High-throughput sequencing and metagenomic analyses were coupled with geochemical data to elucidate mercury biogeochemical cycling within the East Antarctic sea-ice zone. In this study, sea-ice, brine, and seawater metagenomes sequenced from different time points and sampling locations were explored for their functional and taxonomic capacity for mercury cycling. The metagenomic analyses revealed a possible link between nitrite-oxidizing bacteria and the production of the bioaccumulative neurotoxin, methylmercury. Homologous mercury methylating genes (hgcA and hgcB) found in sea-ice, brine, and surface seawater samples, belonged to members of the microaerophilic nitrite-oxidizing clade Nitrospina. Nitrospina are commonly found in sea-ice, surface, and pelagic marine environments, and along with ammonia-oxidizing clade, Nitrosopumilus may play important roles in nitrogen cycling in polar marine waters. Nitrite-oxidizing genes (nxrA and nxrB) related to Nitrospina and ammonia oxidation genes (amoA) related to Nitrosopumilus were detected within the metagenomes. Although chemoautotrophic bacteria and archaea only constituted a small proportion of the sea-ice microbial population, they may play a significant role in polar mercury and nitrogen biogeochemical cycles. Overall, phototrophic eukaryotes and heterotrophic bacteria dominated sea-ice microbiomes. However, areas of intense heterotrophic activity and decaying organic matter within the sea ice may provide environmental niches for chemoautotrophs. Mercury-resistant bacteria were prevalent in the sea-ice metagenome, and were related to heterotrophic members of the Proteobacteria. The presence of mer-operons encoding Hg(II) resistance in the genomes of dominant members of the sea-ice microbiome, and notably distinct from those detected in Arctic environments, suggests the response of the community to mercury toxicity, potentially in response to atmospheric mercury depletion events (AMDE) occurring in the polar spring.