Sulfur Amino Acid Status Controls Selenium Methylation in Pseudomonas tolaasii: Identification of a Novel Metabolite from Promiscuous Enzyme Reactions

Abstract

Selenium (Se) deficiency affects many millions of people worldwide, and the volatilization of methylated Se species to the atmosphere may prevent Se from entering the food chain. Despite the extent of Se deficiency, little is known about fluxes in volatile Se species and their temporal and spatial variation in the environment, giving rise to uncertainty in atmospheric transport models. To systematically determine fluxes, one can rely on laboratory microcosm experiments to quantify Se volatilization in different conditions. Here, it is demonstrated that the sulfur (S) status of bacteria crucially determines the amount of Se volatilized. Solid phase microextraction gas chromatography mass spectrometry showed that Pseudomonas tolaasii efficiently and rapidly (92% in 18h) volatilized Se to dimethyldiselenide and dimethylselenylsulfide through promiscuous enzymatic reactions with the S metabolism. However, when the cells were supplemented with cystine (but not methionine), a major proportion of the Se (∼48%) was channelled to thus far unknown, non-volatile Se compounds at the expense of the previously formed dimethyldiselenide and dimethylselenylsulfide (accounting for < 4% of total Se). Ion chromatography and solid phase extraction were used to isolate unknowns, and electrospray ionization ion trap mass spectrometry, electrospray ionization quadrupole time-of-flight mass spectrometry and microprobe nuclear magnetic resonance spectrometry were used to identify the major unknown as a novel Se metabolite, 2-hydroxy-3-(methylselanyl)propanoic acid. Environmental S concentrations often exceed Se concentrations by orders of magnitude. This suggests that in fact S status may be a major control on selenium fluxes to the atmosphere. Importance Volatilization from soil to the atmosphere is a major driver for Se deficiency. "Bottom up" models for atmospheric Se transport are based on laboratory experiments quantifying volatile Se compounds. The high Se and low S concentrations in such studies poorly represent the environment. Here, we show that S amino acid status has in fact a decisive effect on the production of volatile Se species in Pseudomonas tolaasii. When the strain was supplemented with S amino acids, a major proportion of the Se was channelled to thus far unknown, non-volatile Se compounds at the expense of volatile compounds. This hierarchical control of the microbial S amino acid status on Se cycling has been thus far neglected. Understanding these interactions – if occurring in the environment- will help to improve atmospheric Se models and thus predict drivers of Se deficiency.

Impact of microbial processes on the safety of deep geological repositories for radioactive waste

“…It is a detoxification mechanism for microorganisms since volatile Se methylated compounds are notably less toxic than the oxidized forms ( Davis et al, 2013 ; Favorito et al, 2021 ). The production of methylated selenides has been proved in different bacterial species such as Methylococcus capsulatus , Methylosinus trichosporium OB3b, or Pseudomonas tolaasii ( Eswayah et al, 2017 ; Liu et al, 2021 ). These bacterial strains can produce volatile compounds such as dimethyl selenide (DMSe, CH 3 SeCH 3 ), dimethyl diselenide (DMDSe, CH 3 SeSeCH 3 ), and dimethyl selenenyl sulfide (DMSeS, CH 3 SeSCH 3 ).…”

“…Pseudomonas tolaasii (Eswayah et al, 2017;Liu et al, 2021). These bacterial strains can produce volatile compounds such as dimethyl selenide (DMSe, CH 3 SeCH 3 ), dimethyl diselenide (DMDSe, CH 3 SeSeCH 3 ), and dimethyl selenenyl sulfide (DMSeS, CH 3 SeSCH 3 ).…”

Evaluation of Selenomethionine Entrapped in Nanoparticles for Oral Supplementation Using In Vitro, Ex Vivo and In Vivo Models

“…There are few data on the intestinal absorption of SeMet in human-related models. SeMet can also undergo methylation from enzymes, such as γ-lyase, resulting in excretion and bypassing selenoprotein incorporation [ 15 , 16 ]. Little is also known about the effects of the brush-border enzymes and the effects of the pH environment within the epithelia of the small intestine in SeMet metabolism.…”