Nitrogen is a fundamental element necessary for the synthesis of amino acids and nucleic acids, which are vital for the growth and functioning of living cells. Predominantly present in the atmosphere as dinitrogen (N₂), this inert form of nitrogen poses a significant challenge for most organisms, as it is not readily usable. To harness nitrogen from the atmosphere, it must first undergo a process called nitrogen fixation, whereby it is transformed into a more accessible form, most commonly ammonia. Through this bioconversion, plants and other organisms can utilize nitrogen for their metabolic needs.
Despite the plentiful availability of nitrogen in the air, the biological fixation of this element occurs primarily through two well-defined pathways: one is industrial, exemplified by the Haber-Bosch process, and the other is biological, executed by specialized microorganisms known as diazotrophs. Aiming to unravel a crucial aspect of the biological fixation pathway, researchers from the University of California San Diego, led by Professor Akif Tezcan and Assistant Professor Mark Herzik, have published their findings in the esteemed journal Nature.
The Haber-Bosch process, widely adopted in the early 20th century, revolutionized agriculture by facilitating the large-scale synthesis of fertilizers. Not only did this innovation drive agricultural productivity to unprecedented heights, but it also contributed significantly to the rapid increase in the global population. However, the process is labor-intensive and energy-consuming, typically requiring extreme temperatures and pressures, alongside copious amounts of hydrogen derived from fossil fuels. As a consequence, it has raised substantial environmental concerns due to the greenhouse gas emissions it generates.
Conversely, nitrogen fixation in nature is accomplished by diazotrophs, a group of nitrogen-fixing bacteria that harbor an enzyme known as nitrogenase. This remarkable enzyme operates efficiently at ambient conditions, freeing it from the energy restraints imposed by high pressures and temperatures characteristic of industrial methods. More importantly, nitrogenase does not produce greenhouse gases, rendering it a far more sustainable alternative for nitrogen fixation in ecosystems.
Nonetheless, while nitrogenase has evolved to facilitate the conversion of nitrogen, it is notably sensitive to oxygen, posing a challenge for diazotrophs that require oxygen for the ATP production necessary to fuel their metabolic processes. The conundrum lies in the requirement for diazotrophs to produce energy while simultaneously safeguarding nitrogenase from oxidative damage. This paradox has intrigued scientists for years, raising questions about the protective mechanisms employed by these microorganisms to shield nitrogenase from oxygen.
Diazotrophs have developed various protective strategies to counteract the detrimental impacts of oxygen, although some oxygen infiltration into their cells is inevitable during their metabolic activities. In moments of heightened oxygen presence, certain diazotrophs activate a unique strategy dubbed the “conformational protection mechanism.” This innovative mechanism employs an iron-sulfur protein named FeSII, which plays a crucial role in sensing oxygen levels within the cell.
When oxygen concentrations rise, FeSII binds to the nitrogenase enzyme complex, effectively shielding it from damage. This binding not only protects nitrogenase but also halts ammonia production until oxygen levels decrease again, at which point FeSII disengages, reactivating nitrogenase and resuming ammonia synthesis. While previous studies recognized the existence of FeSII, the precise molecular interactions governing its protective role remained a mystery until now.
The collaborative research initiative led by Tezcan and Herzik employed an array of advanced techniques to elucidate the underlying mechanism of FeSII’s protective action. First author Sarah Narehood characterized the complex interplay of nitrogenase dynamics while simultaneously leveraging advancements in cryogenic electron microscopy (cryoEM). Through a sophisticated method known as single-particle reconstruction, the team achieved near-atomic resolution imaging of the nitrogenase-FeSII complex. This novel approach allowed them to visualize how FeSII effectively “sandwiches” nitrogenase proteins, forming filamentous structures that obstruct oxygen from accessing the reactive metal cofactors essential for nitrogenase’s catalytic function.
This structural insight brought clarity to the manner in which FeSII provides conformational protection, yet questions lingered about its sensing capabilities. To address this, the researchers turned to small-angle X-ray scattering (SAXS), a technique that provides insights into protein dynamics in solution. SAXS experiments revealed that FeSII exhibits significant conformational changes in response to oxygen levels; in an oxygen-rich environment, FeSII adopts a compact shape, intimately fitting between nitrogenase proteins and facilitating their assembly into protective filaments. Conversely, under reduced oxygen conditions, FeSII reverts to a more relaxed structure, leading to the disassembly of these filaments and the restoration of nitrogenase function.
Further validation of their findings was achieved through the use of an analytical ultracentrifuge—a high-velocity spinning device that enables the precise measurement of protein sedimentation based on mass. This analysis confirmed that under increased oxygen exposure, FeSII effectively facilitates the aggregation of nitrogenase proteins into larger filamentous assemblies, thereby providing insights into the mechanisms of oxygen sensing and protection.
Having successfully deciphered the mechanism by which FeSII protects nitrogenase from oxidative damage, the research team is now poised to explore this protective activity in living bacterial cells. Their goal is to utilize cryoEM tomography to visualize the complete 3D architecture of diazotrophic cells actively facilitating nitrogen fixation in real time. This ambitious goal aims to elucidate the in vivo operation of FeSII and its protective functions, potentially unveiling even more intricate details about nitrogenase biology.
Despite nitrogenase’s crucial role in the biosphere and its continuing importance in agricultural contexts, a comprehensive understanding of its operational mechanics remains elusive. The insights garnered regarding the conformational protection mechanism have unveiled a pivotal aspect of the nitrogen fixation puzzle. Moreover, the implications of this research extend beyond theoretical interest; harnessing the nitrogenase pathway within plant systems could reduce humanity’s reliance on synthetic fertilizers, mitigating environmental impacts while sustaining agricultural productivity in a world grappling with population growth and ecological challenges.
In summary, the collaboration between chemists and biochemists at UC San Diego has brought forth a remarkable scientific breakthrough. By determining the structural and functional dynamics of the conformational protection mechanism involving FeSII and nitrogenase, they have unveiled an essential protein interaction that not only enhances our understanding of nitrogen fixation but also has the potential to significantly contribute to sustainable agricultural practices.
Subject of Research: The mechanism of nitrogenase protection from oxygen damage by FeSII proteins
Article Title: Structural basis for the conformational protection of nitrogenase from O2
News Publication Date: 8-Jan-2025
Web References: Nature Article
References: doi:10.1038/s41586-024-08311-1
Image Credits: Credit: Brian Cook and Sarah Narehood / UC San Diego
Keywords
Nitrogen fixation, nitrogenase, FeSII protein, cryogenic electron microscopy, oxygen protection, diazotrophs, amino acids, sustainable agriculture, environmental impact, biochemical pathways, enzymatic mechanisms, protein interactions.
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