Research article
Sorption mechanism and distribution of cadmium by different microbial species

https://doi.org/10.1016/j.jenvman.2019.02.057Get rights and content

Highlights

  • Species identity and Cd concentrations affected the Cd sorption capacity.

  • Cd was mainly allocated on cell wall in P. stutzeri and B. subtilis.

  • Cd allocated on both cell wall and cytomembrane in H. anomala.

  • The three species showed various migration models during biosorption process.

Abstract

Bioremediation programs of cadmium (Cd) by microorganisms have being proposed, but the underlying mechanism of the remediation ion remains unexplored. Here, the sorption efficiency and subcellular fraction distribution of Cd in three selected microbial species were investigated. Our results showed that both species of the microorganisms and initial Cd concentrations strongly affected the Cd sorption capacity. In the three microbial species, the Cd removal efficiency increased with decreased Cd concentrations. Specifically, Hansenula anomala removed the highest Cd ions in low concentration of 0.05 mg L−1; while in medium concentration of 0.5 mg L−1 and high concentration of 5 mg L−1, Bacillus subtilis removed the highest Cd ions. The subcellular fractionation allocation showed that Cd was mainly allocated on cell wall (mantle and inner wall) in Pseudomonas stutzeri and B. subtilis, while cell cytomembrane accumulated similar amount of Cd compared to the cell wall of H. anomala at concentration of 0.5 mg L−1. Meanwhile, the Cd distributions on cell subcellular fractionation of the three species changed along the contact times, suggesting varied migration models during the biosorption process. Moreover, the functional groups involved in biosorption differed among the species based on Fourier Transform Infrared (FTIR) analysis. Our results have important implications for developing and improving Cd remediation by microorganisms, which is a low-cost and environmentally friendly bioremediation strategy of Cd pollution in environments.

Introduction

Cadmium (Cd) is a harmful pollutant which can bring health risks through the food chain (Nogawa et al., 2004; Angeletti et al., 2014; Ajima et al., 2015; Ullah et al., 2016; Peng et al., 2018). Various physical and chemical techniques have being used in the remediation of Cd contaminated sites, while they may co-occurr with secondary pollution for ecosystem structure, fauna and microorganisms (Jiang et al., 2009; Li et al., 2017). Thus, development of eco-friendly techniques is urgently needed, aiming to mitigate the bioavailability of Cd and reduce its accumulation on food production. In recent decades, phytoremediation and micro-remediation were advocated because of low cost, operability, high efficiency and environmental friendly, in especial the in-situ remediation using tolerant microbes (Alluri et al., 2007; Öztürk, 2007). Generally, high tolerant microbial species (Malik, 2004; Radhika et al., 2006; Farhadian et al., 2008; Wang and Sun, 2013; Kossoff et al., 2014) were applied for immobilizing potentially toxic heavy metals (PTHMS) in polluted sites by the form of exogenous addition (Kothe et al., 2005; Öztürk, 2007; Mengual et al., 2016; Peng et al., 2018). Therefore, screening of tolerant microbes with high removal efficiency could be significant for Cd remediation in contaminated environments.

In general, the bio-remediation pattern of resistant microbial species are mainly attributed to physisorption (Blanco, 2000; Pabst et al., 2010), chelation and complexation (Zouboulis et al., 2004) of PTHMS both outside and inside the cells (Shim et al., 2015). When microorganisms are exposed to the PTHMS solutions, the structures and chemical composition of cell wall determine interactions between the organisms and metal ions (Peraferrer et al., 2012). For example, Cd adsorption on cells is mainly depends on the combining ability of Cd by bio-macromolecules, or the exchanging ability of some original metal ions such as Ca 2+, Mg 2+ and H+ on microbial cells (Wu et al., 2009; Rukshana et al., 2012). Chelation is achieved through the exchange of Cd with the protons in the active groups such as -COOH, -PO34+, -SO3H, -NH of cell surface (Blanco, 2000). Cd can also form inorganic deposition and deposited in cell wall or inside cells by means of phosphor salt, sulfate, carbonate or hydroxide (Tangaromsuk et al., 2002; Özdemir et al., 2009). Moreover, microbially induced precipitation resulting from the reaction of ions or compounds with microbial metabolites, is an important form of microbial passivation and thus reduced the bioactivity of Cd (Achal et al., 2009; Mutiat et al., 2018).

However, bio-sorption ability depends on many factors such as cell wall composition, cell physiology and metal concentrations (Gabr et al., 2008; Hassan et al., 2009). Most studies focused on screening of high resistant species and testing their maximum tolerance of different PTHMS ions (Valentina, 2006; Chelliah et al., 2008; Ziagova et al., 2007), or using the functional microbes with specific materials to accelerate the heavy metal removal efficiency (Zhao et al., 2017). However, because of different cellular structure and associated functions (Vijayaraghavan and Yun, 2008), the efficiency and mechanisms of bio-sorption may vary among different microbial species (Say et al., 2003; Ziagova et al., 2007; Guo et al., 2010; Shim et al., 2015). As to bio-sorption mechanisms, various phospho-wall acids and 8–10 nm thick polysaccharide in the cell wall of gram-positive and gram-negative bacteria, respectively, play important roles on cell sorption. They have strong negative charges and can adsorb metal ions, e.g., the remediation efficiency of Bacillus sp. EB L14 could be promoted through inhibiting the activities of ATPase (Guo et al., 2010; Xiao et al., 2010). Cd could also be chelated by the bio-surfactants secreted (Basu and Paul, 2008) or be fixed by silver based single crystals produced (Hassan et al., 2009) of microbial organisms, and reduce the toxic effects of Cd in environment. Except cell wall adsorption, PTHMS could also be accumulated inside the cells through various transport systems (Hewlett and Avery, 1997; Shim et al., 2015). However, mechanisms of removal and cell distribution of Cd on different microbial species remain unclear (Gadd, 2000; Sulaymon et al., 2013), which limit practical applications of the microremediation in situ.

In this study, three typical Cd-tolerant microbial strains including bacterial Pseudomonas stutzeri (Halder and Basu, 2016), Bacillus subtilis (Doyle et al., 1980; Kim et al., 2007) and fungal Hansenula anomala (Watanaben et al., 2009) were selected for studying the biosorption of Cd in solutions. The removal pattern and specific distribution of Cd in the different species were investigated in a gradient of Cd concentration solution. We used the SEM and EDS spectra to verify the Cd sorption on the surface of microcells, and analyzed the functional groups of cell sorption using FTIR spectra. Eventually, the mechanisms of biosorption of the different microbial species were discussed. We hope that our results could provide theoretical guidance for the practical application and facilitate the remediation efficiencies in situ conditions.

Section snippets

Preparation of strains, reagents and medium

P. stutzeri, B. subtilis and H. anomala were selected as target microbial species because they were reported to have Cd resistance (Doyle et al., 1980; Kim et al., 2007; Watanaben et al., 2009; Halder and Basu, 2016) and commonly existed in soil and water. The three strains of P. stutzeri 1.10279, B. subtilis 1.433 and H. anomala 2.0810 were purchased from Institute of Microbiology, Chinese Academy of Sciences. Specifically, the P. stutzeri and B. subtili were maintained and activated in LB

Effects of Cd concentrations on removal efficiencies of different microbial species

The removal efficiency of Cd was strongly microbial species and Cd concentrations depended (Table 1). The removal efficiency by the three microbial species decreased successively with increased Cd concentrations from 0.05, 0.5, 5 mg L−1 consistently (Fig. 1, Fig. S2 in Supplementary Materials), which was consistent with the previous studies (Bai et al., 2008; Panwichian et al., 2010). When Cd concentrations increased, the declining ratio of the Cd removal could mainly attribute to the lack of

Conclusion

Our study reveals the different potential biosorption mechanisms of three Cd-resistant microbial species of different categories including P. stutzeri, B. subtilis and H. anomala. The microbial strains could efficiently remove the Cd ions mainly through bio-sorption of cell wall and/or cytomembrane respectively, but the removal efficiencies were inversed association with the Cd concentrations. Therefore, we advocate that those high Cd-resistant strains to be used in soil or water remediation of

Acknowledgements

This work was financially supported by a grant from National Key Research and Development Plan (No. 2017YFD0801502).

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