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Electron Acceptors in the Arctic: The Roles of Iron, Humic Acids, and Organic Chlorine in Anaerobic Respiration

  • Author(s): Zlamal, Jaime Enid
  • Advisor(s): Lipson, David A
  • et al.
Abstract

Bacteria and archaea have evolved the ability to respire using diverse compounds to produce energy. The use of alternative electron acceptors for anaerobic respiration is critical in environments where oxygen is limited or absent – such as soils of the Arctic Coastal Plain. Continuous permafrost below the active layer of soil restricts drainage, creating anoxic conditions. Thus, anaerobic respiration dominates all but the top few centimeters of soil.

Climate change effects acutely impact the Arctic, and the potential for positive feedback from soil respiration is substantial. Biogeochemical cycling in this environment warrants further study, particularly concerning anaerobic electron acceptors which contribute to CO2 fluxes and can compete with methanogenesis, further impacting greenhouse gas emissions.

The objective of this dissertation is to explore metabolism of unusual electron acceptors in Arctic tundra soils, focusing on the importance of humic substances, their interactions with iron, and the role of organohalide respiration in the Arctic carbon cycle. The research contained within unites microbiological techniques, soil chemistry methods, and innovative interdisciplinary tools to study these compounds from a variety of vantage points.

Soil extract measurements, potentiometric redox titrations, and cyclic voltammetry revealed that metabolism involving humic acids in this environment may contribute nearly 400 moles of electrons per square meter of soil (e-/m2), accounting for over 10% of ecosystem respiration. Performing a field-based soil amendment experiment and laboratory incubations validated that reduction of large, insoluble humic acids can be facilitated by way of soluble iron intermediates, iron is an electron-accepting moiety in humic acids, and iron-reducing bacteria liberate complexed iron from the structure of humic acids. Chlorinated organic compound cycling in tundra soils was studied with field measurements, biological exploration using laboratory incubations and metagenomics, and chemical investigation using elegant tools including Oxidative Combustion Microcoulometry and X-ray absorption near edge structure (XANES). These corroborating methods demonstrated chlorinated organic compounds are widespread, dynamic, and used for anaerobic respiration by diverse microorganisms in essentially pristine Arctic soils. The work contained within this dissertation provides fresh insight into vital yet understudied Arctic soil microbial anaerobic processes which have broader impacts on Arctic carbon cycling and climate change feedback mechanisms.

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