Heterotrophic Sulfur Oxidation of Halomonas titanicae SOB56 and Its Habitat Adaptation to the Hydrothermal Environment

Abstract

Halomonas bacteria are ubiquitous in global marine environments, however, their sulfur-oxidizing abilities and survival adaptations in hydrothermal environments are not well understood. In this study, we characterized the sulfur oxidation ability and metabolic mechanisms of Halomonas titanicae SOB56, which was isolated from the sediment of the Tangyin hydrothermal field in the Southern Okinawa Trough. Physiological characterizations showed that it is a heterotrophic sulfur-oxidizing bacterium that can oxidize thiosulfate to tetrathionate, with the Na2S2O3 degradation reaching 94.86%. Two potential thiosulfate dehydrogenase-related genes, tsdA and tsdB, were identified as encoding key catalytic enzymes, and their expression levels in strain SOB56 were significantly upregulated. Nine of fifteen examined Halomonas genomes possess TsdA- and TsdB-homologous proteins, whose amino acid sequences have two typical Cys-X2-Cys-His heme-binding regions. Moreover, the thiosulfate oxidation process in H. titanicae SOB56 might be regulated by quorum sensing, and autoinducer-2 synthesis protein LuxS was identified in its genome. Regarding the mechanisms underlying adaptation to hydrothermal environment, strain SOB56 was capable of forming biofilms and producing EPS. In addition, genes related to complete flagellum assembly system, various signal transduction histidine kinases, heavy metal transporters, anaerobic respiration, and variable osmotic stress regulation were also identified. Our results shed light on the potential functions of heterotrophic Halomonas bacteria in hydrothermal sulfur cycle and revealed possible adaptations for living at deep-sea hydrothermal fields by H. titanicae SOB56.

Diversity of Mixotrophic Neutrophilic Thiosulfate- and Iron-Oxidizing Bacteria from Deep-Sea Hydrothermal Vents

“…The SUP05 clade of gammaproteobacteria (Thioglobaceae) could act as abundant autotrophs in the hydrothermal fluids and in association with eukaryotes at hydrothermal vents or as heterotrophes throughout the ocean [ 85 ]. The heterotrophic genera Pseudomonas , Halomonas , and Bacillus were all reported to possess the tetrathionate-forming ability using thiosulfate as a supplemental inorganic energy source [ 86 , 87 ]. Many strains in the Pseudomonas genus, such as strains of Pseudomonas stutzeri , were shown to oxidize sodium sulfide, change thiosulfate into tetrathionate, or grow on a variety of substrates, such as FeCl 2, FeCO 3 and FeSO 4 , as their sole energy source under anaerobically in the presence of nitrate [ 88 , 89 , 90 ].…”

Aquificae overcomes competition by archaeal thermophiles, and crowding by bacterial mesophiles, to dominate the boiling vent-water of a Trans-Himalayan sulfur-borax spring

“…Within the Lotus Pond metagenome, 3164 complete or partial CDSs (Tables S1 and S7) could be identified as involved in the biosynthesis of antibiotics such as the monobactams (816), streptomycin (788), prodigiosin (419), acarbose and validamycin (329), novobiocin (288), vancomycin (177), phenazine (105), carbapenems (96), penicillins and cephalosporins (85), neomycin/kanamycin/gentamicin (55), and staurosporine (6).…”

“…from hydrothermal vents or vent-adjacent environments, and found to exhibit varying degrees of thermal endurance [28,80,81,[83][84][85].…”

“…Thus, eight out of the 15 Lotus Pond MAGs, collectively accounting for 5.6% of the metagenome, were affiliated to genera encompassing strains that grow only at temperatures below the range known for Lotus Pond's vent-water. That said, Halomonas, Paracoccus, Tepidimonas, Thiofaba and Vibrio have been isolated from hydrothermal vents or vent-adjacent environments, and found to exhibit varying degrees of thermal endurance [30,94,95,[97][98][99].…”

“…Thus, eight out of the 15 Lotus Pond MAGs, collectively accounting for 5.6% of the metagenome, were affiliated to genera encompassing strains that grow only at temperatures below the range known for Lotus Pond's vent-water. That said, Halomonas, Paracoccus, Tepidimonas, Thiofaba and Vibrio have been isolated from hydrothermal vents or vent-adjacent environments, and found to exhibit varying degrees of thermal endurance [27,50,51,[53][54][55]. as YacG/PmbA/TldD which are known to nullify gyrase activity [58,59]; notably, several homologs of these genes ascribable to other mesophilic taxa were also present in the assembled metagenome.…”