Aquaglyceroporin AqpS from Sinorhizobium meliloti conducts both trivalent and pentavalent methylarsenicals

Chemosphere. 2021 May:270:129379. doi: 10.1016/j.chemosphere.2020.129379. Epub 2020 Dec 27.

Abstract

Arsenic is a toxic metalloid that enters cells adventitiously via uptake systems for phosphate transporters, aquaglyceroporins (AQPs) or sugar permeases. However, transport of highly toxic methylarsenite (MAs(III)) and relatively nontoxic methylarsenate (MAs(V)) by bacterial AQPs has not been characterized. MAs(V) has a history of use as an herbicide. Here we used whole genome sequence analysis of AQPs in arsenic resistance (ars) operons. The aqp genes are frequently located next to MAs(III) resistance genes such as arsH, which suggests that they could be involved in MAs(III) uptake. Bacterial AQPs encoded by ars operons can be classified into two subgroups. One subgroup includes AqpS from the plant symbiont Sinorhizobium meliloti 1021. Our data suggests that AqpS has a substrate selectivity filter different from that of other bacterial AQPs. Both Escherichia coli GlpF and AqpS conduct MAs(III) efficiently, but GlpF conducts the MAs(V) anion poorly, so E. coli takes up MAs(V) inefficiently. In contrast, AqpS conducts MAs(V) under physiological conditions. A homology model of AqpS indicates that it has a substrate channel with a selectivity filter containing the nonpolar residue Val177 instead of the charged arginine residue found in other AQPs. While the selectivity filter in most AQPs prevents movement of anions, Val177 is predicted to allow movement of the MAs(V) anion through the channel. We propose that AqpS is a component of an MAs(III) resistance pathway in which MAs(III) enters cells of S. meliloti via AqpS, is oxidized by ArsH to MAs(V), which exits the cells via AqpS.

Keywords: AqpS; Aquaglyceroporin; Aquaporin; Methylarsenical herbicide; Methylated arsenicals.

MeSH terms

  • Aquaglyceroporins*
  • Aquaporins*
  • Arsenicals* / metabolism
  • Escherichia coli / genetics
  • Escherichia coli / metabolism
  • Escherichia coli Proteins*
  • Operon
  • Sinorhizobium meliloti* / genetics
  • Sinorhizobium meliloti* / metabolism

Substances

  • Aquaglyceroporins
  • Aquaporins
  • Arsenicals
  • Escherichia coli Proteins
  • GlpF protein, E coli