81-12 Surface conformation as a control on nickel bioavailability in a deep-sea hyperthermophilic methanogen

Abstract:

Nickel, though a minor element in Earth’s crust, is essential for methanogens because methanogenesis requires the nickel-containing cofactor F₄₃₀ to catalyze the final step of methane production. As a result, nickel abundance in the rock record has been proposed as a biosignature for methanogenesis throughout Earth history. For example, declining nickel concentrations in late Archean banded iron formations have been linked to the Great Oxidation Event, given the strict anaerobic requirements of methanogens. Resolving such connections between nickel availability and methanogen activity requires a detailed understanding of how this metal interacts with cells. Metal uptake begins with adsorption to the cell surface, where functional groups act as the first step in bioavailability. Here, we probe the molecular-level interactions underlying nickel adsorption onto the surface of the deep-sea hyperthermophilic methanogen Methanocaldococcus FS406-22 using attenuated total reflectance Fourier transform infrared (ATR-FTIR) spectroscopy. Prior ATR-FTIR work on FS406-22 showed evidence of divalent cation-driven conformational changes to surface layer proteins, triggering significant changes to protonation behavior of the cellular envelope.  Building on this, we examined nickel adsorption with and without conformationally induced surface changes, as a function of nickel concentration and pH.  We observed distinct nickel-induced spectral shifts when concentrations exceeded 12 ppm, with the largest changes near pH 6 and shifts persisting, though reduced, at pH>6; notably, these shifts did not occur in NaCl solutions, highlighting the role of protein conformation in nutrient acquisition. Together, these findings demonstrate that nickel adsorption is fundamentally  linked to solution chemistry and protein conformation, a potential adaptive mechanism attuned for metal acquisition at the organism’s optimal growth conditions.  These data hint at the adaptability of methanogens to fluctuating solution chemistries through Earth history and to the geochemical signals they imprinted in the rock record.

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