Defining lower limits of biodegradation: atrazine degradation regulated by mass transfer and maintenance demand inArthrobacter aurescensTC1

Abstract

Exploring adaptive strategies by which microorganisms function and survive in low-energy natural environments remains a grand goal of microbiology, and may help address a prime challenge of the 21st century: degradation of man-made chemicals at low concentrations (“micropollutants”). Here we explore physiological adaptation and maintenance energy requirements of a herbicide (atrazine)-degrading microorganism (Arthrobacter aurescens TC1) while concomitantly observing mass transfer limitations directly by compound-specific isotope fractionation analysis. Chemostat-based growth triggered the onset of mass transfer limitation at residual concentrations of 30 μg L−1 of atrazine with a bacterial population doubling time (td) of 14 days, whereas exacerbated energy limitation was induced by retentostat-based near-zero growth (td = 265 days) at 12 ± 3 μg L−1 residual concentration. Retentostat cultivation resulted in (i) complete mass transfer limitation evidenced by the disappearance of isotope fractionation (ε13C = −0.45‰ ± 0.36‰) and (ii) a twofold decrease in maintenance energy requirement compared with chemostat cultivation. Proteomics revealed that retentostat and chemostat cultivation under mass transfer limitation share low protein turnover and expression of stress-related proteins. Mass transfer limitation effectuated slow-down of metabolism in retentostats and a transition from growth phase to maintenance phase indicating a limit of ≈10 μg L−1 for long-term atrazine degradation. Further studies on other ecosystem-relevant microorganisms will substantiate the general applicability of our finding that mass transfer limitation serves as a trigger for physiological adaptation, which subsequently defines a lower limit of biodegradation.

Genome-scale reconstruction of Paenarthrobacter aurescens TC1 metabolic model towards the study of atrazine bioremediation

“…Model Reactions involved in atrazine degradation pathway and its further conversion into the cellular building blocks were added manually ( Fig. 1) based on the detailed reports of the relevant pathways in the specific strain 24,59 . P. aurescens TC1 degrades atrazine by hydrolytic dechlorination.…”

Phenotypic heterogeneity as key factor for growth and survival under oligotrophic conditions

“…Simulation results to demonstrate the benefit of two subpopulations in the environment Hypothetical scenario 1: Constant low substrate availability -Heterogenous adaptation allows survival of active 'growing' cells at a minimum substrate concentration. Growing cells have a relatively high metabolic activity, and hence, their energy requirement for maintaining particular subcellular processes such as sustaining the proton motive force, osmoregulation, protein turnover, repair and so on known as maintenance energy is much higher than in 'non-growing' cells (Van Bodegom, 2007;Kempes et al, 2017;Kundu et al, 2019). The maintenance energy of 'non-growing' cells is dependent on their physiological adaptation (Morita, 1997;Lever et al, 2015).…”

Toxicity of UV filters on marine bacteria: Combined effects with damaging solar radiation

“…Actinobacteria are involved in phosphate uptake and the degradation of cellulose, hemicellulose and chitin (Yilmaz et al, 2016). Within this phylum, Arthrobacter species are known to degrade PAH (Sawulski et al, 2014), polyethelyene (Balasubramanian et al, 2010), and metabolize pesticide (Kundu et al, 2019). The growth of two out of three Actinobacteria, including one Arthrobacter species, was altered by UV filters.…”