Anaerobic sulfur oxidation underlies adaptation of a chemosynthetic symbiont to oxic-anoxic interfaces
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ABSTRACT:
PROVIDER: PRJNA609171 | ENA |
REPOSITORIES: ENA
Dataset's files
| Action | DRS | |||
|---|---|---|---|---|
| SRR11195886.fastq.gz | Fastqsanger.gz | |||
| SRR11195887.fastq.gz | Fastqsanger.gz | |||
| SRR11195888.fastq.gz | Fastqsanger.gz | |||
| SRR11195889.fastq.gz | Fastqsanger.gz | |||
| SRR11195890.fastq.gz | Fastqsanger.gz |
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Project description:Chemosynthetic symbioses occur worldwide in marine habitats, but comprehensive physiological studies of chemoautotrophic bacteria thriving on animals are scarce. Stilbonematinae are coated by monocultures of thiotrophic Gammaproteobacteria. As these nematodes migrate through the redox zone, their ectosymbionts experience varying oxygen concentrations. Here, by applying omics, Raman microspectroscopy and stable isotope labeling, we investigated the effect of oxygen on the metabolism of Candidatus Thiosymbion oneisti. Unexpectedly, sulfur oxidation genes were upregulated in anoxic relative to oxic conditions, but carbon fixation genes and incorporation of 13C-labeled bicarbonate were not. Instead, several genes involved in carbon fixation, organic carbon assimilation and polyhydroxyalkanoate (PHA) biosynthesis, as well as nitrogen fixation and urea utilization were upregulated in oxic conditions. Furthermore, in the presence of oxygen, stress-related genes were upregulated together with vitamin biosynthesis genes likely necessary to withstand its deleterious effects, and fewer symbionts were detected to divide. Based on this first global physiological study of an uncultured chemosynthetic ectosymbiont, we propose that, in anoxic sediment, its proliferation is powered by anaerobic sulfur oxidation coupled to denitrification, whereas in upper layers it makes use of aerobic respiration to facilitate assimilation of carbon and nitrogen, and to survive oxidative stress. The ectosymbiont’s versatile metabolism is thus well-adapted to exploiting a highly changeable environment.
2020-04-30 | GSE146081 | GEO
Project description:Chemosynthetic symbioses between bacteria and invertebrates occur worldwide in a wide range of marine habitats. Although they have been intensively investigated, molecular physiological studies of chemoautotrophic bacteria colonizing the surface of animals (ectosymbioses) are scarce. Stilbonematinae nematodes are the only known invertebrates capable of cultivating monocultures of thiotrophic Gammaproteobacteria on their surface. Crucially, as these nematodes migrate through the redox zone of marine sediments, the ectosymbionts directly experience drastic variations in oxygen concentration. Here, by applying an array of omics, Raman microspectroscopy and stable isotope labeling-based techniques, we investigated the effect of varying concentrations of dissolved oxygen on physiology and metabolism of Candidatus Thiosymbion oneisti, the longitudinally dividing ectosymbiont of Laxus oneistus. We show that, unexpectedly, sulfur oxidation genes were upregulated in anoxic relative to oxic conditions, and that carbon fixation genes and incorporation of 13C-labeled bicarbonate were not. Instead, several genes involved in carbon fixation in addition to genes responsible for assimilating organic carbon compounds and polyhydroxyalkanoate (PHA) biosynthesis, as well as nitrogen fixation and urea utilization genes were upregulated in oxic versus anoxic conditions. Furthermore, in the presence of oxygen, stress-related genes were upregulated together with vitamin and cofactor biosynthesis genes likely necessary to withstand its deleterious effects. Based on this first global physiological study of an uncultured, chemosynthetic ectosymbiont, we propose that, in anoxic pore water, it proliferates by utilizing nitrate to oxidize reduced sulfur compounds, whereas, when exposed to oxygen, it exploits aerobic respiration to facilitate energetically costly assimilation of carbon and nitrogen to survive oxidative stress. Both anaerobic sulfur oxidation and its decoupling from carbon fixation represent unprecedented adaptations among chemosynthetic symbionts. We postulate that Ca. T. oneisti originated from an obligate anaerobic, denitrifying sulfur-oxidizer, which, while transitioning from the free-living to the symbiotic lifestyle, evolved mechanisms to survive the oxidative stress inherent to a life attached to an animal.
2021-11-10 | PXD017709 | Pride
Project description:Chemosynthetic symbioses occur worldwide in marine habitats, but comprehensive physiological studies of chemoautotrophic bacteria thriving on animals are scarce. Stilbonematinae are coated by thiotrophic Gammaproteobacteria. As these nematodes migrate through the redox zone, their ectosymbionts experience varying oxygen concentrations. However, nothing is known about how these variations affect their physiology. Here, by applying omics, Raman microspectroscopy, and stable isotope labeling, we investigated the effect of oxygen on "Candidatus Thiosymbion oneisti." Unexpectedly, sulfur oxidation genes were upregulated in anoxic relative to oxic conditions, but carbon fixation genes and incorporation of 13C-labeled bicarbonate were not. Instead, several genes involved in carbon fixation were upregulated under oxic conditions, together with genes involved in organic carbon assimilation, polyhydroxyalkanoate (PHA) biosynthesis, nitrogen fixation, and urea utilization. Furthermore, in the presence of oxygen, stress-related genes were upregulated together with vitamin biosynthesis genes likely necessary to withstand oxidative stress, and the symbiont appeared to proliferate less. Based on its physiological response to oxygen, we propose that "Ca. T. oneisti" may exploit anaerobic sulfur oxidation coupled to denitrification to proliferate in anoxic sand. However, the ectosymbiont would still profit from the oxygen available in superficial sand, as the energy-efficient aerobic respiration would facilitate carbon and nitrogen assimilation. IMPORTANCE Chemoautotrophic endosymbionts are famous for exploiting sulfur oxidization to feed marine organisms with fixed carbon. However, the physiology of thiotrophic bacteria thriving on the surface of animals (ectosymbionts) is less understood. One longstanding hypothesis posits that attachment to animals that migrate between reduced and oxic environments would boost sulfur oxidation, as the ectosymbionts would alternatively access sulfide and oxygen, the most favorable electron acceptor. Here, we investigated the effect of oxygen on the physiology of "Candidatus Thiosymbion oneisti," a gammaproteobacterium which lives attached to marine nematodes inhabiting shallow-water sand. Surprisingly, sulfur oxidation genes were upregulated under anoxic relative to oxic conditions. Furthermore, under anoxia, the ectosymbiont appeared to be less stressed and to proliferate more. We propose that animal-mediated access to oxygen, rather than enhancing sulfur oxidation, would facilitate assimilation of carbon and nitrogen by the ectosymbiont.
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Project description:This SuperSeries is composed of the following subset Series: GSE15272: Diurnally synchronized transitions between oxic and anoxic physiologies in an archaeon, experiment "A" GSE15273: Diurnally synchronized transitions between oxic and anoxic physiologies in an archaeon, experiment "B" GSE15274: Diurnally synchronized transitions between oxic and anoxic physiologies in an archaeon, experiment "Control-1" GSE15275: Diurnally synchronized transitions between oxic and anoxic physiologies in an archaeon, experiment "C" GSE15276: Diurnally synchronized transitions between oxic and anoxic physiologies in an archaeon, experiment "Control-2" Refer to individual Series
2009-04-14 | E-GEOD-15282 | biostudies-arrayexpress
Project description:In order to ensure the reproducibility of the transcriptional response of Halobacterium NRC-1 to oxic/anoxic transitions, we repeated global mRNA measurements for the oxygen time series data in GSE5924, except that cultures were equilibrated to high oxygen for 12 hours prior to the start of the experiment rather than low oxygen. The results of these data suggest that there is good (~60%) reproducibility between datasets, and that Halobacterium responds robustly to oxic/anoxic transitions. Keywords: time series
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Project description:To understand the physiological response of Calu-3 cells to dual oxic-anoxic culture
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Project description:To gain a comprehensive systems-level understanding of cellular phenotypes, it is critical to characterize the relationship between the dynamic transcriptome and proteome during environmental perturbations. Previous comparisons have shown a lack of correlation between mRNA and protein level measurements suggesting a predominant role for post-transcriptional regulation in mediating cellular environmental responses. To investigate the extent of post-transcriptional regulation, we have analyzed transcriptome and proteome level changes over a 13-hour 28-point time course during transitions between oxic and anoxic physiologies of Halobacterium. Integrated computational analyses of these data show that temporally shifting mRNA and protein profiles relative to one another significantly increases the mRNA/protein correlation. Although time lags for unrelated genes vary widely, we observe similar temporal lags between the transcription and translation of functionally related genes. In contrast, no significant temporal separation was observed within the transcript profiles. Taken together, these data suggest that while there is indeed a direct correlation between many corresponding changes at mRNA and protein levels, translational delay may be the predominant mechanism for the temporal regulation of protein abundance during physiological oxic/anoxic transitions in Halobacterium. The approach and algorithms delineated in this study provide a framework for incorporating the temporal dimension of information processing across many different layers of gene regulation. Keywords: time course
2007-07-31 | GSE5924 | GEO
Project description:Wastewater from anoxic-oxic processes for swine wastewater treatment Metagenome
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Project description:By sensing changes in one or few environmental factors biological systems can anticipate future changes in multiple factors over a wide range of time scales (daily to seasonal). This anticipatory behavior is important to the fitness of diverse species, and in context of the diurnal cycle it is overall typical of eukaryotes and some photoautotrophic bacteria but is yet to be observed in archaea. Here, we report the first observation of light-dark (LD)-entrained diurnal oscillatory transcription in up to 12% of all genes of a halophilic archaeon Halobacterium salinarum NRC-1. Significantly, the diurnally entrained transcription was observed under constant darkness after removal of the LD stimulus (free-running rhythms). The memory of diurnal entrainment was also associated with the synchronization of oxic and anoxic physiologies to the LD cycle. Our results suggest that under nutrient limited conditions halophilic archaea take advantage of the causal influence of sunlight (via temperature) on O2 diffusivity in a closed hypersaline environment to streamline their physiology and operate oxically during nighttime and anoxically during daytime.
2009-04-15 | GSE15275 | GEO