Characterization of an Autotrophic Sulfide-Oxidizing Marine Arcobacter sp. That Produces Filamentous Sulfur

Abstract

A coastal marine sulfide-oxidizing autotrophic bacterium produces hydrophilic filamentous sulfur as a novel metabolic end product. Phylogenetic analysis placed the organism in the genus Arcobacter in the epsilon subdivision of the Proteobacteria. This motile vibrioid organism can be considered difficult to grow, preferring to grow under microaerophilic conditions in flowing systems in which a sulfide-oxygen gradient has been established. Purified cell cultures were maintained by using this approach. Essentially all 4,6-diamidino-2-phenylindole dihydrochloride-stained cells in a flowing reactor system hybridized with Arcobacter-specific probes as well as with a probe specific for the sequence obtained from reactor-grown cells. The proposed provisional name for the coastal isolate is "Candidatus Arcobacter sulfidicus." For cells cultured in a flowing reactor system, the sulfide optimum was higher than and the CO 2 fixation activity was as high as or higher than those reported for other sulfur oxidizers, such as Thiomicrospira spp. Cells associated with filamentous sulfur material demonstrated nitrogen fixation capability. No ribulose 1,5-bisphosphate carboxylase/oxygenase could be detected on the basis of radioisotopic activity or by Western blotting techniques, suggesting an alternative pathway of CO 2 fixation. The process of microbial filamentous sulfur formation has been documented in a number of marine environments where both sulfide and oxygen are available. Filamentous sulfur formation by "Candidatus Arcobacter sulfidicus" or similar strains may be an ecologically important process, contributing significantly to primary production in such environments.In the marine environment, hydrogen sulfide is a ubiquitous end product of anaerobic processes of organic matter remineralization (5,23,29,30). At ridge crest sites on the ocean floor, it is produced from the geothermal transformation of sulfate and elemental sulfur leaching via seawater-basaltic rock interaction (26,40,62). When brought into contact with the aerobic biosphere, hydrogen sulfide becomes an energy-yielding substrate for chemosynthetic colorless sulfur-oxidizing bacteria. Members of this group include free-living rods or ovoids of the genera Thiobacillus, Thiomonas, Acidiphilium, Thiomicrospira, and Thiovulum (31,32,34,42) as well as the morphologically conspicuous gliding and nongliding filamentous forms of the genera Beggiatoa, Thioploca, and Thiothrix (19,47,48,69). These organisms are characterized by their ability to catalyze the oxidation of sulfide and its chemically and biologically mediated partial oxidation products (polysulfides, S n 2Ϫ ; elemental sulfur, S 0 ; sulfane monosulfonic acids, HSS n O 3 2Ϫ ]; and polythionates, S n O 6 2Ϫ ) (14, 33, 66) coupled to the fixation of carbon dioxide to organic carbon by utilizing the same CalvinBassham-Benson cycle enzymes as those used by oxygenic phototrophs.Because of the differential rates of oxidation of hydrogen sulfide and derived oxidation products, intermediates may substantially accu...

Niche differentiation among sulfur-oxidizing bacterial populations in cave waters

“…This study is the first to our knowledge to retrieve a significant percentage of Arcobacter clones from a freshwater environment. A marine strain (Candidatus Arcobacter sulfidicus) that grows attached to solid substrates via filamentous sulfur strands in high-flow, microoxic, sulfidic environments has recently been described (Wirsen et al, 2002). Sulfide concentrations for growth of the marine Arcobacter (400-1200 mM) are broadly consistent with the Frasassi environment.…”

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

“…(⩽94 or ⩽ 95%, respectively), whereas Otu7 was 95% similar to Candidatus Arcobacter (Wirsen et al, 2002). Deltaproteobacteria OTUs were most abundant at the later time points d45 and d49 and were dominated by Otu3 (496% of the Deltaproteobacteria).…”

“…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.…”

“…Thiomargarita (Gammaproteobacteria) mats develop within highly dynamic habitats where hydrogen sulfide and oxygen (or nitrate) gradients are unstable . Arcobacter (Epsilonproteobacteria) mats develop in niches where hydrogen sulfide and oxygen co-occur (Wirsen et al, 2002;Moussard et al, 2006;Grünke et al, 2011). Finally, Beggiatoa (Gammaproteobacteria) mats reduce the narrow overlap region between hydrogen sulfide and oxygen (or nitrate) and promote a steep gradient within the mat (Felden, 2009).…”

Primary producing prokaryotic communities of brine, interface and seawater above the halocline of deep anoxic lake L'Atalante, Eastern Mediterranean Sea

“…(Fujiwara et al, 2001;Fang et al, 2006). This physiological group is characterized by the ability to gain energy from the oxidation of sulfide and other reduced sulfur products, which drives fixation of CO 2 to organic carbon by means of the enzymes of the Calvin-Bassham-Benson (CBB) cycle, similar to those used by oxygenic phototrophs (Wirsen et al, 2002).…”