neutral mining lakes in Lusatia (Brandenburg, Germany)

A vast number of lakes developed in the abandoned opencast lignite mines of Lusatia (East Germany) contain acidic waters (<pH 3) with high concentrations of dissolved iron and sulfate. The elimination of iron and sulfate by microbially mediated reduction processes produces alkalinity, whereas the reoxidation of reduced sulfur compounds consumes alkalinity. In order to determine the influence of environmental factors with the prospect of biological remediation strategies, these processes were investigated in sediments of two acidic and one pH-neutral mining lake. Slightly acidic sediment underlying permanently anoxic waters showed a higher accumulation rate of reduced inorganic sulfur than the pH-neutral sediment (60 v.s. 45 mmol S m−2 a−). Potential Fe(III) reduction measured by the accumulation of Fe(II) during anoxic incubation yielded similar rates in both types of sediments, however, the responses towards the supplementation of Fe(III) and organic carbon were different. Sulfate reduction rates estimated with 35S-radiotracer were much lower in the slightly acidic sediment than in the pH-neutral sediment (156 v.s. 738 mmol SO4 2− m−2 a−1). However, sulfate reduction rates were increased by the addition of organic carbon. Severe limitation of sulfate-reducing bacteria under acidic conditions was also reflected by low most probable numbers (MPN). High MPN of acidophilic iron- and sulfur-oxidizing bacteria in acidic sediments indicated a high reoxidation potential. The results show that potentials for reductive processes are present in acidic sediments and that these are determined mainly by the availability of oxidants and organic matter.

Microbial cycling of iron and sulfur in acidic coal mining lake sediments

Lakes caused by coal mining processes are characterized by low pH, low nutrient status, and high concentrations of Fe(II) and sulfate due to the oxidation of pyrite in the surrounding mine tailings. Fe(III) produced during Fe(II) oxidation precipitates to the anoxic acidic sediment, where the microbial reduction of Fe(III) is the dominant electron-accepting process for the oxidation of organic matter, apparently mediated by acidophilic Acidiphilium species. Those bacteria can reduce a great variety of Fe(III)-(hydr)oxides and reduce Fe(III) and oxygen simultaneously which might be due to the small differences in the redox potentials under low pH conditions. Due to the absence of sulfide, Fe(II) formed in the upper 6 cm of the sediment diffuses to oxic zones in the water layer where itcan be reoxidized by Acidithiobacillus species. Thus, acidic conditions are stabilized by the cycling of iron which inhibits fermentative and sulfate-reducing activities. With increasing sediment depth, the amount of reactive iron decrease, the pH increases above 5, and fermentative and as yet unknown Fe(III)-reducing bacteria are also involved in the reduction of Fe(III). Sulfate is reduced apparently by the activity of spore-forming sulfate reducers including new species of Desulfosporosinus that have their pH optimum similar to in situconditions and are not capable of growth at pH 7. However, generation of alkalinity via sulfate reduction is reduced by the anaerobic reoxidation of sulfide back to sulfate. Thus, the microbial cycling of iron at the oxic-anoxic interface and the anaerobic cycling of sulfur maintains environmental conditions appropriate for acidophilic Fe(III)-reducing and acid-tolerant sulfate-reducing microbial communities.

Phototrophs in high-iron-concentration microbial mats: physiological ecology of phototrophs in an iron-depositing hot spring.

At Chocolate Pots Hot Springs in Yellowstone National Park the source waters have a pH near neutral, contain high concentrations of reduced iron, and lack sulfide. An iron formation that is associated with cyanobacterial mats is actively deposited. The uptake of [(14)C]bicarbonate was used to assess the impact of ferrous iron on photosynthesis in this environment. Photoautotrophy in some of the mats was stimulated by ferrous iron (1.0 mM). Microelectrodes were used to determine the impact of photosynthetic activity on the oxygen content and the pH in the mat and sediment microenvironments. Photosynthesis increased the oxygen concentration to 200% of air saturation levels in the top millimeter of the mats. The oxygen concentration decreased with depth and in the dark. Light-dependent increases in pH were observed. The penetration of light in the mats and in the sediments was determined. Visible radiation was rapidly attenuated in the top 2 mm of the iron-rich mats. Near-infrared radiation penetrated deeper. Iron was totally oxidized in the top few millimeters, but reduced iron was detected at greater depths. By increasing the pH and the oxygen concentration in the surface sediments, the cyanobacteria could potentially increase the rate of iron oxidation in situ. This high-iron-content hot spring provides a suitable model for studying the interactions of microbial photosynthesis and iron deposition and the role of photosynthesis in microbial iron cycling. This model may help clarify the potential role of photosynthesis in the deposition of Precambrian banded iron formations.

The Use of Biologically Produced Ferrihydrite for the Isolation of Novel Iron-Reducing Bacteria

Ferric iron was produced anaerobically from ferrous iron through the metabolic activity of recently described ferrous iron-oxidizing, nitrate-reducing bacteria. It was identified as poorly crystallized 2-line ferrihydrite with a particle size of 1-2 nm. This biologically produced ferrihydrite was shown to be a suitable electron acceptor for dissimilatory ferric iron-reducing bacteria in freshwater enrichment cultures, and was completely reduced to the ferrous state; no magnetite formation occurred. Geobacter metallireducens was also able to completely reduce the biologically produced ferrihydrite. These results indicate the possibility of an anaerobic, microbial cycling of iron. Using the biologically produced ferric iron, two isolates of obligately anaerobic, dissimilatory ferric iron-reducing bacteria, strains Dfr1 and Dfr2, were obtained from freshwater enrichment cultures. Analysis of 16S rRNA gene sequences revealed an affiliation with the Geobacter cluster within the family Geobacteraceae. The sequence similarity between strains Dfr1 and Dfr2 is 92.5%. The closest relative of strain Dfr1 is Geobacter sulfurreducens with 92.9%, and of strain Dfr2 Geobacter chapelleii with 93.7% sequence similarity. In addition, strains Dfr1 and Dfr2 are both able to grow by dissimilatory reduction of Mn(IV), S degree, and fumarate. Furthermore, strain Dfr2 is able to reduce akaganeite (beta-FeOOH), a more crystallized type of ferric iron oxide.