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

Welles, Laurens; Abbas, Ben; Sorokin, Dimitry Y.; López-Vázquez, Carlos M.; Hooijmans, Christine M.; Loosdrecht, Mark C.M. van; Brdjanović, Damir

doi:10.3389/fmicb.2016.02121

Cited by 37 publications

(21 citation statements)

References 62 publications

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“…Accumulibacter subclades switched from IA to IIA. Previously, Acevedo et al (2012) and Welles et al (2015, 2017) showed that both clades of Ca . Accumulibacter could solely rely on glycogen for the generation of ATP and NADH under phosphate limiting conditions.…”

Section: Discussionmentioning

confidence: 94%

Effect of Lactate on the Microbial Community and Process Performance of an EBPR System

et al. 2019

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Candidatus Accumulibacter phosphatis is in general presented as the dominant organism responsible for the biological removal of phosphorus in activated sludge wastewater treatment plants. Lab-scale enhanced biological phosphorus removal (EBPR) studies, usually use acetate as carbon source. However, the complexity of the carbon sources present in wastewater could allow other potential poly-phosphate accumulating organism (PAOs), such as putative fermentative PAOs (e.g., Tetrasphaera ), to proliferate in coexistence or competition with Ca . Accumulibacter. This research assessed the effects of lactate on microbial selection and process performance of an EBPR lab-scale study. The addition of lactate resulted in the coexistence of Ca . Accumulibacter and Tetrasphaera in a single EBPR reactor. An increase in anaerobic glycogen consumption from 1.17 to 2.96 C-mol/L and anaerobic PHV formation from 0.44 to 0.87 PHV/PHA C-mol/C-mol corresponded to the increase in the influent lactate concentration. The dominant metabolism shifted from a polyphosphate-accumulating metabolism (PAM) to a glycogen accumulating metabolism (GAM) without EBPR activity. However, despite the GAM, traditional glycogen accumulating organisms (GAOs; Candidatus Competibacter phosphatis and Defluvicoccus ) were not detected. Instead, the 16s RNA amplicon analysis showed that the genera Tetrasphaera was the dominant organism, while a quantification based on FISH-biovolume indicated that Ca . Accumulibacter remained the dominant organism, indicating certain discrepancies between these microbial analytical methods. Despite the discrepancies between these microbial analytical methods, neither Ca . Accumulibacter nor Tetrasphaera performed biological phosphorus removal by utilizing lactate as carbon source.

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Section: Discussionmentioning

confidence: 94%

Effect of Lactate on the Microbial Community and Process Performance of an EBPR System

et al. 2019

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“…For both cultures, anaerobic P-release per C-fed indicated that the PAO present in the sludge are likely saturated with polyphosphate and that glycogen accumulating organisms (GAO) are not present (37). Furthermore, microbial characterization by FISH showed Accumulibacter from clade I were the majority of the microorganisms across all biomass samples as it can be seen by the high overlap between the Accumulibacter-specific probe and the general Bacteria probe (micrographs available in Supplementary Document S3).…”

Section: Resultsmentioning

confidence: 99%

“…Experiments show that the ratio between glycogen and acetate consumption by PAOs is variable, e.g. between high/low temperature (42) or polyphosphate/glycogen availability (37, 43, 44). To reflect this variability, simulations were performed for a range of acetate and glycogen mixtures ranging from only acetate to only glycogen and results were compared to experimental data reported in literature.…”

Section: Resultsmentioning

confidence: 99%

“…The minimum carbon conserving strategy is the one that only uses the oxidative TCA branch. Experimental datasets were retrieved from (10, 37, 50–59, 41, 42, 44–49) and normalized to respect carbon and energy conservation principles (see Supplementary Document S5). Similar plots for Pr-CoA*, CO 2 , alternative simulations and including error bars on the experimental data points can be found in Supplementary Document S6.…”

Section: Resultsmentioning

confidence: 99%

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Revealing metabolic flexibility ofCandidatusAccumulibacter phosphatis through redox cofactor analysis and metabolic network modeling

Silva

Olavarría

Gomes

et al. 2018

Preprint

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23Environmental fluctuations in the availability of nutrients lead to intricate 24 metabolic strategies. Candidatus Accumulibacter phosphatis, a polyphosphate 25 accumulating organism (PAO) responsible for enhanced biological phosphorus 26 removal (EBPR) from wastewater treatment systems, is prevalent in 27 aerobic/anaerobic environments. While the overall metabolic traits of these 28 bacteria are well described, the inexistence of isolates has led to controversial 29 conclusions on the metabolic pathways used. 30Here, we experimentally determined the redox cofactor preference of 31 different oxidoreductases in the central carbon metabolism of a highly enriched 32 Ca. A. phosphatis culture. Remarkably, we observed that the acetoacetyl-CoA 33 reductase engaged in polyhydroxyalkanoates (PHA) synthesis is NADH-34 preferring instead of the generally assumed NADPH dependency. Based on 35 previously published meta-omics data and the results of enzymatic assays, a 36 reduced central carbon metabolic network was constructed and used for 37 simulating different metabolic operating modes. In particular, scenarios with 38 different acetate-to-glycogen consumption ratios were simulated. For a high 39 ratio (i.e. more acetate), a polyphosphate-based metabolism arises as optimal 40 with a metabolic flux through the glyoxylate shunt. In case of a low acetate-to-41 glycogen ratio, glycolysis is used in combination with reductive branch of the 42 TCA cycle. Thus, optimal metabolic flux strategies will depend on the 43 environment (acetate uptake) and on intracellular storage compounds 44 availability (polyphosphate/glycogen). 45 This metabolic flexibility is enabled by the NADH-driven PHA synthesis. It 46 allows for maintaining metabolic activity under varying environmental substrate 47 3 conditions, with high carbon conservation and lower energetic costs compared 48 to NADPH dependent PHA synthesis. Such (flexible) metabolic redox coupling 49 can explain PAOs' competitiveness under oxygen-fluctuating environments. 50 IMPORTANCE 51 Here we demonstrate how microbial metabolism can adjust to a wide range 52 of environmental conditions. Such flexibility generates a selective advantage 53 under fluctuating environmental conditions. It can also explain the different 54 observations reported in PAO literature, including the capacity of Ca. 55Accumulibacter phosphatis to act like glycogen accumulating organisms 56 (GAO). These observations stem from slightly different experimental conditions 57 and controversy only arises when one assumes metabolism can only operate 58 in one single mode. Furthermore, we also show how the study of metabolic 59 strategies is possible when combining -omics data with functional assays and 60 modeling. Genomic information can only provide the potential of a 61 microorganism. The environmental context and other complementary 62 approaches are still needed to study and predict the functional application of 63 such metabolic potential. 64

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“…Previous studies reported PAOs mainly affiliated with the Rhodocyclus group of the Betaproteobacteria, which were named "Candidatus Accumulibacter phosphatis" (6). From laboratory-scale to full-scale EBPR systems, "Candidatus Accumulibacter" was a numerically dominant PAO (7,8). Real-time quantitative PCR (qPCR) and fluorescence in situ hybridization (FISH) are the primary approaches for quantitative analysis of PAOs.…”

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confidence: 99%

Population Structure and Morphotype Analysis of “ Candidatus Accumulibacter” Using Fluorescence In Situ Hybridization-Staining-Flow Cytometry

Zeng

Guo

et al. 2019

Appl Environ Microbiol

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“Candidatus Accumulibacter” is the dominant polyphosphate-accumulating organism (PAO) in denitrifying phosphorus removal (DPR) systems. In order to investigate the community structure and clade morphotypes of “Candidatus Accumulibacter” in DPR systems through flow cytometry (FCM), denitrifying phosphorus removal of almost 100% using nitrite and nitrate as the electron acceptor was achieved in sequencing batch reactors (SBRs). An optimal method of flow cytometry combined with fluorescence in situ hybridization and SYBR green I staining (FISH-staining-flow cytometry) was developed to quantify PAOs in DPR systems. By setting the width value of FCM, bacterial cells in a sludge sample were divided into three groups in different morphotypes, namely, coccus, coccobacillus, and bacillus. Average percentages that the three different PAO populations accounted for among total bacteria from SBR1 (SBR2) were 42% (45%), 14% (13%), and 4% (2%). FCM showed that the ratios of PAOs to total bacteria in the two reactors were 61% and 59%, and the quantitative PCR (qPCR) results indicated that IIC was the dominant “Candidatus Accumulibacter” clade in both denitrifying phosphorus removal systems, reaching 50% of the total “Candidatus Accumulibacter” bacteria. The subdominant clade in the reactor with nitrite as the electron acceptor was IID, accounting for 31% of the total “Candidatus Accumulibacter” bacteria. The FCM and qPCR results suggested that clades IIC and IID were both coccus, clade IIF was coccobacillus, and clade IA was bacillus. FISH analysis also indicated that PAOs were major cocci in the systems. An equivalence test of FCM-based quantification confirmed the accuracy of FISH-staining-flow cytometry, which can meet the quantitative requirements for PAOs in complex activated sludge samples. IMPORTANCE As one group of the most important functional phosphorus removal organisms, “Candidatus Accumulibacter,” affiliated with the Rhodocyclus group of the Betaproteobacteria, is a widely recognized and studied PAO in the field of biological wastewater treatment. The morphotypes and population structure of clade-level “Candidatus Accumulibacter” were studied through novel FISH-staining-flow cytometry, which involved denitrifying phosphorus removal (DPR) achieving carbon and energy savings and simultaneous removal of N and P, thus inferring the different denitrifying phosphorus removal abilities of these clades. Additionally, based on this method, in situ quantification for specific polyphosphate-accumulating organisms (PAOs) enables a more efficient process and more accurate result. The establishment of FISH-staining-flow cytometry makes cell sorting of clade-level noncultivated organisms available.

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

Cited by 37 publications

References 62 publications

Effect of Lactate on the Microbial Community and Process Performance of an EBPR System

Effect of Lactate on the Microbial Community and Process Performance of an EBPR System

Revealing metabolic flexibility ofCandidatusAccumulibacter phosphatis through redox cofactor analysis and metabolic network modeling

Population Structure and Morphotype Analysis of “ Candidatus Accumulibacter” Using Fluorescence In Situ Hybridization-Staining-Flow Cytometry

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