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From Photosynthesis to Detoxification: Microbial Metabolisms Shape Earth’s Surface Chemistry


Wang, Renée Zurui (2024) From Photosynthesis to Detoxification: Microbial Metabolisms Shape Earth’s Surface Chemistry. Dissertation (Ph.D.), California Institute of Technology. doi:10.7907/kf85-cq89.


Earth’s chemistry, through geologic time and in the present, is inextricably linked with biologically mediated reactions. All major elemental cycles on Earth’s surface have arisen from two competing processes – life shaping its chemical environment through the evolution of key biochemical pathways, and the environment constraining metabolism by dictating which reactions will occur. Understanding this complicated interplay motivates the research presented in this thesis, which studies this phenomenon over two major elemental cycles – the modern Nitrogen (N) and ancient Carbon (C) cycle.

Chapters One and Two focus on the evolution of ribulose-1,5-bisphosphate carboxylase/oxygenase (rubisco), the enzyme that catalyzes the key carbon fixation step in modern oxygenic photosynthesis. This reaction also imparts a large kinetic isotope effect (KIE) that causes the fixed carbon to be relatively depleted in natural abundance ¹³C compared to its substrate; this isotopic fingerprint can be seen in both the modern C cycle and in rock records recording the ancient C cycle. Therefore, this KIE has been used both in vitro (outside the cell) by biochemical models to rationalize rubisco’s reaction mechanism, and in vivo (in the cell) as a proxy for environmental CO₂ concentrations in the past and present. However, both the in vitro and in vivo measurements are calibrated using modern organisms even though rubisco and oxygenic photosynthesis have undergone profound evolution over geologic time. Therefore, we measured the KIE in vitro and in vivo of a reconstructed ancestral Form IB rubisco dating to >> 1 Ga, and the KIE in vitro of a recently discovered Form I’ rubisco that presents a modern analogue to ancestral Form I rubiscos prior to the evolution of the small subunit. Overall, we find that the KIEs of both rubiscos are smaller than their modern counterparts, which is surprising given that the rock record indicates overall carbon isotope fractionations in vivo are larger in the past. In addition, we find that models strictly based on modern organisms may not apply to the past, questioning the basic assumption that uniformitarianism can be readily applied to biological processes. However, these models can be rescued by accounting for other aspects of cell physiology.

Chapter Three focuses on disentangling the source of key metabolites, like nitrous oxide (N₂O) in the modern N cycle. Like Chapters 1 and 2, an isotopic fingerprint that measures the ‘preference’ of ¹⁵N for the central or outer nitrogen site in N₂O (“Site Preference” or “SP”) has primarily been calibrated using dissimilatory, or energy-generating, nitric oxide (NO) reductases (NORs). However, there exists a much larger and phylogenetically widespread class of NO-detoxifying enzymes; in particular, flavohemoglobin proteins (Fhp/Hmp) produce N₂O as a strategy to neutralize damaging NO-radicals in anoxic conditions. This enzyme, which generates N₂O in non-growing and anoxic conditions, may be more relevant to natural environments where N₂O production has been detected. Surprisingly, we found that Fhp imparts a distinct SP on N₂O that differs from both bacterial and eukaryotic NORs, and that this value better aligns with existing in situ measurements of N₂O from soils. In addition, we find that in strains with both Fhp and NOR, the Fhp signal dominates when cells are first exposed to high concentrations of NO in oxic conditions while growing before being shifted to an anoxic, non-growing state. Therefore, in addition to telling us ‘Who’s there,’ the SP fingerprint may also be able to tell us something about cell physiology in vivo. We propose a new framework for interpreting the source of N₂O based on SP values.

Item Type:Thesis (Dissertation (Ph.D.))
Subject Keywords:Microbial Metabolism; Isotope; Site Preference; Rubisco; Carbon Isotope Fractionation; Nitrogen Isotope; Enzyme
Degree Grantor:California Institute of Technology
Division:Geological and Planetary Sciences
Major Option:Geochemistry
Awards:Dr. James King Jr. Student Diversity Award, 2021.
Thesis Availability:Public (worldwide access)
Research Advisor(s):
  • Newman, Dianne K. (co-advisor)
  • Eiler, John M. (co-advisor)
Thesis Committee:
  • Sessions, Alex L. (chair)
  • Fischer, Woodward W.
  • Mazmanian, Sarkis K.
  • Newman, Dianne K.
  • Eiler, John M.
Defense Date:29 September 2023
Funding AgencyGrant Number
David and Lucille Packard Foundation12540178
Simons Foundation554187
NASA Exobiology00010652
Schwartz-Reisman Collaborative Science Program12520057
NSF Graduate Research FellowshipUNSPECIFIED
Department of Energy (DOE)DE-SC00016240
Science-Brano Weiss FellowshipUNSPECIFIED
Caltech Center for Evolutionary SciencesUNSPECIFIED
NASA Exobiology80NSSC21K0484
Record Number:CaltechTHESIS:10102023-024622119
Persistent URL:
Related URLs:
URLURL TypeDescription adapted for Ch. 2 adapted for Ch. 3
Wang, Renée Zurui0000-0003-3994-3244
Default Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:16204
Deposited By: Renee Wang
Deposited On:12 Oct 2023 21:18
Last Modified:17 Jun 2024 19:35

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