Studies were conducted in opposing gradients of oxygen and sulfide in microslide capillaries to (i) characterize the chemical microenvironment preferred by Candidatus Arcobacter sulfidicus, a highly motile, sulfur-oxidizing bacterium that produces sulfur in filamentous form, and (ii) to develop a model describing the mechanism of filamentous-sulfur formation. The highly motile microorganisms are microaerophilic, with swarms effectively aggregating within oxic-anoxic interfaces by exhibiting a chemotactic response. The position of the band was found to be largely independent of the sulfide concentration as it always formed at the oxic-anoxic interface. Flux calculations based on steady state gradients of oxygen and sulfide indicate that sulfide is incompletely oxidized to sulfur, in line with the formation of filamentous sulfur by these organisms. It is proposed that Candidatus Arcobacter sulfidicus effectively competes with other sulfur-oxidizing bacteria in the environment by being able to tolerate higher concentrations of hydrogen sulfide (1-2 mM) and by possessing the ability to grow at very low oxygen concentrations (1-10 muM). The formation of mat-like structures from filamentous sulfur appears to be a population mediated effort allowing these organisms to effectively colonize environments characterized by high sulfide, low oxygen and dynamic fluid movement.