Dataset Information

Metabolic Response of "Candidatus Accumulibacter Phosphatis" Clade II C to Changes in Influent P/C Ratio.

ABSTRACT: The objective of this study was to investigate the ability of a culture highly enriched with the polyphosphate-accumulating organism, "Candidatus Accumulibacter phosphatis" clade IIC, to adjust their metabolism to different phosphate availabilities. For this purpose the biomass was cultivated in a sequencing batch reactor with acetate and exposed to different phosphate/carbon influent ratios during six experimental phases. Activity tests were conducted to determine the anaerobic kinetic and stoichiometric parameters as well as the composition of the microbial community. Increasing influent phosphate concentrations led to increased poly-phosphate content and decreased glycogen content of the biomass. In response to higher biomass poly-phosphate content, the biomass showed higher specific phosphate release rates. Together with the phosphate release rates, acetate uptake rates also increased up to an optimal poly-phosphate/glycogen ratio of 0.3 P-mol/C-mol. At higher poly-phosphate/glycogen ratios (obtained at influent P/C ratios above 0.051 P-mol/C-mol), the acetate uptake rates started to decrease. The stoichiometry of the anaerobic conversions clearly demonstrated a metabolic shift from a glycogen dominated to a poly-phosphate dominated metabolism as the biomass poly-phosphate content increased. FISH and DGGE analyses confirmed that no significant changes occurred in the microbial community, suggesting that the changes in the biomass activity were due to different metabolic behavior, allowing the organisms to proliferate under conditions with fluctuating phosphate levels.

SUBMITTER: Welles L

PROVIDER: S-EPMC5216660 | biostudies-literature | 2016

REPOSITORIES: biostudies-literature

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Metabolic Response of "<i>Candidatus</i> Accumulibacter Phosphatis" Clade II C to Changes in Influent P/C Ratio.

Welles Laurens L Abbas Ben B Sorokin Dimitry Y DY Lopez-Vazquez Carlos M CM Hooijmans Christine M CM van Loosdrecht Mark C M MC Brdjanovic Damir D

Frontiers in microbiology 20170105

The objective of this study was to investigate the ability of a culture highly enriched with the polyphosphate-accumulating organism, "<i>Candidatus</i> Accumulibacter phosphatis" clade IIC, to adjust their metabolism to different phosphate availabilities. For this purpose the biomass was cultivated in a sequencing batch reactor with acetate and exposed to different phosphate/carbon influent ratios during six experimental phases. Activity tests were conducted to determine the anaerobic kinetic a ...[more]

PMID: 28111570

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Project description:Candidatus Accumulibacter phosphatis is an important microorganism for enhanced biological phosphorus removal (EBPR). In a previous study, we found a remarkable flexibility regarding salinity, since this same microorganism could thrive in both freshwater- and seawater-based environments, but the mechanism for the tolerance to saline conditions remained unknown. Here, we identified and described the role of trehalose as an osmolyte in Ca. Accumulibacter phosphatis. A freshwater-adapted culture was exposed to a single batch cycle of hyperosmotic and hypo-osmotic shock, which led to the release of trehalose up to 5.34 mg trehalose/g volatile suspended solids (VSS). Long-term adaptation to 30% seawater-based medium in a sequencing batch reactor (SBR) gave a stable operation with complete anaerobic uptake of acetate and propionate along with phosphate release of 0.73 Pmol/Cmol, and complete aerobic uptake of phosphate. Microbial analysis showed Ca. Accumulibacter phosphatis clade I as the dominant organism in both the freshwater- and seawater-adapted cultures (> 90% presence). Exposure of the seawater-adapted culture to a single batch cycle of hyperosmotic incubation and hypo-osmotic shock led to an increase in trehalose release upon hypo-osmotic shock when higher salinity is used for the hyperosmotic incubation. Maximum trehalose release upon hypo-osmotic shock was achieved after hyperosmotic incubation with 3× salinity increase relative to the salinity in the SBR adaptation reactor, resulting in the release of 11.9 mg trehalose/g VSS. Genome analysis shows the possibility of Ca. Accumulibacter phosphatis to convert glycogen into trehalose by the presence of treX, treY, and treZ genes. Addition of trehalose to the reactor led to its consumption, both during anaerobic and aerobic phases. These results indicate the flexibility of the metabolism of Ca. Accumulibacter phosphatis towards variations in salinity. KEY POINTS: • Trehalose is identified as an osmolyte in Candidatus Accumulibacter phosphatis. • Ca. Accumulibacter phosphatis can convert glycogen into trehalose. • Ca. Accumulibacter phosphatis clade I is present and active in both seawater and freshwater.

Project description:Environmental fluctuations in the availability of nutrients lead to intricate metabolic strategies. "Candidatus Accumulibacter phosphatis," a polyphosphate-accumulating organism (PAO) responsible for enhanced biological phosphorus removal (EBPR) from wastewater treatment systems, is prevalent in aerobic/anaerobic environments. While the overall metabolic traits of these bacteria are well described, the nonavailability of isolates has led to controversial conclusions on the metabolic pathways used. In this study, we experimentally determined the redox cofactor preferences of different oxidoreductases in the central carbon metabolism of a highly enriched "Ca Accumulibacter phosphatis" culture. Remarkably, we observed that the acetoacetyl coenzyme A reductase engaged in polyhydroxyalkanoate (PHA) synthesis is NADH preferring instead of showing the generally assumed NADPH dependency. This allows rethinking of the ecological role of PHA accumulation as a fermentation product under anaerobic conditions and not just a stress response. Based on previously published metaomics data and the results of enzymatic assays, a reduced central carbon metabolic network was constructed and used for simulating different metabolic operating modes. In particular, scenarios with different acetate-to-glycogen consumption ratios were simulated, which demonstrated optima using different combinations of glycolysis, glyoxylate shunt, or branches of the tricarboxylic acid (TCA) cycle. Thus, optimal metabolic flux strategies will depend on the environment (acetate uptake) and on intracellular storage compound availability (polyphosphate/glycogen). This NADH-related metabolic flexibility is enabled by the NADH-driven PHA synthesis. It allows for maintaining metabolic activity under various environmental substrate conditions, with high carbon conservation and lower energetic costs than for NADPH-dependent PHA synthesis. Such (flexible) metabolic redox coupling can explain the competitiveness of PAOs under oxygen-fluctuating environments.IMPORTANCE Here, we demonstrate how microbial storage metabolism can adjust to a wide range of environmental conditions. Such flexibility generates a selective advantage under fluctuating environmental conditions. It can also explain the different observations reported in PAO literature, including the capacity of "Ca Accumulibacter phosphatis" to act like glycogen-accumulating organisms (GAOs). These observations stem from slightly different experimental conditions, and controversy arises only when one assumes that metabolism can operate only in a single mode. Furthermore, we also show how the study of metabolic strategies is possible when combining omics data with functional cofactor assays and modeling. Genomic information can only provide the potential of a microorganism. The environmental context and other complementary approaches are still needed to study and predict the functional expression of such metabolic potential.

Project description:The ability of "Candidatus Accumulibacter phosphatis" to grow and remove phosphorus from wastewater under cycling anaerobic and aerobic conditions has also been investigated as a metabolism that could lead to simultaneous removal of nitrogen and phosphorus by a single organism. However, although phosphorus removal under cyclic anaerobic and anoxic conditions has been demonstrated, clarifying the role of "Ca. Accumulibacter phosphatis" in this process has been challenging, since (i) experimental research describes contradictory findings, (ii) none of the published "Ca. Accumulibacter phosphatis" genomes show the existence of a complete respiratory pathway for denitrification, and (iii) some genomes lacking a complete respiratory pathway have genes for assimilatory nitrate reduction. In this study, we used an integrated omics analysis to elucidate the physiology of a "Ca. Accumulibacter phosphatis" strain enriched in a reactor operated under cyclic anaerobic and microaerobic conditions. The reactor's performance suggested the ability of the enriched "Ca. Accumulibacter phosphatis" strain (clade IC) to simultaneously use oxygen and nitrate as electron acceptors under microaerobic conditions. A draft genome of this organism was assembled from metagenomic reads ("Ca. Accumulibacter phosphatis" UW-LDO-IC) and used as a reference to examine transcript abundance throughout one reactor cycle. The genome of UW-LDO-IC revealed the presence of a full pathway for respiratory denitrification. The observed transcript abundance patterns showed evidence of coregulation of the denitrifying genes along with a cbb3 cytochrome, which has been characterized as having high affinity for oxygen. Furthermore, we identified an FNR-like binding motif upstream of the coregulated genes, suggesting transcription-level regulation of both denitrifying and respiratory pathways in UW-LDO-IC. Taking the results together, the omics analysis provides strong evidence that "Ca. Accumulibacter phosphatis" UW-LDO-IC uses oxygen and nitrate simultaneously as electron acceptors under microaerobic conditions. IMPORTANCE "Candidatus Accumulibacter phosphatis" is widely found in full-scale wastewater treatment plants, where it has been identified as the key organism for biological removal of phosphorus. Since aeration can account for 50% of the energy use during wastewater treatment, microaerobic conditions for wastewater treatment have emerged as a cost-effective alternative to conventional biological nutrient removal processes. Our report provides strong genomics-based evidence not only that "Ca. Accumulibacter phosphatis" is the main organism contributing to phosphorus removal under microaerobic conditions but also that this organism simultaneously respires nitrate and oxygen in this environment, consequently removing nitrogen and phosphorus from the wastewater. Such activity could be harnessed in innovative designs for cost-effective and energy-efficient optimization of wastewater treatment systems.

Dataset Information

Metabolic Response of "Candidatus Accumulibacter Phosphatis" Clade II C to Changes in Influent P/C Ratio.

Publications

Metabolic Response of "<i>Candidatus</i> Accumulibacter Phosphatis" Clade II C to Changes in Influent P/C Ratio.

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