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Precursors to Modern Aerobic Ammonium Oxidation: Oxygenic and Electrogenic Anaerobic Pathways

Periodic Reporting for period 1 - PAERADOX (Precursors to Modern Aerobic Ammonium Oxidation: Oxygenic and Electrogenic Anaerobic Pathways)

Reporting period: 2018-08-01 to 2020-07-31

Earth had gone into dramatic changes since the start of life, and it greatly affected the evolution of life. Evolution of aerobic metabolisms from anaerobiosis is a great specimen, as oxygen breathing is the dominant metabolism of the modern biosphere. Research on the origins of modern metabolisms can ultimately help us to explain how and when life on Earth start to drive biogeochemical cycles and to evaluate and predict the state of evolution of life on other planets.
How did microbes evolve to use O2? How did O2-dependent enzymes and pathways derive from or evolve under anoxic conditions? This central evolutionary mystery remains essentially unresolved, with conflicting opinions and fragments of evidence. PARAEDOX seeks ancient microbial genes to seek answers to those questions. By identifying novel but ancient metabolisms in reconstructing their evolutionary history, it hunts the knowledge of the evolution of aerobiosis on Earth.
I use ammonium oxidizers as a model species in PARAEDOX, a Marie Curie IF project. Findings will provide a major contribution to understanding the transition towards aerobiosis. The overall objectives of PARAEDOX are to discover novel ancient pathways in ammonium oxidizers, to characterize these remnant pathways and to identify their evolutionary history with an ambition to reveal their ancestral relation with aerobic pathways.
During 2018 and 2020, I carried out my Marie-Curie research at Harvard on physiological and genomic characterization of ancient pathways in ammonium oxidizers. At the second half of 2020, I studied at MIT to research molecular phylogenetics to elucidate the evolutionary history of ancient pathways. Firstly, physiological experiments were conducted during this period: (i) enrichments of ammonia oxidizers targeting on anticipated pathways and (ii) pure culture experiments on ammonia oxidizers were established. Isotopic and electrochemical signal tracing of the proposed pathways was executed, followed by genomic and transcription pattern characterisation. The evolutionary history of the proposed pathways was examined. In addition, proposed pathways were investigated within Oxygen Minimum Zones using microbial physiology and genomics tools.
Although my analyses are still under progress, the preliminary results revealed that the proposed pathways are ancient and still exist in the modern era. I discovered that a proposed microbial is dominant in oxygen minimum zones. Multiple evidence suggests the activity and expression of the anticipated pathways in ammonia oxidizers.
The findings in the PÆRADOX have the potential to revolutionize our view of the N cycle and on the evolution of aerobiosis. Identification of ancient pathways in ammonia-oxidizing prokaryotes will provide new perspectives on the interpretation of physiological signals in oxygen-deficient environments. The identification of activity and generality of the proposed pathways will reveal a previously unrecognized mechanism for reactive N transformation in the global N cycle, with implications for the carbon cycle through Earth’s history. The elucidation of evolutionary patterns of these pathways will provide a major contribution to unravelling the early evolution of aerobiosis and aerobic ammonium oxidation.
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