Electron cryo-tomography reveals the surface layer (S-layer) structure of an abundant marine microbe that is crucial to the global nitrogen cycle.
Nitrosopumilus maritimus (N. maritimus) is an ammonia-oxidizing archaeon that can also produce molecular oxygen under anoxic conditions in a process completely unrelated to photosynthesis. These characteristics, together with the abundance of N. maritimus in the oceans, makes it an important player in the global geochemical cycles.
Ammonium ions (fully reduced nitrogen) are the sole energy source for these abundant microbes, and these microorganisms have evolved specialised molecular mechanisms to efficiently harvest ammonium from dilute marine environments for energy production with nitrogen oxidation. However, it has been unclear how ammonium ions are trapped by these microbes living in the depths of the oceans. Tanmay Bharat’s group, in the LMB’s Structural Studies Division, has shed light on this mystery by solving the structure of the molecular machinery responsible for ammonium enrichment, consisting of the surface layer (S-layer) from N. maritimus.
The study, led by postdoctoral researcher Andriko von Kügelgen, reports the molecular structure of the S-layer directly from cells. The group used electron cryo-tomography (cryo-ET) and subtomogram averaging, a powerful image processing technique that aligns multiple 3D volumes of the target complex with averaging to obtain a high-resolution atomic structure within the native environment of cells and tissues. For the microbiology field, this study reports a long-sought function for S-layers, providing an explanation why microbes harbour these abundant molecules on their surfaces at such high copy numbers.
The S-layer provides a large surface area for interaction with the surrounding marine environment, where it acts as a multichannel cation exchanger. Ammonium and other cations (positively charged ions) are bound at the cell surface by the negatively charged S-layer. Due to its gradually increasing negative charge proximal to the cell, ammonium ions accumulate on its cell-facing side, where they can be oxidised.
This in situ structural study illuminates the biogeochemical process of ammonium binding and channelling, common to many marine microorganisms that ultimately control the availability of nitrite, a nitrogen source available to marine phytoplankton. The nitrogen cycle is one of the global geochemical cycles essential for maintaining life on earth. N. maritimus is also capable of converting carbon dioxide to oxygen, so an increased molecular understanding of the organism is crucial to further illuminate integral processes to the continuance of life on Earth.
Finally, this study also shows the efficacy of using cryo-ET and subtomogram averaging to solve molecular structures directly from cells, which paves the way for future studies on a wide range of molecules in their native context.
This work was funded by UKRI MRC, the Human Frontier Science Program, the Vallee Research Foundation, EMBO, the Leverhulme Trust, the Lister Institute for Preventative Medicine, the European Research Council, the University of Missouri-Columbia, the Max Planck Society, and the Horizon 2020 program.
Further references
Membraneless channels sieve cations in ammonia-oxidizing marine archaea. von Kügelgen, A., Cassidy, C.K., van Dorst, S., Pagani, L.L., Batters, C., Ford, Z., Löwe, J., Alva, V., Stansfeld, P.K., and Bharat, T.A.M. Nature.
Tanmay’s group page
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