Award: OCE-1129553

Manganese (Mn) oxide minerals play important roles in elemental biogeochemical cycles and represent an important economic resource. They are some of the strongest natural oxidants found in the environment and participate in a wide range of reactions with organic and inorganic chemicals. With great sorptive capacities, these "scavengers of the sea" control the distribution and bioavailability of many toxic and essential elements and thereby exert a control on oceanic primary productivity. Bacteria and fungi are primarily responsible for the Mn oxides found on the EarthÆs surface by transforming (oxidizing) soluble forms of Mn into insoluble Mn oxide minerals. Hydrothermal systems represent the major source of Mn to the deep ocean and are linked to the deposition of ferromanganese nodules, crusts and metalliferous sediments, mineral resources of great interest. Microbial activity has long been recognized as being important to the fate of Mn in these hydrothermal systems, yet we know very little about the organisms that catalyze Mn oxidation, the mechanisms by which Mn is oxidized or the physiological function that Mn oxidation provides the microorganisms . Because Mn oxide formation and Mn oxides are generally important in the deep sea, and those occurring in hydrothermal systems formed recently (unlike ferromanganese nodules and crusts), near vent hydrothermal Mn deposits are excellent model systems for beginning to unravel the Mn oxidation cycle in the deep sea. Additionally, while high temperature hydrothermal vents have attracted a lot of attention because of their extreme conditions and the potential to discover microorganisms specialized to extreme environments, the organisms that thrive at less extreme temperatures in more diffuse venting environments and which may be quantitatively more important in terms of overall elemental fluxes and transformations, have been largely understudied. The overarching goals of this project were to reveal the organisms and mechanism(s) underlying Mn mineral formation in the vast hydrothermal sediments where Mn oxides are found and to evaluate whether hydrothermal Mn oxidizing microorganisms may benefit by obtaining energy from Mn oxidation. From previous laboratory studies we have identified different types of genes responsible for Mn oxidation. In this project one goal was to determine whether these gene sequences correlated to the presence of Mn oxide minerals (and hence Mn oxidizing microorganisms) by comparing environmental genomic sequences (metagenomes) of microbial communities associated with ferromanganese (containing both Mn and Fe oxides) mat samples with samples of microbial mats containing only Fe oxides. A second goal was to assess the metabolic pathways by which carbon dioxide is incorporated into cell material in these samples as a way to test the possibility that some microbes obtain energy by oxidizing Mn and use this energy to grow. The results of our research demonstrate a strong correlation between the presence of genes known to be involved in Mn oxidation in organisms that have been studied in the laboratory and the presence of Mn oxides in the sample. Mn oxidation genes were not found in samples that contained no Mn oxides. We also found that one class of Mn oxidation genes was found in a defined genomic group (bin) that possessed the genes for the complete Calvin cycle, indicative that this group is capable of fixing carbon dioxide into cell (organic) material and thereby contribute to primary production. A second class of Mn oxidation genes was primarily associated with anaerobic bacteria; we hypothesize that these genes are involved in removing oxygen from the environment and protecting the bacteria from the toxic effects of oxygen. Finally, a third group of Mn oxidation genes were found in organisms that oxidize nitrogen compounds, suggesting a close relationship or possible coupling between the cycling of nitrogen and manganese in hydrothermal syste...