Abstract
The toxic arsenate ion can behave as a phosphate analog, and this can result in arsenate toxicity especially in areas with elevated arsenate to phosphate ratios like the surface waters of the ocean gyres. In these systems, cellular arsenate resistance strategies would allow phytoplankton to ameliorate the effects of arsenate transport into the cell. Despite the potential coupling between arsenate and phosphate cycling in oligotrophic marine waters, relatively little is known about arsenate resistance in the nitrogen-fixing marine cyanobacteria that are key components of the microbial community in low nutrient systems. The unicellular diazotroph, Crocosphaera watsonii WH8501, was able to grow at reduced rates with arsenate additions up to 30 nM, and estimated arsenate to phosphate ratios of 6:1. The genome of strain WH8501 contains homologs for arsA, arsH, arsB, and arsC, allowing for the reduction of arsenate to arsenite and the pumping of arsenite out of the cell. The short-term addition of arsenate to the growth medium had no effect on nitrogen fixation. However, arsenate addition did result in the up-regulation of the arsB gene with increasing arsenate concentrations, indicating the induction of the arsenate detoxification response. The arsB gene was also up-regulated by phosphorus stress in concert with a gene encoding the high-affinity phosphate binding protein pstS. Both genes were down-regulated when phosphate was re-fed to phosphorus-stressed cells. A field survey of surface water from the low phosphate western North Atlantic detected expression of C. watsonii arsB, suggestive of the potential importance of arsenate resistance strategies in this and perhaps other systems.
Highlights
Arsenic is prevalent in the marine environment, where it can occur as arsenite [As (III)] and arsenate [As (V)]
Both oxidation forms are toxic to the majority of living organisms, with arsenite interfering with enzyme function, and arsenate, the thermodynamically dominant form in most oxygenated surface waters, behaving as a phosphate analog (Apte et al, 1986) and disrupting phosphate uptake and utilization (Wängberg and Blanck, 1990; Bleeker et al, 2003)
Due to the potential competitive inhibition between arsenate and phosphate (Smedley and Kinniburgh, 2002; Manomita et al, 2004), arsenate resistance, or detoxification pathways may be important in low phosphate systems like the ocean gyres, including the western North Atlantic where surface phosphate levels are typically around 5 nM and can be sub-nanomolar (Wu et al, 2000; Lomas et al, 2010)
Summary
Arsenic is prevalent in the marine environment, where it can occur as arsenite [As (III)] and arsenate [As (V)]. The microbial detoxification products of arsenic including arsenite and methylated forms of arsenic have surface maxima, and in a study of profiles in the western Atlantic tracked closely with the chlorophylla profile (Cutter and Cutter, 1995). These detoxification products have a short (days–months) residence time and their presence suggests active microbial arsenic detoxification in the surface ocean. Some arsenic accumulation can occur in microbes (Statham et al, 1987), arsenic distributions suggest that the uptake of arsenic by phytoplankton primarily results in cycling between chemical forms within the euphotic zone and that the flux of arsenic into the deep ocean by particle transport is relatively minor (Andreae, 1979; Sanders and Windom, 1980)
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