Sean Crowe

Microorganisms regulate global nitrogen (N) availability by conducting complex series of metabolisms that transform N compounds and can produce bio-unavailable forms of N (N-loss).N-loss primarily occurs in the absence or near-absence of oxygen (O₂), and thus O₂ emerges as an important regulator of N availability. Low-O₂ pelagic marine environments are among the largest venues for N-loss and they are currently expanding as a result of ocean deoxygenation, driven byclimate change. These changes have potential to alter N availability in the ocean and create feedbacks on climate, but the outcomes are difficult to predict, partly because microbial N metabolisms are complex. Three different N metabolisms can occur under low-O₂ conditions: two metabolisms (denitrification, anammox) result in N loss, but another (DNRA) recycles N in the environment. We know relatively less about DNRA and the ways O₂ can influence N loss and recycling. In this thesis I conduct experiments in a model low-O₂ marine environment to createnew knowledge about N-recycling and the ways microbial N metabolisms respond to changing O₂. In chapter 2, I test for metabolisms that can consume N₂O across a range of O₂ conditions todetermine whether N₂O is lost through denitrification or recycled. I find that N₂O cannot be recycled, but N₂O-loss can still be active in the presence of low O₂. In chapter 3, I test theimportance of DNRA in marine waters and generate new information about microorganisms that conduct DNRA. I find that DNRA is highly variable and can be the dominant metabolism, overall.I also find that DNRA is conducted by facultatively aerobic organisms and is most active in intermittently-oxygenated environments. In the fourth chapter I test whether low O₂ can directlyregulate N loss and recycling. I find that O₂ can regulate all three metabolisms and potentially stimulate denitrification and DNRA. The observations that DNRA can be the dominant metabolism in pelagic marine environments and that O₂ can stimulate N metabolisms are two novelfindings that, if widely applicable, could alter models and forecasts for deoxygenation. I suggest future work to test extensibility and build on these results.

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Variation in the composition of chromium (Cr) stable isotopes has emerged as a powerful tracer for environmental processes as a result of the Cr isotope fractionation induced during the reduction of Cr(VI) to Cr(III). Comprehensive characterization of the geochemical processes that act on and can change Cr speciation, and of all processes that result in Cr isotope fractionation, is needed in order to make robust inferences based on the variation in Cr isotopic compositions. Our knowledge of Cr geochemistry in the natural environment is limited, with lab-based experiments often not capturing the natural complexity of the environment, in part due to Cr speciation being driven by kinetic factors, resulting in disequilibrium, as well as limited speciation data, partially due to a lack of reproducible methods. This dissertation presents a new speciation method and a wealth of new Cr speciation data resulting from the application of this method, including the first species-specific Cr isotope compositions measured in seawater across an oxic-anoxic boundary. These results provide clear evidence of positive and negative excursions in water column δ53Cr(III) in response to oxygenation and deoxygenation events, respectively, which are likely to be reflected in the authigenic Cr sedimentary record. Modeling of water column data also highlights the role of reservoir effects in muting Cr isotope fractionation relative to the intrinsic fractionation factor associated with a given process, like Cr(VI) reduction. We find non-redox processes such as water mass mixing to be a key process in Saanich Inlet, while in treated stream waters we find evidence of substantial oxidative remobilization of Cr(VI) due to reaction between reactive Cr(III) precipitates and manganese (Mn) oxides. Together, the work in this dissertation identifies the local key processes controlling Cr speciation and isotopic composition in these studied environments, with water mass mixing and in-situ Cr(III) oxidation in particular having a strong effect on the resulting Cr isotope composition, both of which are underrepresented processes in current studies. By contributing this new knowledge on Cr behaviour in the modern environment, we help to facilitate more robust inferences of Cr cycling in past environments.

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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.

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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.

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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.

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