Characterization of an anaerobic marine microbial community exposed to combined fluxes of perchlorate and salinity

The recent recognition of the environmental prevalence of perchlorate and its discovery on Mars, Earth’s moon, and in meteorites, in addition to its novel application to controlling oil reservoir sulfidogenesis, has resulted in a renewed interest in this exotic ion and its associated microbiology. However, while plentiful data exists on freshwater perchlorate respiring organisms, information on their halophilic counterparts and microbial communities is scarce. Here, we investigated the temporal evolving structure of perchlorate respiring communities under a range of NaCl concentrations (1, 3, 5, 7, and 10 % wt/vol) using marine sediment amended with acetate and perchlorate. In general, perchlorate consumption rates were inversely proportional to NaCl concentration with the most rapid rate observed at 1 % NaCl. At 10 % NaCl, no perchlorate removal was observed. Transcriptional analysis of the 16S rRNA gene indicated that salinity impacted microbial community structure and the most active members were in families Rhodocyclaceae (1 and 3 % NaCl), Pseudomonadaceae (1 NaCl), Campylobacteraceae (1, 5, and 7 % NaCl), Sedimenticolaceae (3 % NaCl), Desulfuromonadaceae (5 and 7 % NaCl), Pelobacteraceae (5 % NaCl), Helicobacteraceae (5 and 7 % NaCl), and V1B07b93 (7 %). Novel isolates of genera Sedimenticola, Marinobacter, Denitromonas, Azoarcus, and Pseudomonas were obtained and their perchlorate respiring capacity confirmed. Although the obligate anaerobic, sulfur-reducing Desulfuromonadaceae species were dominant at 5 and 7 % NaCl, their enrichment may result from biological sulfur cycling, ensuing from the innate ability of DPRB to oxidize sulfide. Additionally, our results demonstrated enrichment of an archaeon of phylum Parvarchaeota at 5 % NaCl. To date, this phylum has only been described in metagenomic experiments of acid mine drainage and is unexpected in a marine community. These studies identify the intrinsic capacity of marine systems to respire perchlorate and significantly expand the known diversity of organisms capable of this novel metabolism.