Microbiology of ‘<i>Candidatus</i> Accumulibacter’ in activated sludge

He, Shaomei; McMahon, Katherine D.

doi:10.1111/j.1751-7915.2011.00248.x

Cited by 116 publications

(94 citation statements)

References 103 publications

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“…This supports the notion that Accumulibacter varies its phosphate transport capabilities under changing EBPR conditions, and suggests that floccular and granular biofilms may have further phosphate transport differences (Wilmes, Andersson, et al, 2008;Burow et al, 2008;He & McMahon, 2011b). There were also differences between Accumulibacter proteins involved in denitrification pathways detected in Floc and Gran biofilms.…”

Section: Proteins Involved In Accumulibacter Core Metabolismsupporting

confidence: 77%

Metagenomic and metaproteomic analyses of Accumulibacter phosphatis‐enriched floccular and granular biofilm

Barr

Dutilh

Skennerton

et al. 2015

Environmental Microbiology

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Biofilms are ubiquitous in nature, forming diverse adherent microbial communities that perform a plethora of functions. Here we operated two laboratory-scale sequencing batch reactors enriched with Candidatus Accumulibacter phosphatis (Accumulibacter) performing enhanced biological phosphorus removal (EBPR). Reactors formed two distinct biofilms, one floccular biofilm, consisting of small, loose, microbial aggregates, and one granular biofilm, forming larger, dense, spherical aggregates. Using metagenomic and metaproteomic methods we investigated the proteomic differences between these two biofilm communities, identifying a total of 2,022 unique proteins. To understand biofilm differences, we compared protein abundances that were statistically enriched in both biofilm states. Floccular biofilms were enriched with pathogenic secretion systems suggesting a highly competitive microbial community. Comparatively, granular biofilms revealed a high stress environment with evidence of nutrient starvation, phage predation pressure, and increased extracellular polymeric substance (EPS) and cell lysis. Granular biofilms were enriched in outer membrane transport proteins to scavenge the extracellular milieu for amino acids and other metabolites, likely released through cell lysis, to supplement metabolic pathways. This study provides the first detailed proteomic comparison between Accumulibacter-enriched floccular and granular biofilm communities, proposes a conceptual model for the granule biofilm, and offers novel insights into granule biofilm formation and stability.

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Section: Proteins Involved In Accumulibacter Core Metabolismsupporting

confidence: 77%

Metagenomic and metaproteomic analyses of Accumulibacter phosphatis‐enriched floccular and granular biofilm

Barr

Dutilh

Skennerton

et al. 2015

Environmental Microbiology

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“…In P. aeruginosa, we find that polyP acts postinitiation to permit efficient completion of open rounds of DNA replication and cell division following nitrogen starvation, and polyP and (p)ppGpp have additive roles in organizing the nucleoid during starvation. The discovery in the 1950s that bacteria synthesize polyP from ATP during nutritional downshift initiated a debate that has remained unresolved for more than half a century as to whether this polymer serves as a physiologically relevant energy store (29)(30)(31). Although polyP may have functions deeper in starvation or cell cycle reentry as an energy store, our results imply that when it drives completion of open rounds of cell division during starvation, net synthesis rather than consumption of polyP is required.…”

Section: Discussionmentioning

confidence: 83%

Polyphosphate granule biogenesis is temporally and functionally tied to cell cycle exit during starvation in Pseudomonas aeruginosa

Racki

Tocheva

Dieterle

et al. 2017

Proc. Natl. Acad. Sci. U.S.A.

111

112

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Polyphosphate (polyP) granule biogenesis is an ancient and ubiquitous starvation response in bacteria. Although the ability to make polyP is important for survival during quiescence and resistance to diverse environmental stresses, granule genesis is poorly understood. Using quantitative microscopy at high spatial and temporal resolution, we show that granule genesis in Pseudomonas aeruginosa is tightly organized under nitrogen starvation. Following nucleation as many microgranules throughout the nucleoid, polyP granules consolidate and become transiently spatially organized during cell cycle exit. Between 1 and 3 h after nitrogen starvation, a minority of cells have divided, yet the total granule number per cell decreases, total granule volume per cell dramatically increases, and individual granules grow to occupy diameters as large as ∼200 nm. At their peak, mature granules constitute ∼2% of the total cell volume and are evenly spaced along the long cell axis. Following cell cycle exit, granules initially retain a tight spatial organization, yet their size distribution and spacing relax deeper into starvation. Mutant cells lacking polyP elongate during starvation and contain more than one origin. PolyP promotes cell cycle exit by functioning at a step after DNA replication initiation. Together with the universal starvation alarmone (p)ppGpp, polyP has an additive effect on nucleoid dynamics and organization during starvation. Notably, cell cycle exit is temporally coupled to a net increase in polyP granule biomass, suggesting that net synthesis, rather than consumption of the polymer, is important for the mechanism by which polyP promotes completion of cell cycle exit during starvation.ost of our understanding of bacterial physiology comes from laboratory studies of bacteria growing under nutrientrich conditions. However, in many environments, bacteria face dramatic fluctuations in nutrient conditions, including long periods of scarcity when they survive in a nonproliferative stationary state. Although eukaryotic cells and some bacteria have discrete cell cycle checkpoints, many fast-growing bacterial species have uncoupled DNA replication and cell division. They use multifork DNA replication to achieve a doubling time that is faster than the time required to copy the chromosome, giving them a competitive edge in nutrient-replete conditions. This strategy requires distinct regulatory mechanisms and comes at a considerable cost when there is a rapid downshift in nutrient availability: stalled open DNA replication forks are vulnerable to potentially lethal double-stranded DNA breaks (1). Therefore, the ability to reallocate resources under such conditions to prioritize completion of DNA replication is critical for survival. Prioritizing chromosome remodeling and compaction by starvation-specific nucleoid structural proteins is also important during such transitions because resources for DNA repair become limited in deep starvation (2-4). Operating an uncoupled cell cycle, where growth, DNA replication, and cell ...

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“…Accumulibacter" (11,36) The capacity for storage of acetate as PHA by "Ca. Accumulibacter" is controlled by the intracellular pools of poly(P) and glycogen (2,17,37,38). Glycine uptake by Tetrasphaera is likely also controlled by the amount of intracellular poly(P) available to provide energy for substrate uptake by the action of the low-affinity Pit transporter that is present in all known PAOs, including Tetrasphaera (12,35).…”

Section: Discussionmentioning

confidence: 99%

Intracellular Accumulation of Glycine in Polyphosphate-Accumulating Organisms in Activated Sludge, a Novel Storage Mechanism under Dynamic Anaerobic-Aerobic Conditions

Nguyen

Kristiansen

Vestergaard

et al. 2015

Appl Environ Microbiol

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Dynamic anaerobic-aerobic feast-famine conditions are applied to wastewater treatment plants to select polyphosphate-accumulating organisms to carry out enhanced biological phosphorus removal. Acetate is a well-known substrate to stimulate this process, and here we show that different amino acids also are suitable substrates, with glycine as the most promising.13 C-labeled glycine and nuclear magnetic resonance (NMR) were applied to investigate uptake and potential storage products when activated sludge was fed with glycine under anaerobic conditions. Glycine was consumed by the biomass, and the majority was stored intracellularly as free glycine and fermentation products. Subsequently, in the aerobic phase without addition of external substrate, the stored glycine was consumed. The uptake of glycine and oxidation of intracellular metabolites took place along with a release and uptake of orthophosphate, respectively. Fluorescence in situ hybridization combined with microautoradiography using 3 H-labeled glycine revealed uncultured actinobacterial Tetrasphaera as a dominant glycine consumer. Experiments with Tetrasphaera elongata as representative of uncultured Tetrasphaera showed that under anaerobic conditions it was able to take up labeled glycine and accumulate this and other labeled metabolites to an intracellular concentration of approximately 4 mM. All components were consumed under subsequent aerobic conditions. Intracellular accumulation of amino acids seems to be a novel storage strategy for polyphosphate-accumulating bacteria under dynamic anaerobic-aerobic feast-famine conditions. T he wastewater treatment process known as enhanced biological phosphorus removal (EBPR) is a widely employed process in wastewater treatment for removal of phosphorus (P). The principle is to create favorable conditions for the enrichment of microorganisms capable of excess uptake and storage of orthophosphate (P i ) as polyphosphate [poly(P)], based on alternating anaerobic and aerobic periods (1). Early metabolic models detailed that in the anaerobic phase, polyphosphateaccumulating organisms (PAOs) take up volatile fatty acids (e.g., acetate and propionate), using polyphosphate as an energy source. These substrates are reduced and stored as intracellular polyhydroxyalkanoates (PHA) with energy obtained from hydrolysis of intracellular polyphosphate and energy and reducing power from glycolysis of intracellular glycogen (2), the tricarboxylic acid (TCA) cycle (3), or both (4). In the subsequent aerobic or denitrifying phase, the PAOs use PHA for growth and for replenishing their polyphosphate and glycogen reserves (5). As the quantity of phosphate removed during the aerobic stage is greater than that released during the initial anaerobic stage, a net removal of phosphate from the wastewater is achieved.While PAOs share the metabolic ability for accumulation of polyphosphate as an energy storage compound, they are phylogenetically diverse (6-9). Rhodocyclus-related bacteria ("Candidatus Accumulibacter"), belonging to the B...

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Microbiology of ‘Candidatus Accumulibacter’ in activated sludge

Cited by 116 publications

References 103 publications

Metagenomic and metaproteomic analyses of Accumulibacter phosphatis‐enriched floccular and granular biofilm

Metagenomic and metaproteomic analyses of Accumulibacter phosphatis‐enriched floccular and granular biofilm

Polyphosphate granule biogenesis is temporally and functionally tied to cell cycle exit during starvation in Pseudomonas aeruginosa

Intracellular Accumulation of Glycine in Polyphosphate-Accumulating Organisms in Activated Sludge, a Novel Storage Mechanism under Dynamic Anaerobic-Aerobic Conditions

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