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Microbial redox cycling of iron (Fe) plays a central role in controlling terrestrial element partitioning, with broader impacts on subsurface contaminant mobility and the development of geochemical cycles on Earth. This dissertation explores the capacity of native microbial communities to oxidize and reduce Fe in terrestrial circumneutral-pH environments by coupling environmental sampling campaigns to bench-top experiments. Microbial Fe-oxide reduction can result in magnetite production, potentially explaining magnetite in Precambrian sedimentary rocks. The only modern analog occurs in sediments at the Bay of Vidy (Lake Geneva, Switzerland), where in situ magnetite formation is directly associated with microbial reduction. Geochemistry and isotope composition of Fe in these sediments was investigated. Despite extensive microbial reduction, very little Fe isotope variation was observed, indicating Fe isotope homogeneity is not sufficient to rule out a biological mechanism for magnetite formation. Microbial oxidation of solid-phase Fe(II) at circumneutral pH is a key pathway in controlling element partitioning and contaminant stability in modern terrestrial environments. Experimental reactors were constructed with sediment from a contaminated subsurface environment (Hanford 300 Area, Richland, WA) to determine how native microbes responded to oxidant flux. Endogenous microbial communities rapidly responded to chemical oxidant input (O2 or NO3) concurrently stabilizing. Uninoculated oxic reactors showed significant Fe(II) oxidation, enhancing our understanding of the capacity for native microbes in subsurface sediment to maintain redox state. A second series of reactors explored the capacity of native microbes to oxidize solid-phase Fe minerals. The first microbial cultures capable of aerobic pyrite (FeS2) oxidation at circumneutral pH were recovered. These enrichment cultures demonstrated growth tied to pyrite oxidation and sulfate generation for over one year of repeated transfers. Aerobic pyrite oxidation has been proposed to be a dominant pathway in Precambrian sulfur cycling. The mineralogical, microbiological, and geochemical changes observed in these experiments shed light on the role of microbes in sulfur cycling in ancient and modern subsurface environments. Finally, my Teaching and Learning Portfolio, the capstone requirement for the Delta Program's Certificate in Research, Teaching, and Learning, is included to highlight some of the broader impacts of my graduate career.
In the past 15 years, there has been steady growth in work relating to the microbial iron cycle. It is now well established that in anaerobic environments coupling of organic matter utilization to Fe reduction is a major pathway for anaerobic respiration. In iron-rich circumneutral environments that exist at oxic-anoxic boundaries, significant progress has been made in demonstrating that unique groups of microbes can grow either aerobically or anaerobically using Fe as a primary energy source. Likewise, in high iron acidic environments, progress has been made in the study of communities of microbes that oxidize iron, and in understanding the details of how certain of these organisms gain energy from Fe-oxidation. On the iron scarcity side, it is now appreciated that in large areas of the open ocean Fe is a key limiting nutrient; thus, a great deal of research is going into understanding the strategies microbial cells, principally phytoplankton, use to acquire iron, and how the iron cycle may impact other nutrient cycles. Finally, due to its abundance, iron has played an important role in the evolution of Earth’s primary biogeochemical cycles through time. The aim of this Research Topic is to gather contributions from scientists working in diverse disciplines who have common interests in iron cycling at the process level, and at the organismal level, both from the perspective of Fe as an energy source, or as a limiting nutrient for primary productivity in the ocean. The range of disciplines may include: geomicrobiologists, microbial ecologists, microbial physiologists, biological oceanographers, and biogeochemists. Articles can be original research, techniques, reviews, or synthesis papers. An overarching goal is to demonstrate the environmental breadth of the iron cycle, and foster understanding between different scientific communities who may not always be aware of one another’s work.
Hydrothermal vent systems, both terrestrial and oceanic, are important environments for astrobiological research because of the hypothesized origin of life on Earth occurring at such environments. Recent and increasing evidence for relic vent deposits on Mars has further piqued the interest of astrobiologists and have become the target for future investigations for potential Martian life. While the origin of life is still highly debated, the redox gradients formed near hydrothermal vents and the energetic advantage this gives life living in such environments is undeniable. Hyperthermophilic prokaryotic organisms are phylogenetically deeply rooted, which supports the notion of originating near hydrothermal vents. Furthermore, many of these deeply rooted organisms encode Fe redox cycling based metabolic pathways suggesting dissimilatory Fe reduction (DIR) and Fe(II) oxidation are ancient microbial metabolisms. Chocolate Pots hot springs (CP) are a collection of Fe-rich circumneutral-pH hydrothermal springs located in northwestern Yellowstone National Park. For the past two decades, one of the more prominent features has been investigated with interest in how oxygenic phototrophs (e.g. cyanobacteria) may have contributed to banded iron formation deposition in the Archean. Here we expand on previous enrichment culture based investigations of the putative Fe cycling microbial community by conducting Fe(III)-reducing incubation experiments and collecting sediment and spring water samples directly from CP to gain a better understanding of the composition of the microbial community and its metabolic potential in situ. High DIR activity was observed in samples collected near the hot spring vent, and diminished further downstream. Results from 16S rRNA gene amplicon and shotgun metagenomic sequencing revealed taxa related to Thermodesulfovibrio and Ignavibacteria which encoded putative extracellular electron transfer pathways as potential indication of the in situ Fe(III)-reducing microbial community. Fe isotope fractionation that occurs as a result of DIR has been recognized as a potential biomarker of microbial activity in the rock record and in modern environments. Although natural variability obfuscated results, samples collected from the vent pool and sediment cores revealed fractionation suggestive of DIR. These studies provide constraint on the potential pathways and signatures of both extant and ancient Fe-based microbial life on Earth, Mars, and other rocky planets.
Elements move through Earth's critical zone along interconnected pathways that are strongly influenced by fluctuations in water and energy. The biogeochemical cycling of elements is inextricably linked to changes in climate and ecological disturbances, both natural and man-made. Biogeochemical Cycles: Ecological Drivers and Environmental Impact examines the influences and effects of biogeochemical elemental cycles in different ecosystems in the critical zone. Volume highlights include: Impact of global change on the biogeochemical functioning of diverse ecosystems Biological drivers of soil, rock, and mineral weathering Natural elemental sources for improving sustainability of ecosystems Links between natural ecosystems and managed agricultural systems Non-carbon elemental cycles affected by climate change Subsystems particularly vulnerable to global change The American Geophysical Union promotes discovery in Earth and space science for the benefit of humanity. Its publications disseminate scientific knowledge and provide resources for researchers, students, and professionals. Book Review: http://www.elementsmagazine.org/archives/e16_6/e16_6_dep_bookreview.pdf
Terrestrial environments contain one of the largest pools of iron (Fe) and organic carbon (OC), making the interaction between these two elements important drivers of biogeochemical cycles in soils and sediments, and critical for predicting future atmospheric carbon dioxide concentrations and climate change. This dissertation aims to understand the chemical and biological stability of Fe (hydr)oxides and OC in redox dynamic soils and sediments. A series of wet chemical techniques, advanced surface characterization methods and comparative metagenomic approaches were combined to (1) evaluate biogeochemical processes governing Fe (hydr)oxide mineralogical changes during redox oscillations, and (2) explore the biological stability of OC under Fe(III) reducing conditions. In Chapter 2, the mineralogical transformation of lepidocrocite and ferrihydrite was evaluated in the presence of freshwater sediment microorganisms under oscillating Fe(III) reducing (i.e., anaerobic glucose addition) and Fe(II) oxidizing (i.e., oxygen or nitrate addition) conditions. The results illustrate that the flux of different electron donors and acceptors can greatly impact Fe (hydr)oxide transformations and alter Fe, C, and N dynamics taking place in Fe-rich, redox active soils and sediments. Chapter 3 examined whether isolated humic substances could serve as both electron shuttles and electron donors for dissimilatory iron (hydr)oxide reduction (DIR) by freshwater sediment microorganisms. Both humic acid (HA) and humin (HM) were able to shuttle electrons and enhance DIR in cultures amended with glucose, but only HA could donate electrons for DIR by undergoing microbial degradation. Evidence for HA metabolism was observed by an overrepresentation of genes involved in polysaccharide degradation in cultures containing HA compared to those with only glucose. Chapter 4 evaluated the stability of Fe (hydr)oxide-HA coprecipitates under Fe(III) reducing conditions. HA enhanced DIR by serving as an electron shuttle and donor, but significant HA desorption was not observed. These results call into question the role of DIR in Fe (hydr)oxide-bound OC release. Overall, the transformation of Fe (hydr)oxides in redox active environments plays a central role in subsurface biogeochemical processes including nutrient availability, contaminant mobility and carbon dynamics.
The most definitive manual of microbes in air, water, and soil and their impact on human health and welfare. • Incorporates a summary of the latest methodology used to study the activity and fate of microorganisms in various environments. • Synthesizes the latest information on the assessment of microbial presence and microbial activity in natural and artificial environments. • Features a section on biotransformation and biodegradation. • Serves as an indispensable reference for environmental microbiologists, microbial ecologists, and environmental engineers, as well as those interested in human diseases, water and wastewater treatment, and biotechnology.
The reactivity of iron(III)-(oxyhydr)oxides toward microbial iron(III)-reduction is dependent on mineral reactive surface area and solubility, properties that can be altered by redox cycling. Because carbon (C) stability and nutrient availability can be influenced by redox dynamics, there is a need to evaluate the mechanisms that govern iron(III)-(oxyhydr)oxide transformations and strategies of microbial iron(III)-reducers to access these phases under fluctuating redox conditions in soils. To do this, we characterized the native iron phases in soils from the Bisley Watershed, Luquillo Critical Zone Observatory (LCZO), PR using selective chemical extractions, X-ray diffraction and 57Fe-Mössbauer spectroscopy. We then conducted laboratory experiments where we exposed the soils to redox cycles with variable iron(II)-oxidation rates and measured changes in the solution and solid phase iron speciation as well as sequenced mRNA extracted from native iron(III)-reducing bacteria. The native iron composition in the LCZO soil comprised goethite and lepidocrocite, with higher solid phase iron(II) correlated with higher lepidocrocite abundance and citrate-ascorbate extractable (low crystallinity) iron. 57Iron-Mössbauer spectra at 140 Kelvin (K) show that iron-(oxyhydr)oxides underwent either an increase or a decrease in crystal order due to rate of iron(II)-oxidation over multiple redox cycles in laboratory incubations. Soil RNA isolated following multiple redox cycles was subsequently depleted of rRNA and enriched for mRNA by linear amplification. De novo assembly of millions of paired-end Illumina reads was used to further examine the importance of several putative c-type cytochrome, pilin, exopolysaccharide, chemotaxis, TCA cycle and carbon degradation transcripts that were collectively binned to iron(III)-reducer genomes of Anaeromyxobacter, Geobacter and Desulfovibrio. We also enriched 57iron in soil incubations to track iron(III)-(oxyhydr)oxide formation. We found that rapid oxidation of enriched iron(II) generates short-range-ordered (i.e. low crystallinity) iron phases that are more readily solubilized by iron(III)-reducing microorganisms than the bulk native soil iron phases at the onset of iron(III)-reduction. Some 57iron-enriched solid iron(III) that is not reduced becomes incorporated into longer-range-order phases (i.e. higher crystallinity) during iron(III)-reduction. A portion of iron(II) formed in the solid phase during iron(III)-reduction displays weak magnetic order in the Mössbauer spectra collected at 4.5 K, perhaps arising from the formation of nano-magnetite or, more generally, iron(II) adsorbed/incorporated at the surface of short-range-ordered iron(III)-(oxyhydr)oxides. These processes regarding mineral-microbial interactions are expected to be linked to ecosystem-level nutrient cycling, carbon stability and global greenhouse gas emissions in highly-active, humid, tropical forest soils.
Cover Image credit: Topic Editor Dr. Andrea Teixeira Ustra