Sulfide as a soil phytotoxin-a review

Abstract

In wetland soils and underwater sediments of marine, brackish and freshwater systems, the strong phytotoxin sulfide may accumulate as a result of microbial reduction of sulfate during anaerobiosis, its level depending on prevailing edaphic conditions. In this review, we compare an extensive body of literature on phytotoxic effects of this reduced sulfur compound in different ecosystem types, and review the effects of sulfide at multiple ecosystem levels: the ecophysiological functioning of individual plants, plant-microbe associations, and community effects including competition and facilitation interactions. Recent publications on multi-species interactions in the rhizosphere show even more complex mechanisms explaining sulfide resistance. It is concluded that sulfide is a potent phytotoxin, profoundly affecting plant fitness and ecosystem functioning in the full range of wetland types including coastal systems, and at several levels. Traditional toxicity testing including hydroponic approaches generally neglect rhizospheric effects, which makes it difficult to extrapolate results to real ecosystem processes. To explain the differential effects of sulfide at the different organizational levels, profound knowledge about the biogeochemical, plant physiological and ecological rhizosphere processes is vital. This information is even more important, as anthropogenic inputs of sulfur into freshwater ecosystems and organic loads into freshwater and marine systems are still much higher than natural levels, and are steeply increasing in Asia. In addition, higher temperatures as a result of global climate change may lead to higher sulfide production rates in shallow waters.

Keywords: global change; iron; microorganism; oxygen; plant; roots; sulfur; symbiosis.

Figure 1

Example of an experimental set-up using rhizotrons showing inflow, outflow, and the tubes of samplers to collect soil porewater (photo: L. Lamers).

Figure 2

Interacting effects of dissolved sulfide and iron (concentrations in μmol L⁻¹) in the soil porewater on biomass production of Caltha palustris. Although both compounds may be toxic for plant growth, they detoxify one another as a result of FeS_x precipitation (quadratic correlation, p = 0.014). Adapted from Van der Welle et al. (2006).

Figure 3

Rhizotron scans for a control (A) and 250 μmol L⁻¹ (B) sulfide treatment (darker soil due to FeS_x deposits). The oxidation potential is clearly visible from the yellow-gray halo of metallic sulfur and other products of oxidation. In each scan, Carex disticha is positioned left (only shallow S oxidation halos) and Juncus acutiflorus right (deep S oxidation halos). On (B), two white soil moisture samplers are visible. Bars represent 40 mm. Adapted after Lamers (2001) and Lamers et al. (2012).

Figure 4

Sulfide-driven coevolution: tripartite mutualistic interactions among seagrasses, lucinid bivalves and sulfide oxidizing bacteria in their gills generate a higher fitness of all species involved under sulfidic conditions. See text for explaining mechanisms. Adapted after Van der Heide et al. (2012).

Figure 5

Conceptual model showing positive feedback loops on plant-rhizophere processes under scenarios of sulfide toxicity (left) and non-toxicity (right). See text for further explanation. Unlike in other studies, impaired uptake of N or Fe was not found in this study. Impaired gas transport by sulfide has been shown by Armstrong et al. (1996). Sulfide oxidation is carried out by free-living prokaryotes in sediment and water, symbiotic prokaryotes of roots and soil fauna, and mitochondrial metabolism in soil fauna and plants.