Arsenobetaine in Seawater: Depth Profiles from Selected Sites in the

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Arsenobetaine in seawater: Depth profiles from selected sites in the North Atlantic Ronald Alexander Glabonjat, Georg Raber, Benjamin A. S. Van Mooy, and Kevin A. Francesconi Environ. Sci. Technol., Just Accepted Manuscript • DOI: 10.1021/acs.est.7b03939 • Publication Date (Web): 12 Dec 2017 Downloaded from http://pubs.acs.org on December 12, 2017

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Environmental Science & Technology

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Arsenobetaine in seawater: Depth profiles from

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selected sites in the North Atlantic

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AUTHOR NAMES

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Ronald A. Glabonjat1, Georg Raber1, Benjamin A. S. Van Mooy2, Kevin A. Francesconi1*

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AUTHOR ADDRESS

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1

University of Graz, NAWI-Graz, Institute of Chemistry, 8010 Graz, Austria

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2

Woods Hole Oceanographic Institution, Department of Marine Chemistry and Geochemistry,

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Woods Hole, MA 02543, USA

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KEYWORDS

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Arsenobetaine – Organic Arsenic – Seawater – Atlantic Ocean – HPLC-ICPMS/ESMS.

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ACS Paragon Plus Environment

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ABSTRACT

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Arsenic occurs in marine waters, typically at concentrations of 1-2 μg As kg-1, primarily as the

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inorganic species arsenate. Marine animals, however, contain extremely high levels of arsenic

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(typically 2,000-20,000 μg As kg-1 wet mass), most of which is present as arsenobetaine, an

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organic form of arsenic that has never been found in seawater. We report a method based on ion-

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exchange pre-concentration and HPLC/mass spectrometry to measure arsenobetaine in seawater,

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and apply the method to samples of seawater collected at various depths from seven sites in the

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North Atlantic. Arsenobetaine was detected in most samples at levels ranging from 0.5 to 10 ng

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As kg-1, and was found at depths down to 4900 m. Furthermore, we report the presence of 15

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additional organoarsenicals in seawater, 14 of which had never been detected in marine waters.

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The arsenobetaine depth profile was related, albeit weakly, to that of chlorophyll; this

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relationship probably reflects arsenobetaine’s release to water from marine animals associated

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with the euphotic zone rather than its direct biosynthesis by primary producers. Future

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application of the new method for seawater analysis will shed new light on the biogeochemical

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cycle of marine arsenic.


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INTRODUCTION

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Seawater contains arsenic mainly as inorganic arsenic in the low μg kg-1 range.1-6 Marine algae

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can bio-transform inorganic arsenic into a wide range of compounds including simple methylated

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arsenic acids7, arsenosugars8,9 and arsenolipids10-12. These algal organoarsenic compounds

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appear to be further transformed in marine animals by currently unknown processes to

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arsenobetaine (AB; (CH3)3As+CH2COO-), a simple cationic compound that is by far the

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predominant arsenic species in fish, crustaceans and mollusks, where concentrations can be as

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high as 30,000 µg kg-1.13 Despite AB’s predominance in marine animals, and its likely release to

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seawater following death of the organisms, AB has never been detected in seawater.

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A possible reason for this conundrum is that AB is fundamentally incompatible with

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commonly used analytical methods for determining arsenicals in seawater, all of which

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incorporate a hydride generation step whereby the two inorganic arsenic species, arsenate and

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arsenite, and the simple methylated arsenicals can be selectively measured.1-6 In a classic

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oceanographic study,2 Andreae used hydride generation together with cryo-trapping, and

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subsequently determined the volatile arsines by atomic absorption spectrometry to provide the

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first seawater depth profiles of arsenite, arsenate, methylarsonate (MA), and dimethylarsinate

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(DMA). That same study showed that the methylated species were associated mainly with the

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euphotic zone where they occurred at ca 8-18 % of the total arsenic in the seawater. Hydride

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generation techniques were also used in subsequent studies on seawater arsenic species, which

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confirmed and extended the earlier results.5,6,14-18 In all such studies, the seawater arsenic species

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were chemically transformed into volatile analytes, which were then cleanly separated from the

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complex and troublesome salt matrix before being measured. AB, however, cannot be directly

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converted to a volatile arsenic species, and hence remains undetectable with hydride generation


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methods. This analytical limitation similarly applies to many other organoarsenicals naturally

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occurring in marine biota.

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Although the hydride-active arsenic species represent the majority of seawater arsenic, our

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understanding of arsenic cycling in the sea would benefit from knowledge of all the arsenic

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compounds involved. To reach this goal, we developed an analytical method capable of

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measuring trace amounts of non-hydride active arsenicals in seawater by incorporating an ion-

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exchange step to simultaneously remove the inorganic cations and anions (mainly Na+ and Cl-

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ions) while concentrating AB and other cationic arsenicals prior to their determination by

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HPLC/mass spectrometry. Furthermore, we applied the method to seawater collected from

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various depths from seven sites in the North Atlantic reflecting high and low nutrient areas.

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Considering the abundance of AB in marine biota, we hypothesize that AB will be present in

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seawater, that its concentrations will be related to planktonic activity in the water column, and,

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given AB’s high chemical stability, that its presence might extend to deeper waters beyond the

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euphotic zone.

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MATERIALS AND METHODS

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Sample collection

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Seawater samples were taken as part of the cruise KN207-01 in the North Atlantic Ocean

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between Woods Hole and Bermuda (21 April to 05 May 2012). Two main maritime regions,

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separated by the Gulf Stream, were covered (Figure 1). The first region, northwest of the Gulf

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Stream, was located in the Labrador Current and is characterized by higher nutrient (HN) levels,

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resulting in high primary production,19 while the second region, southeast of the Gulf Stream

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features lower levels of nutrients (LN) and, therefore, lower primary production. Seawater


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samples were collected at depths between 2 and 4900 m in 10 L Niskin bottles with a 24-position

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CTD rosette (CTD SBE 911plus, Sea-Bird Electronics, Washington, USA). Further parameters

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(depth, salinity, temperature, fluorescence) were also simultaneously recorded at each sampling

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point. For each sample, a portion of seawater (ca 0.4 L) was transferred to a polyethylene bottle

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(0.5 L, acid washed) and immediately filtered through a glass microfiber filter (GF/F, 47 mm

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diameter, 0.7 µm pore size). The last ca 250 mL of the filtrate was retained, and transported

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frozen in a polyethylene bottle to Graz where it was stored at -80 °C until analysis.

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84 85

Figure 1. The cruise route had the Gulf Stream as a dominating oceanographic feature separating

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a region high in nutrients (HN1-HN3) from an area showing much lower nutrient levels (LN1-

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LN4) and therefore also lower primary production (Table S1).

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Chemicals and standards

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Water (18.2 MΩ cm) was obtained from a Milli-Q system (Millipore GmbH, Vienna, Austria).

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Aqueous ammonia (NH3, ≥ 25 % p.a.), nitric acid (HNO3, ≥ 65 % p.a.), hydrochloric acid (HCl,


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≥ 37 % p.a.), formic acid (≥ 98 % p.a.), and ammonium formate (≥ 95 % p.a.) were purchased

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from Carl Roth (Karlsruhe, Germany), pyridine (≥ 99 % p.a.) from Sigma-Aldrich (Vienna,

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Austria), methanol (MeOH, ≥ 99.9 % p.a.) from VWR (Vienna, Austria), and sodium chloride

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(NaCl, ≥ 99.99 % p.a.) from Merck (Darmstadt, Germany). Analytical standards of the following

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eight arsenic compounds were available in house: arsenobetaine (AB, as the bromide salt),

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arsenocholine

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dimethylarsinoylbutanoic

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dimethylarsinoylethanol (DMAE), trimethylarsoniopropionic acid (TMAP, as the bromide salt),

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tetramethylarsonium ion (TETRA, as the bromide salt), and trimethylarsine oxide (TMAO).

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Arsenate (As (V), as NaH2AsO4·7 H2O) and dimethylarsinate (DMA, as the sodium salt) were

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obtained from Sigma-Aldrich. The structures of the main arsenicals discussed in this work are

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shown in Figure 2; reference HPLC-ICPMS chromatograms of selected individual standards are

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shown in Figure S6.

(AC,

as

the acid

bromide (DMAB),

salt),

dimethylarsinoylacetic

dimethylarsinoylpropionic

acid

(DMAA),

acid

(DMAP),

105

106 107

Figure 2. Arsenic species referred to in this work, drawn in their protonated forms.

108 109


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Sample preparation

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Immediately before the sample preparation steps, the frozen seawater sample was thawed at

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room temperature and filtered through a 0.2 µm filter (25 mm syringe filter, nylon membrane;

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obtained from VWR, Vienna, Austria).

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Direct measurement of total arsenic and anionic arsenicals in seawater

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A small portion (0.5 mL) of the 0.2 µm filtered seawater was diluted (1+9, v/v) with HPLC

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mobile phase (see below), and this solution was analyzed for anionic As species (mainly

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arsenate) by using anion-exchange HPLC coupled to an inductively coupled plasma mass

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spectrometer (HPLC-ICPMS); and for total As content by using flow injection ICPMS in

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collision cell mode (He, 5 mL min-1) to minimize polyatomic interferences. As validation of the

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total arsenic measurements, we tested certified reference materials CASS-5 (Nearshore seawater

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reference material for trace metals) and NASS-6 (Seawater reference material for trace metals),

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both from the National Research Council Canada (Ottawa, Canada). For CASS-5, we obtained a

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total arsenic concentration of 1.19 ± 0.03 µg As kg-1, n = 3 (certified at 1.21 ± 0.09 µg As kg-1),

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and for NASS-6 we recorded 1.45 ± 0.05 µg As kg-1, n = 3 (certified at 1.40 ± 0.12 µg As kg-1).

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We also performed anion exchange HPLC-ICPMS on NASS-6 (see below).

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Sample clean-up: removal of salt and concentrating the cationic arsenicals.

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Cationic arsenic species were pre-concentrated from the seawater samples by using a strong

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cation-exchange resin to trap the arsenicals and subsequently washing them from the resin with

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an aqueous ammonia solution. The resin (20 mL DOWEX® 50WX8; H+ form, 100-200 mesh,

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Sigma-Aldrich, Vienna, Austria) was packed into a modified polystyrene pipette (50 mL,


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300 x 18 mm; Fisher Scientific, Schwerte, Germany). Next, the resin was equilibrated by

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washing successively with water (50 mL), 1 M aqueous NH3 (100 mL), water (30 mL), 6 M

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HNO3 (50 mL), and again water (ca 30 mL) until the effluent was neutral. A portion of seawater

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(40 g of the 0.2 µm filtered seawater) was applied to the column after which the resin was

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washed with additional water (40 mL) until the effluent was neutral. A 1 M aqueous ammonia

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solution was then passed through the column and 10 mL fractions were collected in polyethylene

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tubes; the ‘alkaline front’, the point at which the effluent becomes basic, was combined with the

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preceding fraction and the two following fractions. Excess ammonia was evaporated from this

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combined fraction in an oven (50 °C, 1 h), and then the solution was taken to complete dryness

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in a centrifugal lyophiliser (RVC 2-33 CD plus, Martin Christ, Osterode am Hartz, Germany).

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The dry residues were stored frozen (-20 °C); later, they were re-dissolved in water (500 µL) and

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measured by HPLC/mass spectrometry. After each seawater sample, the Dowex 50 resin was

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regenerated by washing with water (30 mL), then 6 M HNO3 (50 mL), and again with water

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(30 mL) before applying the next sample. During periods of non-use, resin was removed from

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the columns, and stored in aqueous 1 % HNO3. Samples were prepared in triplicate, and the

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triplicates were processed in parallel together with a saltwater blank (40 g of water containing

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35 g kg-1 of NaCl) by using four identical resin columns (i.e. a blank was processed with each

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sample’s set of three replicates). Over the course of the analyses, 55 blanks were analyzed, which

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showed no detectable amounts of organoarsenic species (LOD 0.2 ng As kg-1 based on blank +

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3 standard deviations of the blank) except for DMA (LOD 2 ng As kg-1) and TMAO

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(0.5 ng As kg-1); the blank value was subtracted from each sample set measured. In comparison

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with the concentrations found in the seawater samples, the concentrations of DMA in the

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saltwater blanks were always negligible, and those of TMAO were usually negligible (see


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below). We also analyzed reference seawater NASS-6 (40 mL) where we detected two cationic

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arsenicals namely DMA and TMAO with concentrations of 236 ± 31 ng As kg-1 and 45 ± 3 ng

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As kg-1, respectively (n = 3); there was, however, no evidence for the presence of arsenobetaine

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or any other organoarsenical in the processed NASS-6 reference seawater. Recovery of AB

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during the sample preparation procedure was assessed by spiking AB at a level of 10 ng As kg-1

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to a saltwater blank and to natural seawater, and found to be 91 ± 13 % (n = 3) and 96 ± 10 %

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(n = 3), respectively.

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Determination of arsenic species by HPLC-ICPMS and HPLC-HR-ESMS

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Separation of anionic arsenic species for ICPMS detection was performed with an Agilent

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1100 series HPLC (Agilent Technologies, Waldbronn, Germany) on a PRP-X100 column (150 x

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4.6 mm, 5 µm, Hamilton, Reno, USA), using malonate buffer (5 mM, adjusted with aqueous

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NH3 to pH 5.6) at a flow rate of 1.0 mL min-1, at 30 °C, and an injection volume of 25 µL.

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HPLC-ICPMS of arsenic cations was carried out with an IonoSpher 5C column (200 x 3.0 mm, 5

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µm, Varian Inc., Mulgrave, Australia), using pyridine buffer (10 mM, adjusted with formic acid

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to pH 2.6) at a flow rate of 1.0 mL min-1; temperature was 30 °C, and the injection volume was

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50 µL. HPLC separation of arsenic cations for detection by electrospray-high resolution mass

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spectrometry was performed on a Dionex Ultimate 3000 series instrument (Thermo Fisher

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Scientific, Erlangen, Germany) equipped with a IonoSpher 5C column (100 x 3.0 mm, 5 µm,

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Varian), using ammonium formate buffer (20 mM, adjusted with formic acid to pH 2.6,

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containing 3 % methanol) as mobile phase at a flow rate of 1.0 mL min-1; temperature was set to

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30 °C, and 10 µL sample were injected. For detection by electrospray mass spectrometry


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(ESMS), we substituted formate buffer for pyridine in the HPLC mobile phase because it was

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more compatible with the electrospray ionization process.

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Quantification of arsenic species by ICPMS was performed with an Agilent 7900 series

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instrument observing m/z 75 (75As) and 77 (40Ar37Cl for assessing possible interferences on m/z

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75 from

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arsenic signals was achieved by introducing 11 % of argon containing 1 % CO2 as optional gas

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directly into the plasma.

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Ar35Cl) at integration times of 0.3 s and 0.1 s, respectively. Signal enhancement for

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High resolution ESMS was carried out on a Q-Exactive Hybrid Quadrupole-Orbitrap MS

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(Thermo Fisher Scientific). Masses were recorded under positive electrospray ionization

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conditions (capillary voltage was 3.5 kV; capillary temperature 250 °C; sheath gas flow rate 65

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instrument units; auxiliary gas flow rate and temperature were 20 instrument units and 450 °C,

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respectively) in SCAN mode with a resolution of 35,000 (FWHM) in a range of m/z 100-300.

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Determination of nutrients and chlorophyll-a in seawater

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A portion of each seawater sample collected in Niskin bottles, was pre-filtered (0.2 µm) into an

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acid-washed bottle and frozen (-20 °C) until being analyzed for phosphate, silicate, nitrate,

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nitrite, and ammonia by the Marine Chemistry Laboratory at the University of Washington. The

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analyses were performed on a colorimetric auto analyzer (Technicon AAII; SEAL Analytical

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Inc., Wisconsin, USA) following the protocols of the World Ocean Circulation Experiment

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(WOCE) hydrographic program. Fluorescence was separately determined in situ in unfiltered

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waters using an environmental characterization optics device (ex/em: 470/695 nm; ECO

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AFL/FL, Wet Labs, Philomath, USA) as an indicator of active phytoplankton biomass and

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chlorophyll-a concentration in the water column. The LOD for chlorophyll-a was 0.05 mg m-3.


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RESULTS AND DISCUSSION

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Total arsenic and arsenate

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Total As concentrations in the seawater samples were found to be very consistent at

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1.34 ± 0.14 µg As kg-1 throughout the measured sites and depths (2-200 m; 16 samples; Table

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S2) regardless of their low or high nutrient status. Anion-exchange HPLC-ICPMS showed that

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arsenate was the dominant arsenic species at all those sampling points accounting for 90 ± 6 %

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(n = 16) of total As (Figure S1 and Table S2). The remaining arsenic visible in the anionic

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HPLC-ICPMS chromatogram comes at or near the void volume and suffers from matrix

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interference: it likely represents mostly arsenite (which is a neutral species at the mobile phase

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pH 5.6), in addition to DMA (which is poorly retained by the anion-exchange column under the

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used conditions) and the combined sum of any cationic arsenicals in the samples.

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Methylarsonate, which is often found in seawater, albeit usually at trace amounts, was not

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apparent in the chromatograms of our samples (RT ca 2.2 min; LOD ca 0.05 µg As kg-1).

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There are no certified values for arsenic species in the reference seawater NASS-6. Our anion

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HPLC-ICPMS measurements (n = 3) showed that it contained arsenate at a concentration of

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1.05 ± 0.07 µg As kg-1, and that 0.37 ± 0.04 µg As kg-1 was present as void volume arsenic.

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These values are consistent with the total arsenic value of 1.45 ± 0.05 µg As kg-1 that we

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recorded for NASS-6 (the certified value is 1.40 ± 0.12 µg As kg-1). We note also that our values

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are consistent with the values of 1.13 ± 0.04 µg As kg-1 and 0.24 ± 0.03 µg As kg-1 for arsenate

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and arsenite, respectively, reported by Wang and Tyson20 using a hydride generation method.

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Determination of arsenobetaine in seawater – analytical considerations

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Our first analytical challenge was to achieve the very low detection limits required to measure

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AB, an arsenic species that is not hydride-active, in seawater. Because all previous studies had

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indicated that essentially all seawater arsenic was present as inorganic and simple methylated

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species, we expected to find, at most, only trace amounts of AB equivalent to perhaps 1 % or less

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of the total As (ca 0.01 µg As kg-1). The second analytical challenge was to separate the analyte

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from the heavy salt matrix. To effect this separation we investigated the use of a strong cation-

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exchange resin (Dowex 50) in a sample preparation step. AB, along with other weakly cationic

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species, is retained by the Dowex 50 resin in the H+ form, and can then be quantitatively released

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from the resin by elution with aqueous ammonia solution.21 Our preliminary tests showed that, as

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expected, Na+ and other metal ions in seawater were also retained by Dowex 50, but these ions

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were not displaced from the resin by aqueous ammonia. The chloride and other seawater anions

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had no interaction with the Dowex resin and passed straight through the column in the water

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wash, prior to the aqueous ammonia step.

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The efficiency of the separation was tested by adding AB, at a level of 0.01 µg As kg-1,

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initially to 40 g of water containing NaCl at 35 g kg-1, and then to 40 g of natural seawater

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containing 35 g kg-1 of total dissolved solids. The overall mean recovery of AB was > 90 %

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(total n = 6; there was no difference between the two matrices) and only a trace (< 0.5 %) of the

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total dissolved solids remained in the AB fraction. When the residue containing AB was re-

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dissolved in 500 µL of water, we obtained a solution with ca 0.8 µg As kg-1 (as AB), which was

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easily measured by HPLC-ICPMS and by HPLC-ESMS under cation-exchange conditions.

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Further concentration of the sample is possible, but would result in increased handling


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difficulties because of the smaller volumes as well as enhanced matrix effects, particularly for

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ESMS measurements.

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The sample preparation step with Dowex 50 is effective not only for AB but for all weakly

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cationic species, including DMA because it readily protonates (giving Me2As+(OH)2) in the

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presence of H+ ions released from the resin by exchange with the seawater cations. Having

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developed an analytical method capable of measuring our target analyte AB at the low ng kg-1

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level, we then set about testing our hypothesis that AB was present in seawater and that it was

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associated with planktonic activity in oceanic waters.

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Distribution of arsenobetaine and other organoarsenic species in seawater

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Application of the method to seawater samples collected from the North Atlantic revealed the

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presence of AB, albeit at trace levels, in most samples. Although there has been one tenuous

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report22 of AB in an estuarine water sample, this work is the first report of AB in natural

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seawater.

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In addition to AB, we also observed DMA and, unexpectedly, a further 14 cationic arsenic

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species. Of these 16 organoarsenic species, seven are known to occur in marine organisms: AB,

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DMA, DMAA, DMAP, DMAB, DMAE, and TMAO (see Figure 2). These compounds were

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identified by HPLC-ICPMS matching with standard compounds (Figure 3) and by HPLC-HR-

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ESMS with accurate mass determinations (Figure 4). Because the method employed ICPMS as

263

the arsenic-selective detector, we were able to detect traces of nine additional cationic

264

organoarsenic species, even though their identities remain unknown. We note that

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trimethylarsoniopropionate (TMAP), for which we had an authentic standard, did not match the

266

properties of any of the unknowns (Figure S6). Based on the organoarsenicals known to occur in


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marine organisms, two other species namely arsenocholine and tetramethylarsonium ion, might

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also be expected to be present in seawater; these species, however, are not detectable by our

269

method because, being strong permanent cations, they bind strongly to the Dowex 50 resin and

270

cannot be washed off with aqueous ammonia. Arsenosugars are also not measurable by this

271

method because they are not stable under the acidic conditions generated on the Dowex column.8

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Figure 3. Cation-exchange HPLC-ICPMS chromatograms as examples of two processed

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seawater samples (site HN3, 11 m depth; and site LN1, 502 m depth). Note that the dominant

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DMA peak is truncated to show the peaks of the less abundant arsenic species. AB is clearly

277

separated from other arsenic species; DMAA and DMAP (see Figure 2) co-eluted just after

278

DMA and were therefore quantified together and with an estimated combined contribution of

279

< 3 % to the DMA signal, while the broad peak at RT 8.5 min contained both DMAE and

280

DMAB; these unresolved arsenic signals could be easily seen as individual compounds by

281

HPLC-ESMS (Figure 4). The front (void volume) peak contains residual trace chloride (detected

282

as 40Ar35Cl), and neutral and anionic arsenicals remaining after sample preparation with Dowex

283

50. The first group of unknowns (U1-3; not quantified) contains at least three weakly retained

284

arsenic species, while at least six more unidentified signals (U4-9) eluted after AB but before

285

TMAO. HPLC conditions were: IonoSpher 5C (200 x 3.0 mm; 5 µm); mobile phase, pyridine

286

(10 mM; pH 2.6); flow rate, 1.0 mL min-1; column temperature, 30 °C; injection volume, 50 µL.

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Figure 4. Cation-exchange HPLC-HR-ESMS extracted ion chromatograms of processed

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seawater sample from site HN3, 10 m depth. Specific m/z values for DMA, DMAA, DMAP,

291

AB, DMAE, TMAO, and DMAB extracted (resolution 35,000 FWHM; ∆m for the difference

292

between calculated and measured m/z values was < 0.5 mmu for all seven compounds. The

293

specific m/z values for TETRA and AC were also monitored but no signals were found. HPLC

294

conditions were: IonoSpher 5C (100 x 3.0 mm; 5 µm); mobile phase, ammonium formate

295

(20 mM incl. 3 % MeOH; pH 2.6); flow rate, 1.0 mL min-1; column temperature, 30 °C; injection

296

volume, 10 µL.


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The main focus of our work was to determine AB in seawater, and thus the chromatographic

298

separation was optimized for this arsenic species. When we analyzed our processed samples by

299

HPLC-ICPMS, we were surprised by the multiplicity of arsenic compounds. Although many of

300

them were not chromatographically separated, the subsequent use of electrospray-MS with

301

accurate mass capability as the HPLC detector, ‘mass-separated’ the individual species and

302

provided confirmation of their identity. For example, for co-eluting peaks representing

303

DMAE/DMAB, the presence of both arsenicals was shown by HPLC-HR-ESMS measurements.

304

Similarly, DMAA and DMAP could be clearly identified, even in the presence of a large excess

305

of DMA (Figure 3). We could not, however, obtain quantitative data on the individual

306

compounds in the co-eluting peaks because the quantification was based on (arsenic-selective)

307

HPLC-ICPMS. Accordingly, those peaks were grouped together and quantities are reported as

308

the sum of several peaks, as follows: (i) the unknown arsenicals U1-U3; (ii) DMA, DMAA and

309

DMAP; (iii) the unknowns U5-U9; and (iv) DMAE and DMAB (see Table 1 and Figure 3).

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Table 1. Concentrations of AB and other arsenic cations present in seawater samples from seven

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sites at various depths, determined by cation-exchange HPLC-ICPMS (concentrations of

313

arsenicals in ng As kg-1, mean ± standard deviation of n = 3; chlorophyll-a in mg m-3, n = 1). The

314

LOD is 0.2 ng As kg-1 seawater, except for DMA (2 ng As kg-1). Quantification of peaks U1-3

315

was not performed because they eluted close to the void volume; concentrations of DMA include

316

traces of DMAA and DMAP (estimated at < 3 %). Chlorophyll data adopted from Van Mooy

317

and Rauch.23 The precision, depending on the As species and concentration, was typically

318

10-30 %; we consider this precision level acceptable given the double analytical challenge of

319

trace levels and a complex matrix.

Site

HN1

HN2

HN3

All HN

Depth [m] 6 11 21 29 62 200 5 10 18 27 30 150 5 11 29 50 100 150 200

AB

DMA

TMAO

Sum of DMAE + U4 DMAB

1.0 ± 0.2

57 ± 15

9.6 ± 1.4

0.4 ± 0.2

1.4 ± 0.3

4.5 ± 0.9

1.1

5.5 ± 1.4

174 ± 47

17.8 ± 4.0

3.4 ± 0.7

1.1 ± 0.3

3.8 ± 1.0

1.4

8.6 ± 1.3

248 ± 47

68.7 ± 12.1

1.7 ± 0.5

1.0 ± 0.4

2.8 ± 0.5

1.7

1.6 ± 0.3

68 ± 17

12.7 ± 2.6

0.4 ± 0.2

1.4 ± 0.7

4.6 ± 1.7

1.9

2.2 ± 0.2

59 ± 9

12.2 ± 1.5

< 0.2

0.4 ± 0.2

1.9 ± 0.4

0.1

2.0 ± 0.2

44 ± 1

6.0 ± 0.1

< 0.2

< 0.2

< 0.2

< 0.1

1.5 ± 0.2

77 ± 1

14.3 ± 1.1

1.9 ± 0.1

3.8 ± 0.1

9.9 ± 0.3

1.4

1.3 ± 0.1

77 ± 2

13.2 ± 0.2

2.0 ± 0.2

3.9 ± 0.2

10.0 ± 1.1

1.4

1.4 ± 0.2

82 ± 5

14.7 ± 1.2

2.1 ± 0.2

4.1 ± 0.2

10.1 ± 0.7

1.8

1.1 ± 0.1

68 ± 1

13.0 ± 0.4

1.9 ± 0.2

3.8 ± 0.2

9.2 ± 0.5

2.7

1.5 ± 0.1

42 ± 1

12.9 ± 0.4

1.5 ± 0.1

3.3 ± 0.1

8.2 ± 0.4

1.1

0.8 ± 0.1

21 ± 1

10.3 ± 0.4

0.6 ± 0.1

1.6 ± 0.1

5.1 ± 0.3

< 0.1

0.9 ± 0.1

74 ± 6

11.7 ± 0.5

2.2 ± 0.1

3.2 ± 0.3

7.8 ± 0.3

1.2

0.9 ± 0.1

70 ± 5

11.8 ± 0.4

2.1 ± 0.2

3.4 ± 0.3

8.7 ± 0.2

1.2

0.8 ± 0.1

54 ± 2

9.8 ± 0.4

1.8 ± 0.1

2.5 ± 0.3

6.4 ± 0.2

2.1

0.6 ± 0.1

27 ± 1

9.1 ± 0.3

1.3 ± 0.2

1.7 ± 0.1

4.8 ± 0.1

0.3

0.4 ± 0.2

19 ± 1

7.8 ± 0.1

0.6 ± 0.1

1.0 ± 0.1

4.6 ± 0.2

< 0.1

0.7 ± 0.1

21 ± 1

4.0 ± 0.8

0.4 ± 0.2

0.8 ± 0.1

3.5 ± 0.3

< 0.1

0.6 ± 0.1

33 ± 1

0.5 ± 0.1

< 0.2

< 0.2

1.2 ± 0.1

< 0.1

1.7 ± 2.0

69 ± 55

13.7 ± 13.9

1.3 ± 1.0

2.0 ± 1.4

5.6 ± 3.1

Sum of Chlorophyll U5 - U9

320


18

Page 19 of 33

321


Table 1 (continued).

Site

LN1

LN2

LN3

LN4

All LN LN ≤ 200 m

Depth [m] 12 97 150 502 601 676 800 1253 2000 2500 3000 3178 4002 4250 4900 2 5 10 35 50 70 90 150 200 6 19 64 92 151 6 19 36 66 90 200

AB

DMA

Sum of TMAO DMAE + U4 DMAB

0.6 ± 0.1

36 ± 1

8.9 ± 1.5

0.6 ± 0.1

1.1 ± 0.1

5.7 ± 0.4

0.1

0.7 ± 0.1

30 ± 1

10.8 ± 0.2

0.6 ± 0.1

0.8 ± 0.1

4.6 ± 0.1

0.6

0.6 ± 0.1

28 ± 3

11.5 ± 0.4

0.7 ± 0.1

0.7 ± 0.1

4.4 ± 0.2

0.1

0.4 ± 0.2

13 ± 1

2.4 ± 0.3

< 0.2

< 0.2

0.4 ± 0.2

< 0.1

0.8 ± 0.1

10 ± 1

0.8 ± 0.1

< 0.2

< 0.2

0.4 ± 0.2

< 0.1

0.8 ± 0.1

9±1

0.7 ± 0.2

< 0.2

< 0.2

0.4 ± 0.2

< 0.1

0.4 ± 0.2

7±1

0.5 ± 0.2

< 0.2

< 0.2

0.4 ± 0.2

< 0.1

< 0.2

5±1

0.4 ± 0.2

< 0.2

< 0.2

0.4 ± 0.2

< 0.1

6.9 ± 1.6

12 ± 1

1.0 ± 0.1

< 0.2

< 0.2

0.4 ± 0.2

< 0.1

0.6 ± 0.1

12 ± 2

0.6 ± 0.2

< 0.2

< 0.2

0.4 ± 0.2

< 0.1

1.4 ± 0.1

10 ± 1

0.4 ± 0.2

< 0.2

< 0.2

0.4 ± 0.2

< 0.1

< 0.2

5±1

0.9 ± 0.2

< 0.2

< 0.2

0.4 ± 0.2

< 0.1

< 0.2

8±2

0.4 ± 0.2

< 0.2

< 0.2

0.4 ± 0.2

< 0.1

0.4 ± 0.2

12 ± 1

1.0 ± 0.1

< 0.2

< 0.2

0.4 ± 0.2

< 0.1

0.7 ± 0.1

7±1

0.7 ± 0.1

< 0.2

< 0.2

0.4 ± 0.2

< 0.1

0.4 ± 0.2

39 ± 4

12.4 ± 1.0

1.0 ± 0.2

1.3 ± 0.1

4.3 ± 0.2

< 0.1

0.4 ± 0.2

35 ± 7

12.7 ± 1.0

0.8 ± 0.2

1.2 ± 0.1

5.1 ± 0.2

0.1

0.4 ± 0.2

37 ± 1

14.7 ± 0.1

0.4 ± 0.2

1.4 ± 0.1

4.5 ± 0.1

0.1

0.4 ± 0.2

38 ± 2

13.2 ± 0.1

0.8 ± 0.1

1.2 ± 0.1

4.9 ± 0.1

0.1

0.4 ± 0.2

29 ± 2

13.1 ± 0.1

1.0 ± 0.1

1.2 ± 0.1

5.0 ± 0.2

0.3

0.5 ± 0.1

32 ± 2

13.3 ± 0.1

0.9 ± 0.1

1.2 ± 0.1

4.7 ± 0.1

0.4

0.8 ± 0.1

30 ± 2

12.9 ± 0.1

0.9 ± 0.1

1.1 ± 0.1

4.7 ± 0.2

0.7

0.6 ± 0.1

28 ± 4

13.3 ± 0.1

0.9 ± 0.1

1.0 ± 0.1

4.1 ± 0.1

0.1

0.4 ± 0.2

9±5

1.0 ± 0.2

< 0.2

< 0.2

1.3 ± 0.1

< 0.1

0.4 ± 0.2

26 ± 5

8.1 ± 0.3

< 0.2

< 0.2

2.0 ± 0.3

0.1

0.6 ± 0.1

36 ± 6

12.3 ± 1.7

0.4 ± 0.2

0.9 ± 0.2

2.5 ± 0.4

0.1

0.5 ± 0.1

45 ± 8

11.2 ± 0.4

0.4 ± 0.2

1.1 ± 0.1

2.6 ± 0.3

0.3

0.4 ± 0.2

35 ± 5

9.4 ± 0.8

0.2 - 0.5

1.0 ± 0.1

2.2 ± 0.3

0.5

0.4 ± 0.2

34 ± 2

10.2 ± 0.8

0.4 ± 0.2

0.6 ± 0.1

2.0 ± 0.1

0.2

0.8 ± 0.5

29 ± 9

11.4 ± 2.6

0.4 ± 0.2

1.0 ± 0.4

2.5 ± 0.5

0.1

0.4 ± 0.2

26 ± 9

12.2 ± 3.6

0.4 ± 0.2

0.5 ± 0.2

2.9 ± 1.3

0.1

0.4 ± 0.2

21 ± 6

11.0 ± 1.9

0.4 ± 0.2

0.4 ± 0.2

2.5 ± 0.8

0.1

0.4 ± 0.2

17 ± 2

10.1 ± 1.4

< 0.2

0.4 ± 0.2

2.6 ± 0.4

0.3

2.0 ± 0.2

48 ± 3

17.0 ± 7.9

0.7 ± 0.2

0.9 ± 0.2

3.6 ± 1.1

0.6

0.7 ± 0.1

14 ± 3

10.7 ± 2.2

< 0.2

0.4 ± 0.2

2.3 ± 0.4

0.1

0.7 ± 1.1

23 ± 13

7.9 ± 5.6

0.4 ± 0.3

0.6 ± 0.5

2.5 ± 1.8

0.6 ± 0.4

30.8 ± 9.1

11.4 ± 2.9

0.5 ± 0.3

0.9 ± 0.4

3.5 ± 1.4

Sum of Chlorophyll U5-U9


19


Page 20 of 33

322

The concentrations of AB never exceeded 10 ng As kg-1 seawater and were commonly below

323

2 ng As kg-1 (Table 1). The sites from the high nutrient area generally showed a higher content of

324

AB (usually ca 1-2 ng As kg-1 seawater) compared to low nutrient sites (usually

325

ca < 0.2-1 ng As kg-1). Within each site, we also observed a weak positive correlation between

326

AB concentrations and chlorophyll levels (Figure 5 and Figure S2). Algae are not considered to

327

be a significant source of arsenobetaine, although it has been occasionally reported in some

328

macroalgae.24,25 Marine animals, however, including zooplankton,26,27 usually contain high

329

concentrations of arsenobetaine, so probably the observed relationship with chlorophyll is a

330

reflection of increased biomass of zooplankton and predatory animals associated with the photic

331

zone.

332

333 334

Figure 5. Depth profiles of AB (black points) and chlorophyll-a (grey lines) at two sites

335

representing high and low nutrient waters (mean ± standard deviation; n = 3). Red vertical line

336

indicates LOD (0.2 ng As kg-1).


20

Page 21 of 33


337 338

The concentrations we found for DMA ranged from ca 5-250 ng As kg-1 (Table 1 and Figure

339

S3), making it by far the most abundant organoarsenical we detected with our method. These

340

values were in good agreement with the results from earlier studies1-6 employing hydride

341

generation techniques, which reported DMA concentrations ranging from 2 to 400 ng As kg-1

342

throughout a 200 m depth profile. The trimethylated organoarsenical TMAO was the second

343

most abundant arsenic species in our processed samples occurring at all sites and all depths at

344

concentrations up to 70 ng As kg-1 (Table 1 and Figure S4). The average concentrations of both

345

DMA and TMAO in depths < 200 m were 1.3-2.3 times higher in the high nutrient waters

346

compared with the low nutrient samples. At high nutrient sites we also observed a decrease in

347

DMA and TMAO concentrations in the waters deeper than ca 50 m; the low nutrient sites

348

showed a similar but less distinct trend. At depths below 500 m (LN1) concentrations of TMAO

349

were markedly lower (ca 5 to 20-fold) than those in the shallower waters; the DMA pattern here

350

was similar, with 3 to 5-fold lower concentrations in the waters below 500 m.

351

DMAE and DMAB, were the least abundant of the identified arsenicals in the tested seawaters

352

with collective concentrations usually ranging from < 0.2 to 2 ng As kg-1 (Table 1 and Figure

353

S5), and their distribution in the water column was similar to the more abundant arsenic species

354

described above. Concentrations of the unknown arsenicals U4 and collectively U5-U9 ranged

355

between < 0.2 and 10 ng As kg-1 (Table 1, Figure S4 and Figure S5); the low concentrations of

356

the individual arsenic species precluded elucidation of their structure by means of HR-ESMS,

357

and they remain unidentified for now.

358

The sum of all detected species (arsenate by direct HPLC-ICPMS analysis and the 16

359

organoarsenicals measured in the processed samples) in the tested seawaters, constituted a


21


Page 22 of 33

360

recovery of 90-98 % of the total As present. Expressed as an overall average of the 16 seawater

361

samples (for which total arsenic and arsenate measurements were also made), the total arsenic

362

content comprised approximately 90 % arsenate, 3 % DMA, 0.5 % TMAO, 0.1 % AB, and 1.5 %

363

of the remaining organoarsenicals. Arsenite could not be quantified by our methods, neither by

364

direct analysis (it eluted at the void volume) nor in the processed samples (because it is not

365

retained by the Dowex column). Despite the low concentrations of the new seawater arsenic

366

species reported here, which collectively constitute < 3 % of the total arsenic in seawater, they

367

could play a role as intermediates in the cycling of arsenic in the sea, as discussed below.

368 369 370

Arsenic cycling in marine systems - the role of arsenobetaine and other newly discovered organoarsenic compounds

371

It is now generally accepted that algae take up arsenate from seawater and biotransform it into

372

organic forms including DMA, arsenosugars, and arsenolipids; one or more of these arsenic

373

forms is the likely precursor to AB. These biotransformation processes are so efficient that

374

arsenobetaine is by far the most abundant arsenical found in marine animals, and arsenate is

375

usually a trace constituent. Because AB is chemically a very stable compound,28 one might

376

expect to find it not only in the euphotic zone but throughout the water column, albeit at

377

vanishingly low concentrations at depth. The results reported here support that view to some

378

extent with traces of AB still being found in deeper waters. The relevance of this observation to

379

the presence of AB in deep-sea hydrothermal vent organisms including mussels and crustaceans

380

remains to be investigated.29,30 We note, however, that arsenobetaine is accumulated from

381

seawater by mussels much more efficiently than are other arsenic species31 so that even its trace

382

presence in seawater could result in appreciable levels in the organisms.


22

Page 23 of 33


383

The fate of AB in seawater will also depend on the surrounding microbial community.32,33 The

384

ubiquitous presence of potential AB-degrading microorganisms in seawater, particulate matter,

385

and sediments can lead to degradation of AB to TMAO, which is then further decomposed to

386

DMA, and finally to inorganic arsenic.33-35 DMAA was also later identified as an intermediate in

387

these processes.36,37 Thus, several of the organoarsenicals identified in this study could be

388

derived from AB, and might represent intermediates in the regeneration of arsenate in the sea.

389

On the other hand, the short chain arsenic-containing alcohols (e.g. DMAE) and fatty acids (e.g.

390

DMAA; DMAP) can also result from degradation of arsenosugars38 and arsenolipids39.

391

Arsenolipids, some of which also contain an arsenosugar group,10 might appeal as the primary

392

candidates given the fact that they have the potential to be released to the water column by

393

passive transport through the algal cell membrane.40,41 The method we used for this study was

394

not suitable for measuring the arsenosugars or arsenolipids, and hence the natural presence of

395

these compounds in seawater could not be demonstrated.

396

The data reported here on seawater AB and other organoarsenicals, and further application of

397

the method to other marine systems, could provide a new perspective on the complex

398

interactions of the various arsenic species and their role in the cycling of marine arsenic. It is

399

indeed sobering to think that 40 years after the first identification of AB in lobster,42 the origin of

400

AB in marine animals remains elusive, and we still know little about the fate and movement of

401

this key arsenical in marine systems.

402

In summary, we report a method for determining AB and other cationic organoarsenicals in

403

marine water samples at the ng As kg-1 level, and apply the method to seawater collected from

404

seven sites in the North Atlantic at depths down to 4900 m. The study revealed for the first time

405

the presence of AB in seawater together with 15 other organoarsenicals, nine of which remain


23


Page 24 of 33

406

unidentified. Future application of the method in oceanographic studies could provide a more

407

complete picture of arsenic cycling in the sea.


24

Page 25 of 33


408

ASSOCIATED CONTENT

409

Supporting Information. Nutrient concentrations at sampling sites (Table S1), concentrations

410

of total As and arsenate in samples (Table S2), flow injection ICPMS and anion HPLC-ICPMS

411

of a sample (Figure S1), further depth profiles of AB (Figure S2), depth profiles of DMA (Figure

412

S3), depth profiles of U5-U9 and TMAO (Figure S4), depth profiles of U4 and DMAE+DMAB

413

(Figure S5), HPLC-ICPMS chromatograms of selected organoarsenic standards (Figure S6).

414

(PDF)

415

This material is available free of charge via the Internet at http://pubs.acs.org.

416 417

AUTHOR INFORMATION

418

Corresponding Author

419

* E-Mail: [email protected]

420

ORCID: Kevin Francesconi: 0000-0002-2536-0542

421

Notes

422

The authors declare no competing financial interest.

423 424

ACKNOWLEDGEMENTS

425

This research was supported by the Austrian Science Fund (FWF) project number 23761-N17.

426

We also thank NAWI Graz for supporting the Graz Central Lab – Environmental Metabolomics.


25


427 428 429 430 431 432

Page 26 of 33

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104x74mm (300 x 300 DPI)


Arsenobetaine in Seawater: Depth Profiles from Selected Sites in the

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