Abstract
Enhanced biological phosphorus removal (EBPR) involves the cycling of biomass through carbon-rich (feast) and carbon-deficient (famine) conditions, promoting the activity of polyphosphate accumulating organisms (PAOs). However, several alternate metabolic strategies, without polyphosphate storage, are possessed by other organisms, which can compete with the PAO for carbon at the potential expense of EBPR efficiency. The most studied are the glycogen accumulating organisms (GAOs), which utilize aerobically stored glycogen to energize anaerobic substrate uptake and storage. In full-scale systems the Micropruina spp. are among the most abundant of the proposed GAO, yet little is known about their ecophysiology. In the current study, genomic and metabolomic studies were performed on Micropruina glycogenica str. Lg2T and compared to the in situ physiology of members of the genus in EBPR plants using state-of-the-art single cell techniques. The Micropruina spp. were observed to take up carbon, including sugars and amino acids, under anaerobic conditions, which were partly fermented to lactic acid, acetate, propionate, and ethanol, and partly stored as glycogen for potential aerobic use. Fermentation was not directly demonstrated for the abundant members of the genus in situ, but was strongly supported by the confirmation of anaerobic uptake of carbon and glycogen storage in the absence of detectable polyhydroxyalkanoates or polyphosphate reserves. This physiology is markedly different from the classical GAO model. The amount of carbon stored by fermentative organisms has potentially important implications for phosphorus removal – as they compete for substrates with the Tetrasphaera PAO and stored carbon is not made available to the “Candidatus Accumulibacter” PAO under anaerobic conditions. This study shows that the current models of the competition between PAO and GAO are too simplistic and may need to be revised to take into account the impact of potential carbon storage by fermentative organisms.
Highlights
Enhanced biological phosphorus removal (EBPR) activated sludge systems have been widely implemented for the removal of nutrients from wastewaters
The results show that the classical view of polyphosphate accumulating organisms (PAOs)–glycogen accumulating organisms (GAOs) interactions in full-scale EBPR systems needs to be revised
Glucose, the main carbon sources utilized in pure culture incubations, are likely converted to pyruvate via the Embden– Meyerhof–Parnas (EMP) glycolysis pathway and by annotated alanine dehydrogenases (MPLG2_3627; MPLG2_3728), respectively
Summary
Enhanced biological phosphorus removal (EBPR) activated sludge systems have been widely implemented for the removal of nutrients from wastewaters. Some organisms exhibiting the classical GAO and PAO phenotypes reportedly utilize sugars and amino acids directly for PHA production (Liu et al, 1996; Burow et al, 2007; Oyserman et al, 2015) and some may ferment glycogen stores or glucose to lactate as an additional anaerobic energy source (McIlroy et al, 2014). In addition to the fermentative actinobacterial PAO, it has been shown that in dynamic feast–famine systems unidentified organisms can store glucose directly as glycogen anaerobically, energized by fermentation, without cycling polyphosphate (Carucci et al, 1999) The role of these “fermentative GAO” in EBPR is of interest, given their potential as competitors of the abundant fermentative Tetrasphaera PAO. The results show that the classical view of PAO–GAO interactions in full-scale EBPR systems needs to be revised
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