Marine Archaeon Methanosarcina acetivorans Enhances Polyphosphate Metabolism Under Persistent Cadmium Stress

Abstract

Phosphate metabolism was studied to determine whether polyphosphate (polyP) pools play a role in the enhanced resistance against Cd²⁺ and metal-removal capacity of Cd²⁺-preadapted (CdPA) Methanosarcina acetivorans. Polyphosphate kinase (PPK), exopolyphosphatase (PPX) and phosphate transporter transcript levels and their activities increased in CdPA cells compared to control (Cnt) cells. K⁺ inhibited recombinant Ma-PPK and activated Ma-PPX, whereas divalent cations activated both enzymes. Metal-binding polyP and thiol-containing molecule contents, Cd²⁺-removal, and biofilm synthesis were significantly higher in CdPA cells >Cnt cells plus a single addition of Cd²⁺>Cnt cells. Also, CdPA cells showed a higher number of cadmium, sulfur, and phosphorus enriched-acidocalcisomes than control cells. Biochemical and physiological phenotype exhibited by CdPA cells returned to that of Cnt cells when cultured without Cd²⁺. Furthermore, no differences in the sequenced genomes upstream and downstream of the genes involved in Cd²⁺ resistance were found between CdPA and Cnt cells, suggesting phenotype loss rather than genome mutations induced by chronic Cd²⁺-exposure. Instead, a metabolic adaptation induced by Cd²⁺ stress was apparent. The dynamic ability of M. acetivorans to change its metabolism, depending on the environmental conditions, may be advantageous to remove cadmium in nature and biodigesters.

Keywords: archaeal metabolism; biofilm induction; exopolyphosphatase; heavy metal-binding molecules; methanogenesis; polyphosphate kinase.