Abstract
Gaseous sulfide intrusion into seagrasses growing in sulfidic sediments causes little or no harm to the plant, indicating the presence of an unknown sulfide tolerance or detoxification mechanism. We assessed such mechanism in the seagrass Zostera marina in the laboratory and in the field with scanning electron microscopy coupled to energy dispersive X-ray spectroscopy, chromatographic and spectrophotometric methods, and stable isotope tracing coupled with a mass balance of sulfur compounds. We found that Z. marina detoxified gaseous sediment-derived sulfide through incorporation and that most of the detoxification occurred in underground tissues, where sulfide intrusion was greatest. Elemental sulfur was a major detoxification compound, precipitating on the inner wall of the aerenchyma of underground tissues. Sulfide was metabolized into thiols and entered the plant sulfur metabolism as well as being stored as sulfate throughout the plant. We conclude that avoidance of sulfide exposure by reoxidation of sulfide in the rhizosphere or aerenchyma and tolerance of sulfide intrusion by incorporation of sulfur in the plant are likely major survival strategies of seagrasses in sulfidic sediments.
Highlights
Seagrasses colonize coastal sediments characterized by low oxygen concentrations and high concentrations of toxic, reduced substances such as iron, manganese, and sulfide [1]
The δ34S of sediment sulfide shifted in the glucose treatment (p < 0.0001; δ34S acid-volatile sulfide (AVS): 6.9 ± 1.5‰ for High sediment sulfide levels (HS) and −16 ± 1.3% for C; δ34S chromium-reducible sulfur (CRS): −12.7 ± 1.5‰ for HS and −22.6 ± 0.5‰ for C), reflecting the expected increase in δ34S due to glucose enrichment
Of the three possible sulfur sources for seagrasses, the δ34S values of two—the pore water sulfate (20.9 ± 0.8‰) and the water column sulfate (20.4 ± 1.2‰)—did not respond to treatment (p > 0.05), whereas the third, the δ34S of sediment sulfide (AVS), shifted (p < 0.0001) by a Δδ34S of 22.9 ± 0.4‰
Summary
Seagrasses colonize coastal sediments characterized by low oxygen concentrations and high concentrations of toxic, reduced substances such as iron, manganese, and sulfide [1]. The effect of sulfide on growth and health of seagrasses is puzzling. Sulfide is toxic to eukaryotic cells including seagrass cells even at concentrations as low as 1 to 10 μmol L-1 [2,3,4]. Seagrasses can thrive in sediments with sulfide concentrations in the millimolar range [5]. Field and laboratory studies show that oxygen and sulfide dynamics in the water column, sediment, and plant tissues are key factors for seagrass growth, colonization, and survival [8,10,11]. Seagrasses avoid root anoxia and sulfide intrusion by leakage of oxygen from the roots (radial oxygen loss, ROL) [12,13]: photosynthetically derived oxygen diffuses via the PLOS ONE | DOI:10.1371/journal.pone.0129136 June 1, 2015
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