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Promotion of Arsenic Phytoextraction Efficiency in the Fern

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Promotion of Arsenic Phytoextraction Efficiency in the Fern ORIGINAL RESEARCH ARTICLE published: 18 February 2015 doi: 10.3389/fpls.2015.00080 Promotion of arsenic phytoextraction efficiency in the fern Pteris vittata by the inoculation of As-resistant bacteria: a soil bioremediation perspective Silvia Lampis1*, Chiara Santi 1, Adriana Ciurli 2 , Marco Andreolli 1 and Giovanni Vallini 1* 1 Department of Biotechnology, University of Verona, Verona, Italy 2 Department of Agricultural, Food and Agro-Environmental Sciences, University of Pisa, Pisa, Italy Edited by: A greenhouse pot experiment was carried out to evaluate the efficiency of arsenic Antonella Furini, University of Verona, phytoextraction by the fern Pteris vittata growing in arsenic-contaminated soil, with or Italy without the addition of selected rhizobacteria isolated from the polluted site. The bacterial Reviewed by: strains were selected for arsenic resistance, the ability to reduce arsenate to arsenite, Lena Ma, University of Florida, USA Agnieszka Galuszka, Jan Kochanowski and the ability to promote plant growth. P. vittata plants were cultivated for 4 months University, Poland in a contaminated substrate consisting of arsenopyrite cinders and mature compost. *Correspondence: Four different experimental conditions were tested: (i) non-inoculated plants; (ii) plants Silvia Lampis and Giovanni Vallini, inoculated with the siderophore-producing and arsenate-reducing bacteria Pseudomonas Department of Biotechnology, sp. P1III2 and Delftia sp. P2III5 (A); (iii) plants inoculated with the siderophore and University of Verona, Strada le Grazie 15, 37134 Verona, Italy indoleacetic acid-producing bacteria Bacillus sp. MPV12, Variovorax sp. P4III4, and e-mail: [email protected]; Pseudoxanthomonas sp. P4V6 (B), and (iv) plants inoculated with all five bacterial strains [email protected] (AB). The presence of growth-promoting rhizobacteria increased plant biomass by up to 45% and increased As removal efficiency from 13% without bacteria to 35% in the presence of the mixed inoculum. Molecular analysis confirmed the persistence of the introduced bacterial strains in the soil and resulted in a significant impact on the structure of the bacterial community. Keywords: arsenic, arsenopyrite cinders, phytoextraction, plant growth-promoting rhizobacteria, Pteris vittata, rhizosphere-enhanced phytoremediation INTRODUCTION Arsenic is acutely toxic to humans and also has a chronic impact Arsenic is widely dispersed in the Earth’s crust with an average on health, as well as genotoxic and carcinogenic effects (Léonard concentration of ∼5mgkg−1. It is a component of more than 200 and Lauwerys, 1980; Ratnaike, 2003; Hughes et al., 2011). It is minerals, although it primarily exists as arsenopyrite and other considered to be five times as dangerous as lead (United States sulfides. Rocks can release arsenic compounds during weathering, Department of Health and Human Services [US-DHHS], 2007). allowing dispersion by wind and water. The natural arsenic con- The chronic effects of arsenic include gastrointestinal disorders, tent of soils ranges from 0.01 to more than 600 mg kg−1 (Yan-Chu, anemia, peripheral neuropathy, skin lesions, hyperpigmentation, 1994). Approximately one third of the arsenic in the atmosphere gangrene of the extremities, vascular lesions, liver and kidney dam- is also from natural sources, such as volcanoes and forest wild- age, and spontaneous abortions (Szymañska-Chabowska et al., fires (United States Environmental Protection Agency [US-EPA], 2002; Fernández et al., 2012). The inhalation of arsenic-containing 1998). compounds is a minor exposure route with the exception of work- The remaining arsenic in the environment is anthropogenic ers in the copper-smelting and pesticide-manufacturing indus- in origin. Arsenic is used in the pharmaceutical, glass, timber, tries, and in power plants burning arsenic-rich coal (Naujokas and leather industries, and for the production of pigments, metal et al., 2013). Arsenic exposure through contaminated drinking alloys, semiconductors, and optoelectronics. Uncontaminated water is common in mine drainage areas and where the bedrock soils usually contain 0.2–40 mg kg−1 arsenic but concentra- has a high arsenic content (Nordstrom, 2002; Rahman et al., 2009) − tions of 100–2500 mg kg−1 can be found in the vicinities of exceeding the 10 μgl 1 safety limit established by the United States copper-smelting plants and in heavily pesticide-contaminated Environmental Protection Agency (US-EPA, 1998) and the World agricultural soils, which are the greatest sources of arsenic pol- Health Organization (WHO, 2000). Arsenic may also be present lution (World Health Organization [WHO], 2000). The diverse in the diet, particularly in seafood, e.g., marine fish, mussels, industrial uses of arsenic provide many opportunities for human and certain crustaceans (European Food Safety Authority [EFSA], exposure to the element (Garelick et al., 2008). Arsenic in soils 2009). 2− exists predominantly as arsenate (AsV), which includes HAsO4 The presence of arsenic in the environment and its associ- − and H2AsO4 . However, arsenite (AsIII), arsine (AsH3), and ated health risks have led to the deployment of conventional several organoarsenic compounds are also found (Roy et al., remediation strategies for the cleanup of contaminated sites 2015). including removal (excavation and landfilling) and containment www.frontiersin.org February 2015 | Volume 6 | Article 80 | 1 Lampis et al. PGPR-enhanced As-phytoextraction in Pteris vittata (capping). Because both these approaches are expensive, plant- promote plant growth by producing indoleacetic acid (IAA) or assisted bioremediation (phytoremediation) has been considered siderophores. The overall aim was to identify bacterial strains that as an inexpensive and environmentally beneficial in situ treatment promote the translocation of arsenic from contaminated environ- for polluted soils (Pilon-Smits, 2005). This is based on the ability mental matrices into plant tissues, especially the epigeal portion of hyperaccumulator plants to extract metals (including metal- of P. vittata. loids such as arsenic) from contaminated soils and sequester the minerals in their aboveground biomass (Lasat, 2002). However, MATERIALS AND METHODS effective phytoremediation in metal/metalloid-contaminated soils THE CONTAMINATED SITE requires a detailed understanding of the complex interactions in The contaminated site is located in the Scarlino industrial area the rhizosphere, because soil microbes influence metal bioavail- (Province of Grosseto, south–west Tuscany, GR, Italy) adjacent to ability (Rani and Juwarkar, 2013). For example, microbes catalyze a former Nuova Solmine SpA sulfuric acid production facility that redox reactions leading to changes in the mobility of metals and was operational between 1962 and 1995. The production method their ions, and thus the efficiency with which they are taken up involved the roasting of arsenopyrite mined from the Colline Met- by roots (Sessitsch et al., 2013). Microbes therefore play a crucial allifere source, 20 km to the east of the processing plant (Figure 1). role in arsenic geochemical cycling through biochemical transfor- The Nuova Solmine SpA site has been classified by the Regional mation, e.g. reduction, oxidation, and methylation (Smedley and Government of Tuscany as an industrial landfill suitable for recla- Kinniburgh, 2002; Lloyd and Oremland, 2006; Páez-Espino et al., mation (Site GR66, Resolution No. 384, 21 December, 1999; Ciurli 2009). et al., 2014). During the operational lifetime of the facility, ∼1.5 Here we focus on a severe case of arsenic contamination in the million tons of arsenopyrite cinders with an average arsenic con- Scarlino industrial area (south–west Tuscany, GR, Italy) caused by tent of 370 mg kg−1 was dumped in the landfill site, exposing ∼550 the dumping of 1.5 million tons of arsenopyrite cinders gener- tons of arsenic to rainfall and creating a serious risk of leaching and ated during the manufacture of sulfuric acid. The cinder layer groundwater contamination (Focardi and Tiezzi, 2009). Nuova covering the soil is currently being removed as the first step Solmine SpA is facilitating the reclamation of this site by excavat- toward restoring the site, but a more refined strategy is required ing the cinders and reusing them for industrial processes such as to regenerate the underlying soil, which is now heavily contam- steel production and brick manufacturing, leaving 700,000 tons inated with arsenic minerals. We tested a remediation strategy of cinders remaining on site. These remnants have sunk 2–5 m for soil mixed with arsenopyrite cinders based on microbially below the ground level, so the excavated field is being progres- enhanced phytoextraction using the arsenic hyperaccumulator sively refilled with clean agricultural cover soil from a nearby site fern species Pteris vittata. We carried out a mesocosm experi- to prevent the dispersion of contaminated dust. ment under glasshouse conditions as a preliminary test to evaluate the efficiency of arsenic phytoextraction by P. vittata with or ISOLATION OF ARSENIC-RESISTANT BACTERIAL STRAINS FROM without the help of bacterial inoculums comprising species iso- ENRICHMENT CULTURES lated from the rhizosphere of autochthonous plants grown on Soil aliquots (5 g) from samples collected within the rhizosphere of surrounding soil. The bacteria were enriched by selection with different autochthonous plants growing in the Scarlino area were arsenite As(III) or arsenate As(V) to identify
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