Arsenobetaine: an ecophysiologically important organoarsenical confers cytoprotection against osmotic stress and growth temperature extremes

Abstract

Summary Arsenic, a highly cytotoxic and cancerogenic metalloid, is brought into the biosphere through geochemical sources and anthropogenic activities. A global biogeochemical arsenic biotransformation cycle exists in which inorganic arsenic species are transformed into organoarsenicals, which are subsequently mineralized again into inorganic arsenic compounds. Microorganisms contribute to this biotransformation process greatly and one of the organoarsenicals synthesized and degraded in this cycle is arsenobetaine. Its nitrogen‐containing homologue glycine betaine is probably the most frequently used compatible solute on Earth. Arsenobetaine is found in marine and terrestrial habitats and even in deep‐sea hydrothermal vent ecosystems. Despite its ubiquitous occurrence, the biological function of arsenobetaine has not been comprehensively addressed. Using Bacillus subtilis as a well‐understood platform for the study of microbial osmostress adjustment systems, we ascribe here to arsenobetaine both a protective function against high osmolarity and a cytoprotective role against extremes in low and high growth temperatures. We define a biosynthetic route for arsenobetaine from the precursor arsenocholine that relies on enzymes and genetic regulatory circuits for glycine betaine formation from choline, identify the uptake systems for arsenobetaine and arsenocholine, and describe crystal structures of ligand‐binding proteins from the OpuA and OpuB ABC transporters complexed with either arsenobetaine or arsenocholine.

Arsenic and high affinity phosphate uptake gene distribution in shallow submarine hydrothermal sediments

“…This has resulted in the spread of As resistance mechanisms in the simplest to the most complex organisms inhabiting both oxic and anoxic habitats exposed to As(V) and As(III). Organic forms of As mostly found in highly productive waters, are believed to decrease and enhance toxicity at various instances (Wilkin et al 2003; Hoffmann et al 2018; Chen et al 2017), but are also thought to be quantitatively negligible relative to As(III) and As(V) enrichment in the natural environment (Smedley and Kinniburgh 2002). …”

Transcriptional response of the obligate anaerobe Desulfuribacillus stibiiarsenatis MLFW‐2T to growth on antimonate and other terminal electron acceptors

“…Growth on As(V), in relation to Sb(V), was associated with highly elevated transcription of the opuAB and gbuC genes involved in the uptake of tertiary amines, such as glycine betaine and choline, that typically serve as osmoand thermo-protectants (Caldas et al, 1999;Sleator and Hill, 2002). Recent literature has shown that arsenobetaine, the organoarsenical analog of glycine betaine, can be transported into the cell by the same systems as other tertiary amines (Hoffmann et al, 2018). Although the exact reason these transporters might be upregulated is unclear, it appears that tertiary amines play an important role in the response of MLFW-2 T to toxic As.…”

The Arsenic Methylation Cycle: How Microbial Communities Adapted Methylarsenicals for Use as Weapons in the Continuing War for Dominance

“…For example, methylated organoarsenicals play a significant role in controlling host bacterial populations and dominance in complex environments. Both AB and the similar nitrogen−containing compound glycine betaine protect against osmotic stress and a wide variety of temperature extreme environments (Hoffmann et al, 2018). Natural methylated organoarsenicals have already been produced biologically for billion years, however, the major species of arsenic in the environment are inorganic, which implies that most of the methylated species are degraded biologically or abiotically into inorganic arsenic.…”