Adaptations of Methanococcus maripaludis to its unique lifestyle

Abstract

Methanococcus maripaludis is an obligate anaerobic, methane-producing archaeon. In addition to the unique methanogenesis pathway, unconventional biochemistry is present in this organism in adaptation to its unique lifestyle. The Sac10b homolog in M. maripaludis, Mma10b, is not abundant and constitutes only ~ 0.01% of the total cellular protein. It binds to DNA with sequence-specificity. Disruption of mma10b resulted in poor growth of the mutant in minimal medium. These results suggested that the physiological role of Mma10b in the mesophilic methanococci is greatly diverged from the homologs in thermophiles, which are highly abundant and associate with DNA without sequence-specificity. M. maripaludis synthesizes lysine through the DapL pathway, which uses diaminopimelate aminotransferase (DapL) to catalyze the direct transfer of an amino group from L-glutamate to L-tetrahydrodipicolinate (THDPA), forming LL-diaminopimelate (LL-DAP). This is different from the conventional acylation pathway in many bacteria that convert THDPA to LL-DAP in three steps: succinylation or acetylation, transamination, and desuccinylation or deacetylation. The DapL pathway eliminates the expense of using succinyl-CoA or acetyl-CoA and may represent a thriftier mode for lysine biosynthesis. Methanogens synthesize cysteine primarily on tRNACys via the two-step SepRS/SepCysS pathway. In the first step, tRNACys is aminoacylated with O-phosphoserine (Sep) by O-phosphoseryl-tRNA synthetase (SepRS). In the second step, the Sep moiety on Sep-tRNACys is converted to cysteine with a sulfur source to form Cys-tRNACys by Sep-tRNA:Cys-tRNA synthase (SepCysS). The nature of the physiological sulfur donor for the tRNA-dependent cysteine biosynthesis is unknown. Based upon activity assays in M. maripaludis cell extracts, a rhodanese-like, protein-mediated sulfur transfer is proposed to be involved in the sulfur assimilation for cysteine biosynthesis. This is different from cysteine biosynthesis in enteric bacteria and plants, which use direct sulfhydrylation with sulfide. Finally, M. maripaludis does not use cysteine as the sulfur source for Fe-S cluster biosynthesis. Instead, the sulfur in Fe-S clusters is derived predominantly from exogenous sulfide. This challenges the concept that cysteine is always the sulfur source for Fe-S cluster biosynthesis. The unique sulfur metabolism in M. maripaludis may be an adaptation to sulfide-rich living environments.