The biogeochemistry of hydrogen sulfide: Phytoplankton production in the surface ocean

Hydrogen sulfide can exist in oxic waters in the form of a dissolved gas, dissociated ions, dissolved metal sulfide complexes, and particulate metal sulfides. The sum of the dissolved species is termed total dissolved sulfide (TDS). In addition to the hydrolysis of carbonyl sulfide, it has been speculated that phytoplankton may produce TDS. We present results from preliminary culture studies which demonstrate that phytoplankton produce TDS and particulate acid-volatile sulfide (pAVS). The phylogenetic order of TDS + pAVS production (per unit cell volume) for the oceanic species examined is Synechococcus sp. > Emiliania huxleyi x Pyramimonas obovata > Thalassiosira oceanica. Moreover, TDS and pAVS production increases when the concentrations of uncomplexed trace metals in culture media are also increased, suggesting metal detoxification via the formation of metal sulfide complexes. Aqueous hydrogen sulfide exists in seawater as the dissolved gas, its dissociated bisulfide (SH-), and sulfide (S2-) ions and is also associated with dissolved metals in metal sulfide complexes. Here the term “total dissolved sulfide” (TDS) refers to the sum of these species. TDS was previously considered too unstable with respect to oxidation by oxygen in surface waters to play any significant role in the biogeochemistry of sulfur (Gstlund and Alexander 1963). Nevertheless, the presence of picato nanomolar concentrations of TDS in the upper ocean has been reported (Cutter and Krahforst 1988; Luther and Tsamakis 1989; Andreae et al. 199 1). Luther and Tsamakis (1989) reported that sulfide can persist in seawater for months, even in the presence of the oxidants 02, H202, and 103-. They concluded that this stability arises from the formation of metal sulfide complexes. These results have focused interest on the contribution of TDS to the atmospheric sulfur budget (Andreae et al. 199 1) and on the possible role of TDS in trace metal complexation (Dyrssen and Wedborg 1989). Acknowledgments We thank John Donat, Tiffany Moison, Beth Ahner, and two anonymous reviewers whose comments greatly improved the manuscript. This work was supported by NSF grant OCE 9018484 to G. Cutter. However, the mechanisms responsible for the production of TDS in surface waters are not well understood. One likely source of TDS in oxic seawater is carbonyl sulfide (OCS) hydrolysis, which proceeds at a rate sufficient to support the observed surface concentrations of TDS (Elliott et al. 1987, 1989). In depth profiles from the western North Atlantic, however, subsurface maxima in TDS occasionally correspond to those of chlorophyll a (Cutter and Krahforst 1988; Luther and Tsamakis 1989), implying the involvement of phytoplankton in TDS production. Indeed, the possibility that marine phytoplankton might produce TDS has been suggested by Andreae (1990). Biotic production of TDS under oxic conditions is not unprecedented; H,S,, emission by terrestrial plants is well documented (e.g. Rennenberg 1984), although very little is known about production by marine plants. In studies of resistance to Hg poisoning, Davies ( 1976) measured up to 1 pmol liter-’ TDS in cultures of the neritic phytoplankter Dunaliella tertiolecta. The remarkable tolerance of D. tertiolecta to Hg was largely attributed to the detoxification of the metal within the cell, possibly by the precipitation of highly insoluble mercuric sulfide (Davies 1976). We examine the production of TDS using results from laboratory cultures of four oceanic phytoplankton species and two neritic species. We had two objectives. The first was to ascertain whether oceanic phytoplankton species are capable of TDS production. Our goal here was to determine whether TDS production is a general feature of marine phytoplankton populations. Our second objective was to identify factors that affect TDS production. With respect to this second objective, we investigated two factors that could control the production of TDS: nutrient and trace metal concentrations. Under low nutrient conditions, TDS production could be a part of the assimilatory sulfate uptake pathway. In this scenario, which was first proposed by Rennenberg (1984) to account for H,S,, emission by terrestrial plants,