Doctor of Philosophy in Microbiology and Immunology (PhD)
Oxygen loss in our oceans and the environmental impacts of marine microorganisms
Banded iron formations (BIFs), which host the world’s largest iron ore deposits, formed predominantly through the deposition of ferric iron (Fe[III]) from ferruginous oceans during the Archean Eon. Available evidence suggests that phototrophic iron oxidation (photoferrotrophy) may have played a key role in coupling the carbon and iron cycles during the Archean Eon, depositing BIFs, and, in doing so, underpinned global primary production at this time. To date, however, all known photoferrotrophs form a close association with the ferric iron metabolites they produce during growth. This intimate association calls into question the involvement of photoferrotrophs in BIF deposition, their ability to act as primary producers, and their role in sustaining the biosphere for millions of years. Furthermore, a lack of quantitative knowledge on the growth of photoferrotrophs and the interactions between them and other microorganisms limit our ability to constrain models of BIF deposition and the Archean ocean-atmosphere system as a whole. This dissertation generates new knowledge on extant photoferrotrophy that can be used to inform and constrain models of primary production and BIF deposition during the Archean Eon. I create new knowledge on photoferrotrophy under laboratory conditions and in natural environments through data collected on the physiology and metabolic capacity of pelagic photoferrotroph Chlorobium phaeoferrooxidans strain KB01. I also measure process rates and analyze the composition of the microbial community in a ferruginous lake--Kabuno Bay--that is dominated by photoferrotrophy. I subsequently integrate this new knowledge into models that examine the antiquity of nutrient acquisition in the photoferrotrophic Chlorobia and the role of photoferrotrophs as primary producers during the Archean. These models provide an explanation for the formation of BIFs as a by-product of the activity of photoferrotrophic bacteria. Additionally, I demonstrate how photoferrotrophs could have sustained the biosphere, likely fueled microbial methanogenesis, and, therefore, helped to stabilize Earth’s climate under a dim early Sun.
The oxygen concentration of the ocean atmosphere system regulates the nature, activity and diversity of life on Earth. Atmospheric and ocean oxygenation is tightly coupled to the global biogeochemical cycles of C, N, P, S and Fe, as well as climate. Reconstructing the history of oxygen on planet Earth, therefore, is a key component to understanding the evolution of life. Our emergent picture of the evolution of Earth’s surface redox state with its links to the evolution of life and climate relies heavily on interpretations of geochemical information preserved in the rock record. The Cr isotope and Fe-speciation proxies are two widely applied tools used to diagnose redox conditions in both modern and ancient depositional environments. Many aspects of the precise mechanisms that lend the use of these two transition metals as paleoredox proxies, however, remain unclear, confounding accurate reconstructions of paleo-oxygen concentrations that rely on Cr isotope and Fe-speciation data. In this work I studied Cr isotope and Fe speciation proxy systematics to develop more nuanced frameworks for how these two paleoredox proxies may be employed to reconstruct depositional redox states in both modern and past environments. I determined the Cr isotope and Fe mineral composition of modern marine hydrothermal sediments, revealing Cr isotope fractionations that imply deposition from an oxygenated deep ocean. I determined Cr isotope fractionations associated with the reduction of Cr(VI) in modern ferruginous sediments, revealing that the magnitude of Cr isotope fractionation in such environments is linked to the speciation of Fe and the oxygen penetration depth of the sediments. I determined Fe-speciation and trace metal abundances of sediments deposited during oceanic anoxic event 1a (OAE1a), revealing that during this interval the oceans were anoxic and Fe-rich (ferruginous) for more than 1 million years. Lastly, I determined the Fe-speciation of suspended and sedimented material from two modern ferruginous lakes, revealing that the mineral magnetite forms authigenically in the ferruginous water columns. This new knowledge of Cr and Fe proxy systematics will allow for more refined interpretations of paleo oxygen concentrations based on Cr isotope and Fe-speciation signals captured in the rock record through time.
Cycling of N occurs through a multitude of microbial reactions used by microorganisms to harnessenergy and generate growth. These microbial reactions are the main controls on the availabilityof fixed-N and can often limit primary production in marine ecosystems. The microorganismsinvolved in the N-cycle are diverse and the metabolic pathways are further distributed acrossmany taxa, rendering the modeling of the N-cycle complex. Indeed, models of N-cycling fall shortof making robust and explicit predictions, in part due to a lack of ecophysiological informationdescribing the relevant processes at a molecular scale. Direct ecophysiological information isobtained from process rate measurements, yet these generally lack coupled information onmicrobial community composition limiting their extensibility across multiple environments. Thisdissertation creates a new framework for the modeling of the N-cycle by measuring the rates andpathways of N-cycling in anoxic pelagic environments. This new and quantitative knowledgeis incorporated into models of N-cycling to improve reconstructions of past and future N-cycle.I describe the rates and pathways of Fe-dependent NO¯₃ reduction in a ferruginous pelagicenvironment, analogous to the Proterozoic oceans. I then describe the nutrients status andthe implications of NO¯₃ reduction through DNRA and denitrification for biological productionthrough a flux-balance model for ancient oceans. I also study the environmental factors thatinfluence the partitioning of N-loss between anammox and denitrification in an anoxic fjord(Saanich Inlet). A flux-balance model was built to describe the competition between anammoxand denitrification based on the rates of N₂ production as well as changes in microbial communitycomposition and ecophysiological parameters. We show that recycling of N through DNRA, ratherthan N-loss, dominates annual NO¯₃ reduction in Saanich Inlet, challenging current assumptionsthat DNRA does not need to be considered as an important pathway of N-cycling in the ocean.Overall, the work presented here offers a new and integrated approach that combines geochemicalinformation such as nutrient profiles and process rate measurements, microbiological informationsuch as microbial community composition, structure and functions analysis, and applies it toquantitative models that can be used to further test hypotheses about the N-cycle.
Fracing technology has revolutionized the natural gas industry, and currently, it is the most widely used method to extract gas from shale in Western Canada. Microbial activity in fracing fluids can lead to biofouling, corrosion, and gas souring. Biocides are commonly applied to inhibit microbial activity, but in many cases biocide application is partly or even wholly ineffective. This is, in part, because biocides are rarely tested using real environmental communities relevant to fracing systems. To address this problem, I investigated the efficacy of glutaraldehyde, which is one of most commonly used biocides to control microbial activity, on microbial sulfur reduction in fracing fluids. To do this, I collected fracing fluids from the shale gas play in the Fort St. John area of northern British Columbia, Canada. In the lab, I conducted incubation experiments by amending fracing fluids with glutaraldehyde and yeast extract and incubating these fluids for 30 days at room temperature. During the incubation, I measured sulfide and sulfate concentrations to track rates of microbial sulfur metabolisms with and without glutaraldehyde and yeast extract amendments. To link these results to the relevant microbial taxa, I determined the microbial community present in the incubated fluids using 16S rRNA gene amplicon sequencing. Overall, I found that glutaraldehyde is only moderately effective in controlling microbial sulfide production in fracing fluids and that even in the presence of glutaraldehyde, amendment with reactive organic matter stimulates sulfide production.