Growth and mechanism of filamentous‐sulfur formation by Candidatus Arcobacter sulfidicus in opposing oxygen‐sulfide gradients

Abstract

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.

Ecological succession leads to chemosynthesis in mats colonizing wood in sea water

“…These bacteria, like the chemolithoautotroph Candidatus A. sulfidicusrelated OTU (Otu7), would prefer to fix the inorganic carbon present in seawater. Arcobacter-related OTUs may be responsible for the white coloration observed on our mat because they do an incomplete oxidation of sulfide to elemental sulfur, which produces white sulfur filaments visible to the naked eye (Wirsen et al, 2002;Sievert et al, 2007). In addition to the visual observation of this elemental sulfur, we detected Deferribacteres OTUs that might utilize this Figure 6 Schematic illustration of the ecological succession within the epixylic mat.…”

“…This genera of sulfatereducing bacteria is strictly anaerobic, uses fermentation end products as a carbon source, respires sulfate and thus produces hydrogen sulfide (Pradel et al, 2013). The mat thickness increase with time may be linked to the displacement of the oxygensulfide interface from the wood surface toward the seawater as observed on other Epsilonproteobacteria mats (Wirsen et al, 2002;Sievert et al, 2007). This displacement limits the penetration of potential electron acceptors like oxygen and nitrate, thus promoting the development of anaerobic and nitrate depleted niches (Van Houten et al, 1994;Okabe et al, 2005) on the wood side of the mat as shown by the microsensor measurements taken in our second experiment (Figure 5c).…”

“…Another dominant Epsilonproteobacteria (Otu8) was closely related to Arcobacter nitrofigilis (Pati et al, 2010), which is a chemoorganotrophic bacteria that use nitrate as electron acceptor. The white appearance of the biofilm may indicate the capacity of Otu8 to produce elemental sulfur from hydrogen sulfide oxidation as observed for Candidatus Arcobacter sulfidicus (Wirsen et al, 2002;Sievert et al, 2007). Hydrogen sulfide or organic compounds (used by the A. nitrofigilisrelated Otu8) were all shown to be breakdown products of wood degradation (Leschine, 1995; 6.6 6.8 7.0 7.2 7.4 7.6 7.…”

Central Role of the Cell in Microbial Ecology

“…The degree of flexibility in regard to oxygen not only defines the ecological niches of specific organisms but largely affects cultivation success (202). Recently, several microaerophilic organisms that thrive strictly at the oxic-anoxic interface and tolerate oxygen only at specific and low concentrations have been isolated (55,153,193,216). To maximize the cultivation success, the simulation of the natural environmental conditions is critical, and the degree of specificity increases with the specificity of the requirements and tolerances of the organism.…”

Productivity, metabolism and physiology of free-living chemoautotrophic Epsilonproteobacteria

“…For example, in all incubations, the amount of nitrate and oxygen consumed was never sufficient to account for the complete oxidation of sulfide to sulfate (supplemental spreadsheet), suggesting that sulfide was oxidized to an intermediate oxidation state sulfur species. Some autotrophic Epsilonproteobacteria can catalyze sulfide oxidation to elemental sulfur (S 0 ) (Wirsen et al, 2002;Sievert et al, 2007), and indeed white flocculent material (likely composed of S 0 ) continuously emanates from Crab Spa.…”