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Author ORCID Identifier

https://orcid.org/0000-0003-4950-9636

AccessType

Open Access Dissertation

Document Type

dissertation

Degree Name

Doctor of Philosophy (PhD)

Degree Program

Microbiology

Year Degree Awarded

2021

Month Degree Awarded

February

First Advisor

James F. Holden

Second Advisor

Kristen M. DeAngelis

Third Advisor

M. Darby Dyar

Fourth Advisor

Klaus R. Nüsslein

Subject Categories

Biogeochemistry | Environmental Microbiology and Microbial Ecology | Microbial Physiology

Abstract

Dissimilatory iron reduction by hyperthermophilic archaea occurs in many geothermal environments and typically relies on microbe-mineral interactions that transform various iron oxide minerals. However, the kinds of iron oxides that can be used, growth rates, extent of iron reduction, and the mineral transformations that occur due to this metabolism are poorly understood. This dissertation improves our fundamental understanding of the physiological mechanisms and mineral transformations of hyperthermophilic iron reduction using two model crenarchaea, Pyrodictium delaneyi and Pyrobaculum islandicum. Using growth yields and metabolite production rates, we demonstrated that a broad range of Fe(III) (oxyhydr)oxides of variable thermodynamic stability was bioreduced by two hyperthermophilic archaea when presented as nanophase minerals. The degree of conversion and reduction rate varied with Fe(III) (oxyhydr)oxide and microorganism. Both organisms grew at the highest rates and produced the most Fe(II) using ferrihydrite, although P. delaneyi produced much more Fe(II) compared to P. islandicum. Lepidocrocite and akaganéite were the next two most accessible mineral species for reduction by both organisms. Highly (or more) crystalline phases such as hematite, goethite, and maghemite were poorly reduced in comparison. Transmission electron microscopy revealed an increase in crystal size for transformation products of ferrihydrite, lepidocrocite and akaganéite with P. delaneyi but not P. islandicum. Spectral analyses using visible-near-infrared, Fourier-transform infrared (FTIR) attenuated total reflectance (ATR), Raman, and Mossbauer spectroscopies revealed the formation of magnetite and/or maghemite phases with ferrihydrite, a ferrous carbonate phase reminiscent of siderite with lepidocrocite, and a ferrous phosphate similar to vivianite and magnetite with akaganéite. Lastly, physiological mechanisms of iron reduction were described for P. delaneyi using iron barrier experiments and differential proteomic analyses. P. delaneyi reduced Fe(III) oxide minerals through direct contact potentially using a novel cytochrome respiratory complex and a membrane-bound molybdopterin respiratory complex, setting iron reduction in this organism apart from previously described iron reduction processes. Collectively, findings from this dissertation help contextualize hyperthermophilic iron reduction, assess its biogeochemical impact and possibly improve its detection in environments on Earth and beyond.

DOI

https://doi.org/10.7275/20182588

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