Abstract
Present in many industrial effluents and as common degradation product of organic matter, phenol is a widespread compound which may cause serious environmental problems, due to its toxicity to animals and humans. Degradation of phenol from the environment by mesophilic bacteria has been studied extensively over the past decades, but only little is known about phenol biodegradation at high temperatures or low pH. In this work we studied phenol degradation in the thermoacidophilic archaeon Saccharolobus solfataricus P2 (basonym: Sulfolobus solfataricus) under extreme conditions (80°C, pH 3.5). We combined metabolomics and transcriptomics together with metabolic modeling to elucidate the organism’s response to growth with phenol as sole carbon source. Although S. solfataricus is able to utilize phenol for biomass production, the carbon source induces profound stress reactions, including genome rearrangement as well as a strong intracellular accumulation of polyamines. Furthermore, computational modeling revealed a 40% higher oxygen demand for substrate oxidation, compared to growth on glucose. However, only 16.5% of oxygen is used for oxidation of phenol to catechol, resulting in a less efficient integration of carbon into the biomass. Finally, our data underlines the importance of the phenol meta-degradation pathway in S. solfataricus and enables us to predict enzyme candidates involved in the degradation processes downstream of 2-hydroxymucconic acid.
Highlights
Phenol is a widespread environmental pollutant, present in the effluents of various industries including coal conversion, production of phenolic resins and the textile industry (Naguib and Badawy, 2020)
Phenotypic Characterization of S. solfataricus P2 Growing on Phenol as Sole Carbon Source
S. solfataricus showed a reduced growth rate and a lower biomass yield on 10 mM phenol compared to growth on 22 mM D-glucose (Supplementary Material S2)
Summary
Phenol is a widespread environmental pollutant, present in the effluents of various industries including coal conversion, production of phenolic resins and the textile industry (Naguib and Badawy, 2020). There have been several studies on thermophilic phenol degradation in Bacilli (Gurujeyalakshmi and Oriel, 1989; Antranikian, 1998; Duffner et al, 2000), Saccharolobus solfataricus (basonym: Sulfolobus solfataricus) was the first hyperthermophilic archaeon reported to be able to grow aerobically on phenol (Izzo et al, 2005). Since this organism has been studied extensively with respect to its phenol degrading capacity and evidence has been found for an active phenol meta-degradation pathway in S. solfataricus (Christen et al, 2011, 2012; Comte et al, 2013). The monooxygenase gene cluster and the catechol-2,3-diooxygenase of S. solfataricus have been characterized so far (Izzo et al, 2005; Chae et al, 2007)
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