The ecological niche of nitrate-storing Beggiatoa, and their contribution to the removal of sulfide were investigated in coastal sediment. With microsensors a clear suboxic zone of 2-10 cm thick was identified, where neither oxygen nor free sulfide was detectable. In this zone most of the Beggiatoa were found, where they oxidize sulfide with internally stored nitrate. The sulfide input into the suboxic zone was dominated by an upward sulfide flux from deeper sediment, whereas the local production in the suboxic zone was much smaller. Despite their abundance, the calculated sulfideoxidizing capacity of the Beggiatoa could account for only a small fraction of the total sulfide removal in the sediment. Consequently, most of the sulfide flux into the suboxic layer must have been removed by chemical processes, mainly by precipitation with Fe 2 þ and oxidation by Fe(III), which was coupled with a pH increase. The free Fe 2 þ diffusing upwards was oxidized by Mn(IV), resulting in a strong pH decrease. The nitrate storage capacity allows Beggiatoa to migrate randomly up and down in anoxic sediments with an accumulated gliding distance of 4 m before running out of nitrate. We propose that the steep sulfide gradient and corresponding high sulfide flux, a typical characteristic of Beggiatoa habitats, is not needed for their metabolic performance, but rather used as a chemotactic cue by the highly motile filaments to avoid getting lost at depth in the sediment. Indeed sulfide is a repellant for Beggiatoa.

Marine sediments are frequently covered by mats of the filamentous Beggiatoa and other large nitrate-storing bacteria that oxidize hydrogen sulfide using either oxygen or nitrate, which they store in intracellular vacuoles. Despite their conspicuous metabolic properties and their biogeochemical importance, little is known about their genetic repertoire because of the lack of pure cultures. Here, we present a unique approach to access the genome of single filaments of Beggiatoa by combining whole genome amplification, pyrosequencing, and optical genome mapping. Sequence assemblies were incomplete and yielded average contig sizes of approximately 1 kb. Pathways for sulfur oxidation, nitrate and oxygen respiration, and CO2 fixation confirm the chemolithoautotrophic physiology of Beggiatoa. In addition, Beggiatoa potentially utilize inorganic sulfur compounds and dimethyl sulfoxide as electron acceptors. We propose a mechanism of vacuolar nitrate accumulation that is linked to proton translocation by vacuolar-type ATPases. Comparative genomics indicates substantial horizontal gene transfer of storage, metabolic, and gliding capabilities between Beggiatoa and cyanobacteria. These capabilities enable Beggiatoa to overcome non-overlapping availabilities of electron donors and acceptors while gliding between oxic and sulfidic zones. The first look into the genome of these filamentous sulfur-oxidizing bacteria substantially deepens the understanding of their evolution and their contribution to sulfur and nitrogen cycling in marine sediments.