Abstract

The modern nitrogen cycle consists of a web of microbially mediated redox transformations. Among the most crucial reactions in this cycle is the oxidation of ammonia to nitrite, an obligately aerobic process performed by a limited number of lineages of bacteria (AOB) and archaea (AOA). As this process has an absolute requirement for O2, the timing of its evolution—especially as it relates to the Great Oxygenation Event ~ 2.3 billion years ago—remains contested and is pivotal to our understanding of nutrient cycles. To estimate the antiquity of bacterial ammonia oxidation, we performed phylogenetic and molecular clock analyses of AOB. Surprisingly, bacterial ammonia oxidation appears quite young, with crown group clades having originated during Neoproterozoic time (or later) with major radiations occurring during Paleozoic time. These results place the evolution of AOB broadly coincident with the pervasive oxygenation of the deep ocean. The late evolution AOB challenges earlier interpretations of the ancient nitrogen isotope record, predicts a more substantial role for AOA during Precambrian time, and may have implications for understanding of the size and structure of the biogeochemical nitrogen cycle through geologic time.

Highlights

  • The modern nitrogen cycle consists of a web of microbially mediated redox transformations

  • The evolution of oxygenic photosynthesis in Cyanobacteria led to the accumulation of atmospheric ­O2 to biologically meaningful concentrations ~ 2.3 billion years ago (Ga) during the Great Oxygenation Event (GOE), and it has been suggested that the onset of the aerobic nitrogen cycle occurred shortly t­ hereafter[8]

  • We show that ammonia oxidation in bacteria has evolved convergently at least twice and that crown group AOB clades originated

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Summary

Introduction

The modern nitrogen cycle consists of a web of microbially mediated redox transformations. Among the most crucial reactions in this cycle is the oxidation of ammonia to nitrite, an obligately aerobic process performed by a limited number of lineages of bacteria (AOB) and archaea (AOA). As this process has an absolute requirement for ­O2, the timing of its evolution—especially as it relates to the Great Oxygenation Event ~ 2.3 billion years ago—remains contested and is pivotal to our understanding of nutrient cycles. Bacterial ammonia oxidation appears quite young, with crown group clades having originated during Neoproterozoic time (or later) with major radiations occurring during Paleozoic time These results place the evolution of AOB broadly coincident with the pervasive oxygenation of the deep ocean. This suggests that bacteria did Scientific Reports | (2021) 11:2070

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