Root activities and arsenic translocation of Avicennia marina (Forsk.) Vierh seedlings influenced by sulfur and iron amendments

Highlights

• Avicennia marina exhibit a high As tolerance potential.

• The supplies of iron and sulfur showed positive growth effects under As stress.

• Both iron and sulfur facilitated the formation of ROL-induced iron plaque.

• The presence of iron plaque may act as a barrier for protection against As.

Abstract

Sulfur and iron are abundant and have close, complex interactions with the biogeochemical cycle of arsenic (As) in mangrove ecosystems. A hydroponic experiment was conducted to investigate the influences of variable SO₄²⁻ and Fe²⁺ supplies on radial oxygen loss (ROL), iron plaque formation and As translocation in Avicennia marina upon exposure to As(III). The results indicate that A. marina is an As-tolerant plant, the application of iron and sulfur not only showed positive growth effects but also induced much higher amounts of ROL-induced iron plaque formation on root surfaces. The presence of iron plaque remarkably improved the proportion of As sequestration near this area but consequently reduced the proportion of As translocation in root. Therefore, it is concluded that iron plaque may act as a barrier for protection against As, and iron and sulfur play important roles in controlling the growth and translocation of As in A. marina seedlings.

Introduction

As an important links between terrestrial and marine ecosystems, mangroves act as a “natural filter” or “green barrier” of industrial and domestic wastewaters and solid wastes in estuary and coastal areas (Nath et al., 2014; Ramos e Silva et al., 2006). However, due to their anaerobic and organic-rich muddy sediments, mangroves are also commonly regarded as a potential sink and source of heavy metal(loid)s (Silva et al., 1990; Zhou et al., 2011). Moreover, the uniquely high production of this ecosystem coupled high rates of litter production may induce an aggravating sedimentary sink for heavy metals (Gonneea et al., 2004; Mandal et al., 2009).

Arsenic (As), cited as a hazardous pollutant by the US Environmental Protection Agency (USEPA) (ATSDR, 2012), is a Group V element of the periodic table and a ubiquitous, non-essential metalloid for plants. Natural and anthropogenic sources of As have resulted in As enrichment in mangroves, posing threats to ecological environment and plant health (Khan et al., 2016). Arsenic content as high as 30–320 mg kg⁻¹ was previously reported in the surface sediment of Bothnian Bay (Leivuori and Niemistti, 1993), and 33.80–48.18 mg kg⁻¹ was reported in the surface sediments of various mangrove vegetation communities in the Leizhou Peninsula of China (Liu et al., 2015). As enrichment was also observed in the shelf sediment, adjacent beach sands, and mangrove sediments of Brazil (Chakraborty et al., 2012a, Chakraborty et al., 2012b; Mirlean et al., 2012). Because of the carcinogenic and non-biodegradable properties of arsenic, the risks of a high As load in mangroves have received considerable attention.

Like most aquatic plants that must acclimate to anaerobic conditions due to waterlogging, such as Oryza sativa and Phragmites australis, mangroves have evolved a strategy that involves releasing excessive oxygen via the root aerenchyma to the rhizosphere (namely, radial oxygen loss, ROL) (Armstrong et al., 1992; Armstrong, 1964; Khan et al., 2016). The oxygen released by the root is commonly known as a strong oxidizing agent (Husson, 2013) and can oxidize reduced soluble Fe(II) to form a thin Fe(III) precipitation zone in the rhizosphere (Eq. (1)) on root surfaces (Taylor and Crowder, 1983; Williams et al., 2014).

$${\text{4Fe}}^{2+}+{\mathrm{O}}_2+{\text{6H}}_2\mathrm{O}=\text{4FeOOH}+{\text{8H}}^{+}$$

As the main component of iron (Fe) plaque on root surfaces, Fe (hydro-) oxides with a large specific surface area (>200 m² g⁻¹) (Hansel and Fendorf, 2001) have a high affinity for metals. Thus, the Fe plaque is regarded as a main buffer and an efficient scavenger of heavy metals (Khan et al., 2016; Mirlean et al., 2012; Taylor and Crowder, 1983; Wang et al., 2012). Seyfferth et al. (2011) found that As could easily enter rice plants via the root and translocate to the shoots without Fe plaque coverage. Therefore, it is generally accepted that the biogeochemical cycling of iron closely affects the fate of As (Al-Sid-Cheikh et al., 2015). To date, the formation of Fe plaques on root surfaces has been reported to control the uptake and accumulation of several metals (e.g., Cd, Cr, Zn, Mn, Pb, Ni, and Cu) (Du et al., 2013; Li et al., 2015; Machado et al., 2005; Pi et al., 2011). Nonetheless, the potential effects of various rates of iron nutrition (due to complex abiotic environments in different mangroves) on the activity of roots and the behavior of As by mangroves is still unclear.

Mangrove environments are characterized by sulfur-rich and contain potentially acidic sulfate sediment (Ferreira et al., 2007). Sulfur is not only an essential component macronutrient for plants but is also closely related to redox conditions. According to previous investigations of sulfate sediment, the fate of As is more complicated; sulfur, not only iron, is closely related to the biogeochemical process of As contamination (Stuckey et al., 2015; Wang et al., 2012). The effects of sulfur in mediating As toxicity have been reported in several plants (especially in Oryza sativa and Pteris vittata). However, the studies on the effects of sulfur application on alleviating As toxicity and regulating As uptake by plants have conflicting results (de Oliveira et al., 2014; Srivastava and D'Souza, 2010; Zhang et al., 2011). As far as we know, only one study related to the potential effects of sulfur supply on As behavior by mangroves has been reported by Wu et al. (2015), who found that the presence of sulfur (S₀) could change As translocation in Aegiceras conriculatum seedlings and mitigate the As toxicity at low sulfur concentrations. Unfortunately, limited information is available on the potential functions of ROL and Fe plaque formation under As exposure in relation to the external S supply by mangrove plants.

Given the complex relationship between iron and sulfur biogeochemistry, and the limited information about the three-way interactions among arsenic, iron and sulfur in mangrove environments, it is essential to explore this topic further. The objectives of this study were 1) to explore the potential effects of iron and sulfur nutrition on plant growth and root activities when subjected to different rates of As contamination in hydroponic culture and 2) to unravel whether the formation of Fe plaques and the rates of ROL by roots affected the tolerance and translocation of As in mangrove seedlings. Our experiment was employed in gray mangroves, Avicennia marina (Forsk.) Vierh, which have typical and complex root systems (Chaudhuri et al., 2014).