The role of sewage sludge biochar in methylmercury formation and accumulation in rice

Highlights

• SSB application reduced MeHg accumulation in rice in acid soil.

• SSB application resulted in the increase of MeHg concentration in acid soil.

• MeHg accumulation in rice root decreased during rice growth period.

• Release of rice root exudates lowered soil pH and further promoted MeHg formation.

Abstract

Methylmercury (MeHg) can accumulate in rice and this has been demonstrated to be an important human MeHg exposure pathway. How to reduce MeHg concentrations in rice grains has therefore become a very important public health issue. Previous studies have investigated the role of plant biochars on Hg bioavailability in soils but knowledge of the influence of sewage sludge biochars (SSB) on MeHg formation and bioaccumulation in different soils is lacking. In the present study, SSB was applied to two Hg-contaminated soils, one acid and the other calcareous, in an attempt to stabilize MeHg in the soil and further mitigate MeHg accumulation in rice grains. The results indicate that the presence of SSB may promote Hg methylation in an acid soil. Moreover, MeHg concentrations increased gradually during rice growth, perhaps due to the release of root exudates. SSB can inhibit both MeHg and total Hg (THg) accumulation in different rice tissues. Both MeHg and THg decreased in the rice grains by up to 73.4 and 81.9%, respectively. However, the inhibitory effect was less pronounced in a calcareous soil. This study further demonstrates that biochar application can inhibit MeHg accumulation in soils despite the promotion of MeHg formation in soil by SSB application. However, an effect of biochar on MeHg accumulation was observed only in the acid soil. These results are useful in managing applications of biochars to Hg-contaminated paddy fields.

Introduction

Mercury is a global contaminant and a toxicant of major concern in human beings and wildlife. There are several species of Hg including elemental Hg, inorganic Hg and organic Hg. An organic species of Hg, methylmercury (MeHg), is highly toxic and bioaccumulative (Ullrich et al., 2001). The process of MeHg formation and bioaccumulation has therefore been studied extensively over the last 40 years (Schaefer and Morel, 2009). Previous studies demonstrate that MeHg can be formed under anaerobic conditions in aquatic systems, e.g. oceans, lakes and rivers (Hammerschmidt and Fitzgerald, 2004, Marvin-DiPasquale et al., 2009, Tsui et al., 2010). Sulfate-reducing bacteria play an important role in this process. However, recent studies show that MeHg can also be formed in anaerobic conditions in paddy fields, and furthermore, MeHg can accumulate in rice plants and especially in rice grains (Meng et al., 2011, Zhang et al., 2010b, Zhao et al., 2016).

The toxicity of different Hg species varies widely with MeHg compounds considerably more toxic than elemental Hg and its inorganic salts, and MeHg in our food is rapidly absorbed in the gastrointestinal tract and readily enters the brain. The nervous system is its principal target tissue (UNEP, 2002). In comparison, the kidney and the central nervous system are critical organs for human exposure to Hg. High exposure to Hg may cause (immune-complex mediated) glomerulonephritis with proteinuria and nephritic syndrome (UNEP, 2002).

Zhang et al. (2010a) pointed out that rice rather than fish is the major source of MeHg exposure to humans in inland China. Development of mitigation measures to lower MeHg levels in rice is therefore an urgent task because people who eat rice from Hg-contaminated sites are at high risk of Hg toxicity. Different methods have been used in attempts to inhibit the accumulation of Hg in rice. Peng et al. (2012) showed that growing rice aerobically markedly reduced the bioaccumulation of total Hg and MeHg within the grains because the aerobic conditions substantially decreased the bioavailability of total Hg and MeHg in the soil. Selenium (Se) addition largely reduces net MeHg production due to the formation of HgSe nanoparticles in the soil. In addition, recent studies indicate that a wide range of biochars including those made from pine dust, peanut hulls, barley straw, acai pits, turkey litter, chicken litter, Phragmites biomass and rice straw can effectively sorb and stabilize MeHg at low porewater concentrations in sediments and soils (Gomez-Eyles et al., 2013, Shu et al., 2016), leading to lower plant availability of MeHg. Moreover, amendment with biochars such as rice straw and sulfur-modified rice husk biochars can also increase plant biomass, leading to lower MeHg levels in grains by a dilution effect (O'Connor et al., 2018a, Shu et al., 2016). In addition to pot experiments, field experiments demonstrate that biochar application can potentially reduce contaminant bioavailability and reduce the amount of mineral fertilizer used in the field by supplying plant nutrients (O'Connor et al., 2018b).

Large amounts of sewage sludge are generated during the operation of wastewater treatment plants. Conventional disposal methods or uses of sewage sludges include landfill, combustion with energy production and application to agricultural land to recycle the plant nutrients present. However, the use of sewage sludges for food production has been prohibited in some countries because of risks from pathogens and contaminants, although sewage sludges can supply large amounts of carbon and plant nutrients to agricultural land (Méndez et al., 2012). The reuse of sewage sludges to produce biochars presents both environmental and economic opportunities because biochar products may reduce the amounts and volumes of the sewage sludge and also stabilize any contaminants present in soils and further decrease the accumulation of potentially toxic contaminants by plants (Jiang et al., 2012, Khan et al., 2013a, Méndez et al., 2012). Previous studies demonstrate that amendment with SSB significantly reduced the bioaccumulation of potentially toxic elements (PTEs) such as As, Cr, Co, Cu, Ni, and Pb in rice (Oryza sativa) (Khan et al., 2013a) and of persistent organic pollutants such as polyaromatic hydrocarbons (PAHs) in cucumber (Cucumis sativa) (Waqas et al., 2014) and lettuce (Lactuca satuva) (Khan et al., 2013b).

However, there have been few studies on the mitigation effects of SSB on MeHg accumulation in rice. Furthermore, most previous studies have been conducted in acid soils rather than calcareous soils. The objectives of the present study were therefore to investigate (1) the influence of SSB on MeHg formation in two soils of contrasting pH and (2) the role of SSB application to the soils in the mitigation of MeHg accumulation in rice tissues.