8Metabolically-active obligate aerobes are unheard-of in tightly-anoxic environments. Present 2 9culture-independent and culture-dependent investigations revealed aerobic microbial 3 0 communities along two, ~3-meter-long sediment-cores underlying the eastern Arabian Sea 3 1 oxygen minimum zone, where high H 2 S disallows O 2 influx from the water-column. While genes 3 2 for aerobic respiration by aa 3 -/cbb 3 -type cytochrome-c oxidases and cytochrome-bd ubiquinol 3 3 oxidase, and aerobic oxidation of methane/ammonia/alcohols/thiosulfate/sulfite/organosulfur-3 4 compounds, were present across the cores, so were live aerobic, sulfur-chemolithoautotrophs 3 5 and chemoorganoheterotrophs. The 8820-years-old, highly-sulfidic, methane-containing 3 6 sediment-sample from 275 cmbsf of 530 mbsl yielded many such obligately-aerobic bacterial-3 7 isolates that died upon anaerobic incubation with alternative electron-acceptors/fermentative-3 8 substrates. Several metatranscriptomic reads from this sediment-sample matched aerobic-3 9 respiration-/oxidase-reaction-/transcription-/translation-/DNA-replication-/membrane-transport-4 0 /cell-division-related genes of the obligately-aerobic isolates, thereby corroborating their active 4 1 aerobic metabolic-status in situ. Metagenomic and metatranscriptomic detection of perchlorate-4 2
The ecology of aerobic microorganisms is never explored in marine oxygen minimum zone (OMZ) sediments. Here we reveal aerobic bacterial communities along ∼3 m sediment-horizons of the eastern Arabian Sea OMZ. Sulfide-containing sediment-cores retrieved from 530 mbsl (meters beneath the sea-level) and 580 mbsl were explored at 15–30 cm intervals, using metagenomics, pure-culture-isolation, genomics and metatranscriptomics. Genes for aerobic respiration, and oxidation of methane/ammonia/alcohols/thiosulfate/sulfite/organosulfur-compounds, were detected in the metagenomes from all 25 sediment-samples explored. Most probable numbers for aerobic chemolithoautotrophs and chemoorganoheterotrophs at individual sample-sites were up to 1.1 × 107 (g sediment)−1. The sediment-sample collected from 275 cmbsf (centimeters beneath the seafloor) of the 530-mbsl-core yielded many such obligately aerobic isolates belonging to Cereibacter, Guyparkeria, Halomonas, Methylophaga, Pseudomonas and Sulfitobacter which died upon anaerobic incubation, despite being provided all possible electron acceptors and fermentative substrates. High percentages of metatranscriptomic reads from the 275 cmbsf sediment-sample, and metagenomic reads from all 25 sediment-samples, matched the isolates’ genomic sequences including those for aerobic metabolisms, genetic/environmental information processing and cell division, thereby illustrating the bacteria's in-situ activity, and ubiquity across the sediment-horizons, respectively. The findings hold critical implications for organic carbon sequestration/remineralization, and inorganic compounds oxidation, within the sediment realm of global marine OMZs.
Abstract. To explore the potential role of tetrathionate in the sedimentary sulfur cycle, population ecology of microorganisms capable of metabolizing this polythionate was revealed at 15–30 cm resolution along two, ∼3 m long, cores collected from 530 and 580 m below the sea level, off India's west coast, within the oxygen minimum zone (OMZ) of the Arabian Sea. Metagenome analysis along the cores revealed widespread occurrence of genes involved in the formation, oxidation, and reduction of tetrathionate; high diversity and relative abundance were also detected for bacteria that are known to render these metabolisms in vitro. Results of slurry culture of the sediment samples in thiosulfate- or tetrathionate-containing microbial growth media, data obtained via pure-culture isolation, and finally metatranscriptome analyses corroborated the in situ functionality of the tetrathionate-forming, tetrathionate-oxidizing, and tetrathionate-reducing microorganisms. Ion chromatography of pore waters revealed the presence of up to 11.1 µM thiosulfate in the two cores, whereas tetrathionate remained undetected in spectroscopic assay based on its reaction with cyanide. While thiosulfate oxidation by chemolithotrophic bacteria prevalent in situ is the apparent source of tetrathionate in this ecosystem, high biochemical and geochemical reactivity of this polythionate could be instrumental in its cryptic status in the sulfur cycle. Potential abiotic origin of tetrathionate in the sediment horizon explored could neither be ruled out nor confirmed from the geochemical information available. On the other hand, tetrathionate potentially present in the system can be either oxidized to sulfate or reduced back to thiosulfate/sulfide via chemolithotrophic oxidation and respiration by native bacterial populations, respectively. Up to 2.01 mM sulfide present in the sediment cores may also reduce tetrathionate abiotically to thiosulfate and elemental sulfur. However, in the absence of measured data for O2 or other oxyanions having possibilities of serving as electron acceptors, the biogeochemical modalities of the oxidative half of the tetrathionate cycle remained unresolved.
For a holistic understanding of microbial life’s high-temperature adaptation, it is imperative to explore the biology of the phylogenetic relatives of mesophilic bacteria which get stochastically introduced to geographically and geologically diverse hot spring systems by local geodynamic forces. Here, in vitro endurance of high heat up to the extent of growth under special (habitat-inspired) conditions was discovered in a hot-spring-dwelling phylogenetic relative of the mesophilic Paracoccus species. Thermal conditioning, extreme oligotrophy, metabolic deceleration, presence of certain habitat-specific inorganic/organic solutes, and potential genomic specializations were found to be the major enablers of this conditional (acquired) thermophilicity.
Abstract. Marine sedimentation rate and bottom-water O2 concentration control organic carbon remineralization and sequestration across continental margins, but whether and how they shape microbiome architecture (the ultimate effector of all biogeochemical phenomena) across shelf and slope sediments is still unclear. Here we reveal distinct microbiome structures and functions, amidst comparable pore fluid chemistries, along 300 cm sediment horizons underlying the seasonal (shallow coastal; water depth: 31 m) and perennial (deep sea; water depths: 530 and 580 m) oxygen minimum zones (OMZs) of the Arabian Sea, situated across the western Indian margin. The sedimentary geomicrobiology was elucidated by analyzing metagenomes, metatranscriptomes, enrichment cultures, and depositional rates measured via radiocarbon and lead excess dating; the findings were then evaluated in light of the other geochemical data available for the cores. Along the perennial-OMZ sediment cores, microbial communities were dominated by Gammaproteobacteria and Alphaproteobacteria, but in the seasonal-OMZ core communities were dominated by Euryarchaeota and Firmicutes. As a perennial-OMZ signature, a cryptic methane production–consumption cycle was found to operate near the sediment surface, within the sulfate reduction zone; overall diversity, as well as the relative abundances of anaerobes requiring simple fatty acids (methanogens, anaerobic methane oxidizers, sulfate reducers, and acetogens), peaked in the topmost sediment layer and then declined via synchronized fluctuations until the sulfate–methane transition zone was reached. The microbiome profile was completely reversed in the seasonal-OMZ sediment horizon. In the perennial-OMZ sediments, deposited organic carbon was higher in concentration and rich in marine components that degrade readily to simple fatty acids; simultaneously, lower sedimentation rate afforded higher O2 exposure time for organic matter degradation despite perennial hypoxia in the bottom water. The resultant abundance of reduced carbon substrates eventually sustained multiple inter-competing microbial processes in the upper sediment layers. The entire geomicrobial scenario was opposite in the sediments of the seasonal OMZ. These findings create a microbiological baseline for understanding carbon–sulfur cycling in distinct depositional settings and water column oxygenation regimes across the continental margins.
Chemolithotrophic sulfur oxidation represents a significant part of the biogeochemical cycling of this element. Due to its long evolutionary history, this ancient metabolism is well known for its extensive mechanistic and phylogenetic diversification across a diverse taxonomic spectrum. Here we carried out whole-genome sequencing and analysis of a new betaproteobacterial isolate, Pusillimonas ginsengisoli SBSA, which is found to oxidize thiosulfate via the formation of tetrathionate as an intermediate. The 4.7 Mb SBSA genome was found to encompass a soxCDYZAXOB operon, plus single thiosulfate dehydrogenase (tsdA) and sulfite : acceptor oxidoreductase (sorAB) genes. Recombination-based knockout of tsdA revealed that the entire thiosulfate is first converted to tetrathionate by the activity of thiosulfate dehydrogenase (TsdA) and the Sox pathway is not functional in this bacterium despite the presence of all necessary sox genes. The ∆soxYZ and ∆soxXA knockout mutants exhibited a wild-type-like phenotype for thiosulfate/tetrathionate oxidation, whereas ∆soxB, ∆soxCD and soxO::KanR mutants only oxidized thiosulfate up to tetrathionate intermediate and had complete impairment in tetrathionate oxidation. The substrate-dependent O2 consumption rate of whole cells and the sulfur-oxidizing enzyme activities of cell-free extracts, measured in the presence/absence of thiol inhibitors/glutathione, indicated that glutathione plays a key role in SBSA tetrathionate oxidation. The present findings collectively indicate that the potential glutathione : tetrathionate coupling in P. ginsengisoli involves a novel enzymatic component, which is different from the dual-functional thiol dehydrotransferase (ThdT), while subsequent oxidation of the sulfur intermediates produced (e.g. glutathione : sulfodisulfane molecules) may proceed via the iterative action of soxBCD .
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