Arsenic and phosphorus biogeochemistry in the ocean: Arsenic species as proxies for P‐limitation

Abstract

Arsenic and phosphorus are biochemically very similar, and hence arsenate (As 5+ ) is toxic by interfering with the energy metabolism, in particular during P limitation. However, many phytoplankton detoxify As by reducing arsenate to arsenite (As 3+ ), and/or methylating it to mono and dimethyl As. Such As detoxification becomes operative in oligotrophic waters when phosphate concentrations are below those for As; therefore, we evaluated the potential use of these detoxification products as indicators of P limitation by measuring As speciation during the US GEOTRACES North Atlantic transect. The distribution of As 3+ concentrations in surface waters is similar to that of N : P ratios and alkaline phosphatase activity (APA), two conventional proxies for P-limitation. As 3+ concentrations have a very similar relationship to phosphate as APA to phosphate, and therefore indicate the potential of As 3+ as proxy for P-limitation. From the relationship to phosphate we derived threshold values of As 3+ concentration to indicate moderate and extreme P-limitation. We then applied these threshold values to assess P-limitation with high horizontal resolution in the North Atlantic, improving on the contradictory assessments using the conventional proxies. Our new evaluation is consistent with the general concept that the North Atlantic is moderately to extremely limited in phosphate.Arsenic and phosphorus are biochemically very similar, so that phytoplanktonic uptake of arsenate (As 5+ ) induces toxic effects due to its substitution in the adenotriphosphate (ATP) cycle, effectively decoupling the energy metabolism (Lehninger 1975). Many phytoplankton species evolved different strategies to ameliorate the toxic effects of As 5+ , including reduction to arsenite (As 3+ ) and methylation to monomethyl-(MMAs) and dimethylarsenic (DMAs). These detoxification products are less harmful and easier to excrete (Andreae and Klumpp 1979;Sanders and Riedel 1993;Hellweger et al. 2003). Hellweger et al. (2003) proposed a mechanistic model with a limited methylation capacity due to slower kinetics compared with the preceding reduction. Such capacity may be exceeded during luxury P uptake because the chances of taking up As 5+ increase with higher rates of P uptake. Hellweger et al. (2003) proposed that exceeding methylation capacity leads to the excretion of the reduced As 3+ . Surface waters of oligotrophic central gyres have particularly high As : P ratios, with As 5+ concentrations in a range of 10-15 nmol L 21 (Cutter et al. 2001;Cutter and Cutter 2006), while phosphate is typically within a range of 0.2-10 nmol L 21 (Wu et al.

Alkaline phosphatase activity in the subtropical ocean: insights from nutrient, dust and trace metal addition experiments

“…The drawdown of DOP is suggested by the lower DOP concentration and higher APA activity in the phosphate-deplete subtropical North Atlantic compared to the phosphate-replete subtropical South Atlantic where DOP concentrations are elevated and APA almost immeasurable (Mather et al, 2008). There is also a zonal contrast, with higher APA in the western subtropical Atlantic than the eastern subtropical Atlantic Wurl et al, 2013;Reynolds et al, 2014), suggesting that phosphate limitation is more prevalent in the western subtropical Atlantic. These northsouth and east-west basin scale contrasts in phosphorus dynamics are partially constrained by the spatial extent of wet and dry dust deposition (Moore et al, 2006;Schlosser et al, 2014) and hence magnitude and distribution of nitrogen fixation, as well as physical transfer of nutrients via nutrient streams (Williams et al, 2011).…”

“…However, when phosphate is in short supply, many marine organisms, including the marine filamentous diazotroph, Trichodesmium (Sohm et al, 2008;Orcutt et al, 2013), cyanobacteria such as Synechococcus (Tetu et al, 2009) and Prochlorococcus (Kathuria and Martiny, 2011), some species of dinoflagellate (Dyhrman and Palenik, 1999;Lin et al, 2012), coccolithophores (Jakuba et al, 2008), diatoms (Dyhrman and Ruttenberg, 2006) and bacteria (Huang and Hong, 1999) are known to synthesize hydrolytic enzymes in order to access the DOP pool. Since the late 1980s, studies on phosphohydrolytic enzymes have largely focused on the activity of alkaline phosphatase (AP; Sebastián et al, 2004a,b;Sohm and Capone, 2006;Mather et al, 2008;Sohm et al, 2008;Duhamel et al, 2010Duhamel et al, , 2011Lomas et al, 2010;Orchard et al, 2010;Suzumura et al, 2012;McLaughlin et al, 2013;Lin et al, 2013;Sato et al, 2013;Wurl et al, 2013;Martin et al, 2014;Reynolds et al, 2014), a group of metalloenzymes that hydrolyse phosphomonoester bonds (Cembella et al, 1984a,b;Hoppe, 2003). As phosphate esters account for up to 70% of the DOP pool (Karl and Yanagi, 1997;Kolowith et al, 2001;Karl and Björkman, 2002), AP plays a significant role in the cycling and metabolism of phosphorus in the ocean.…”

Genomic potential for arsenic efflux and methylation varies among global Prochlorococcus populations

“…Along an open ocean transect that covered varying phosphate regimes, when the PO 4 :AsO 4 ratio was less than 1, the total arsenic pool consisted of a greater proportion of reduced and methylated arsenicals compared with the relatively phosphate-rich region, with an inorganic PO 4 :AsO 4 ratio of 100:1 (Cutter and Cutter, 2006). In the North Atlantic, both methylated arsenicals and arsenite detoxification products have been identified and the spatial distribution of arsenite closely corresponded with phosphate availability and can be used in conjunction with measures of alkaline phosphatase to identify regions of phosphorus limitation (Wurl et al, 2013). There is also evidence that the diazotrophic cyanobacterial communities in these phosphate-poor regions are responding to arsenic toxicity.…”

“…In the marine environment, inorganic arsenate accounts for about 85% of the standing pool of arsenic with the remaining portion of the arsenic pool comprised of the inorganic arsenite and various organoarsenicals, including two of the main products of the methylation pathway, monomethylarsonic acid and dimethylarsinic acid (Andreae, 1979;Cutter et al, 2001;Cutter and Cutter, 2006;Wurl et al, 2013). Arsenate has a nutrient-like depth distribution because it is a bioactive molecule which is transformed by marine biota in the surface waters via the two pathways described above (Andreae, 1979).…”

“…to available phosphate (Karl and Tien, 1997;Wurl et al, 2013). While inorganic arsenic concentrations are relatively stable throughout the surface waters of the open ocean ranging from 12.9-15.7 nmol l − 1 (Andreae, 1979;Cutter and Cutter, 1998;Cutter et al, 2001;Ellwood and Maher, 2002;Cutter and Cutter, 2006), surface phosphate concentrations are far more variable, ranging fromo0.1 μmol l − 1 in oligotrophic subtropical gyres to 42.0 μmol l − 1 in the Southern Ocean (Karl, 2007).…”