Iron cycling and metal utilization by phototrophic and diazotrophic bacteria in iron-rich aquatic systems
Date
2024-12
Authors
Stevenson, Zackry
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Swanner, Elizabeth D
Beattie, Gwyn
Schmitz-Esser, Stephan
Johnson, Benjamin
Hall, Steven J
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Abstract
Background. The availability of bioessential metals influenced the evolutionary trajectory and activity of life on early Earth. Bacteria utilize trace metals such as Mo in biological nitrogen fixation, which supports the productivity of the entire biosphere. Bacteria transform Fe between different valence states with the conservation of energy, all the while transforming Fe between dissolved and mineral forms. These biological processes were carried out by the early microbial biosphere as early as the Archean Eon and are still carried out by microbes today. Although the Earth today has drastically different atmospheric and aquatic chemical conditions than the early Earth, investigating these ancient microbial processes can help decipher their role in modern phenomena such as contaminant degradation and maintaining water quality. When we can contextualize these microbial reactions in a modern system that simulates a past environment, i.e., an analog, we can also deduce how early metabolisms were regulated by and influenced the chemistry of early Earth environments.
Aims. To investigate how molybdenum and iron availability influence key microbial processes in both iron and nitrogen cycles using modern organisms and ecosystems that are analogs to early Earth. Three studies specifically (1) investigate the role that photosynthetic iron oxidation plays in the generation of reactive iron minerals that may degrade organic contaminants; (2) determine the sources of iron to a terrestrial aquatic system and how iron cycling organisms influence iron mineral formation; and (3) explore whether low Mo availability in an iron-rich Archean analog lake limits biological nitrogen fixation.
Methods. These studies used microbial and environmental sampling to document biogeochemical and biological trends. Specifically, anoxic culturing, physiological experiments, and high-performance liquid chromatography determined the metabolic capacities of Fe-cycling bacteria and metals of minerals in 2,4-D degradation. 16S rRNA amplicon sequencing assessed the abundance of microbes within mineralized creek samples, and hydrological approaches provided the context for the formation of iron mineralization. Scanning and transmission electron microscopy provided an in-depth view of the mineralogy of iron, while chemical extractions and assays quantified the forms of iron and informed its source. In iron-rich Deming Lake, environmental sensors and laboratory analysis provided context on the distribution of oxygen, nutrients, and metals within the lake. Isotope tracer studies and metagenomics/transcriptomics were used to indicate the major organisms involved in nitrogen fixation and the strategies they use to overcome low Mo availability.
Results. The increasing use of 2,4-D in agriculture raises concerns about its persistence in surface and groundwater and the environmental repercussions on ecosystems. Microbial degradation of 2,4-D is poorly understood under anoxic conditions, and we highlight this limitation as it relates to the metabolic functions of microorganisms and potential abiotic degradation in iron-rich conditions. Agricultural Fe-rich aquatic systems could play an underrecognized role in herbicide degradation and other biogeochemical element transformations due to microbial iron cycling. Clear Creek on the Iowa State University Campus has visible iron mineralization linked to episodic shallow groundwater discharge bearing Fe(II). The microbial community comprised putative iron-oxidizing and reducing organisms that likely influence the timing and type of these mineralization patterns. Fe-rich Deming Lake, MN is a chemical and biological analog for Archean oceans. Nitrogen fixation in the upper water column is dominated by Cyanobacteria despite Mo concentrations lower than predicted Archean concentrations. Despite this, nitrogen fixation is not Mo limited and alternative nitrogenases using Fe or V instead of Mo are not expressed. Mo-requiring nitrogenase likely relies on high-affinity Mo transport system and other ABC transporter cassettes necessary for transporting oxyanions, including Mo, into the cell.
Conclusions. Collectively, these findings enhance our understanding of the ecological roles of biogeochemical cycles in Fe-rich systems across Earth’s history, with implications in nutrient redox cycling and contamination mitigation. Moreover, it demonstrates the critical roles of trace metals, Fe and Mo, in shaping microbial metabolisms that have persisted through time. Further studies need to investigate the genetic basis of anaerobes in anoxic herbicide degradation, particularly when iron is present. Bacteria found in Clear Creek contribute to the formation of iron mineralization at sites of groundwater discharge, emphasizing the ecological diversity of agricultural watersheds and their potential to be hot spots for nutrient and element cycling. Deming Lake results suggest early diazotrophs could have sustained nitrogen fixation under Mo-limited conditions, shedding light on the adaptability of the nitrogenase enzyme and Mo-uptake systems in low-sulfate systems. Moreover, these results help resolve the paradox of the ancestral Mo nitrogenase utilization in the mid-Archean seen in phylogenetic studies and bulk δ15N isotope values found in Archean sediments.
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dissertation