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Evaluation of Metal Tolerance of Fungal Strains Isolated from Contaminated Mining Soil of Nanjing, China

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Evaluation of Metal Tolerance of Fungal Strains Isolated from Contaminated Mining Soil of Nanjing, China biology Article Evaluation of Metal Tolerance of Fungal Strains Isolated from Contaminated Mining Soil of Nanjing, China Fiza Liaquat 1, Muhammad Farooq Hussain Munis 2, Urooj Haroon 2, Samiah Arif 1, Saddam Saqib 3,4 , Wajid Zaman 3,4 , Ali Raza Khan 5, Jianxin Shi 6 , Shengquan Che 7 and Qunlu Liu 7,* 1 School of Agriculture and Biology, Shanghai Jiao Tong University, Shanghai 200240, China; fi[email protected] (F.L.); [email protected] (S.A.) 2 Department of Plant Sciences, Faculty of Biological Sciences, Quaid-i-Azam University, Islamabad 45320, Pakistan; [email protected] (M.F.H.M.); [email protected] (U.H.) 3 State Key Laboratory of Systematic and Evolutionary Botany, Institute of Botany, Chinese Academy of Sciences, Beijing 100093, China; [email protected] (S.S.); [email protected] (W.Z.) 4 University of Chinese Academy of Sciences, Beijing 100049, China 5 Zhejiang Key Lab of Crop Germplasm, Department of Agronomy, College of Agriculture and Biotechnology, Zhejiang University, Hangzhou 310058, China; [email protected] 6 Joint International Research Laboratory of Metabolic and Developmental Sciences, School of Life Science and Biotechnology, Shanghai Jiao Tong University, Shanghai 200240, China; [email protected] 7 Department of Landscape Architecture, School of Design, Shanghai Jiao Tong University, Shanghai 200240, China; [email protected] * Correspondence: [email protected]; Tel.: +86-2134205736 Received: 28 October 2020; Accepted: 8 December 2020; Published: 15 December 2020 Simple Summary: In this study, cadmium, chromium, and lead tolerant microbes have been isolated from contaminated mining soil and characterized. Molecular characterization of isolated fungi was performed and amplified sequences were deposited in the GenBank NCBI database. Metal tolerance of the various strains has been determined by measuring the minimum inhibitory concentrations (MICs) and the tolerance indexes of all the tested strains against Cd, Cr, and Pb. Bioaccumulation capacities of Trichoderma harzianum and Komagataella phaffi have also been assessed. These findings helped us find a novel strain of Komagataella phaffi and suggested it to be the potential mycoremediation microbe to alleviate the contamination of Cd, Cr, and Pb. Future studies of this fungal strain can help us to understand its resistance mechanism against other heavy metals, too. Abstract: Rapidly increasing industry has resulted in greater discharge of hazardous chemicals in the soil. In the current study, soil samples were collected from Nanjing mine (32◦09019.2900 N 118◦56057.0400 E) and subjected to heavy metal analysis and microbe isolation. A total of 460 fungi were isolated, and five of these were yeast strains. Most of the strains exhibited tolerance to one metal. Five multimetal tolerant strains were selected and identified as Aspergillus sclerotiorum, Aspergillus aculeatus, Komagataella phaffii, Trichoderma harzianum, and Aspergillus niger. Isolated strains were grown in high concentrations of cadmium (Cd), chromium (Cr) and lead (Pb), for induced-tolerance training. The tolerance index (TI) revealed the highest Cd tolerance of novel K. phaffii strain at 5500 ppm (TI: 0.2). K. phaffii also displayed resistance at 4000 ppm against Cr (TI: 0.32) and Pb (TI: 0.32). In contrast, tolerance training for A. niger was not that successful. K. phaffii also displayed the highest bioaccumulation capacity for Cd (25.23 mg/g), Cu (21.63 mg/g), and Pb (20.63 mg/g) at 200 ppm. Scanning electron microscopy (SEM) explored the morphological changes in the mycelia of stressed fungi. Results of this study describe this delicate approach to be species and metal dependent and suggest a potential utilization of this fungal strain for the bioremediation of contaminated soils. Biology 2020, 9, 469; doi:10.3390/biology9120469 www.mdpi.com/journal/biology Biology 2020, 9, 469 2 of 12 Keywords: heavy metals; Komagataella phaffii; tolerance index; Cd; Cr; Pb; bioaccumulation capacity 1. Introduction Industrialization has resulted in increasing heavy metal contamination in the soil and its remediation is one of the biggest challenges of this century. Due to different industrial activities, metal pollutants are released into the soil and environment where various living organisms are being affected. Heavy metals are usually released and deposited in the soils with industrial wastes [1]. Plants need essential metals such as zinc, copper, iron, and manganese for proper growth. Non-essential metals including cadmium, lead, and mercury impose toxic effects on plant morphology [2]. Industrial soils contain high quantities of cadmium and lead which are very toxic to the environment [3]. Previously, chemical methods were adopted to remove soil toxicity such as utilizing electric fields, use of ammonium bicarbonate, and EDTA washing. [4]. Recently, researchers found that fungal species possess significant potential to absorb toxic compounds, such as heavy metals from soil, in an eco-friendly way [5,6]. Previously, various techniques such as precipitation and ion exchange have been applied to remove heavy metals from wastewaters [7]. These techniques have many limitations—for example, potential of chemical decline over time and not being able to remove heavy metals [8]. Moreover, removing heavy metals from soil is an even more difficult task. In this situation, biological approaches can rescue plants from heavy metals. Biological approaches include the use of living organisms such as plants, bacteria, and fungi [9]. Microorganisms absorb pollutants and they can survive under metal stress due to their innate adsorption capability [10]. In addition, the potential of microbes to oxidize various inorganic elements through oxidative phosphorylation facilitates this process. Mycoremediation refers to the utilization of lower or higher fungi for the remediation of heavy metals and it has been fascinating to researchers for the last few decades [11,12]. From an industrial perspective, fungal colonization is very important because fungi possess thermotolerant and pH tolerant extremophilic enzymes [13]. The significant difficulties in the mycoremediation of fields include the bulk production of fungal inoculum, the use of right inoculum in the soil, and the determination of appropriate transporter material [14]. Mycoremediation of Chromium (Cr) and Nickel (Ni) has been reported in many fungal species such as Penicillium and Aspergillus [15–17]. Fungal species can efficiently remove heavy metals from the soil. Scientists are working on understanding remediation mechanism of these microbes. Many studies describe that the microbes possess biosorption or bioaccumulation ability and can bind metals on their surfaces. Few studies have also described the involvement of genes such as hydrohobin in imparting metal tolerance ability to different fungi [18]. Similar bioremediation mechanisms of Rhizopus spp., Penicillium spp., Trichoderma spp., and Aspergillus spp. have been described earlier [19,20]. Through the process of biosorption, Penicillium simplicissimum can remove Copper (Cu) and Lead (Pb) in liquid media [21]. Trichoderma asperellum can tolerate Cadmium (Cd), Pb, Zinc (Zn), Cu, and Chromium (Cr) through a biosorption mechanism [20]. Some studies describe that the gradual exposure of microbes to high metal concentrations results in enhanced metal tolerance and increases their capability to eliminate heavy metals [16]. Along with other microbes, yeast is also an important ubiquitous microbe for the potential bioremediation of heavy metals [22]. The present study was designed to isolate microbes from the contaminated mine soil of the Nanjing area. This study further assessed the influence of toxic metals (Cr, Cd, and Pb) on the development of these isolates and determined their metal bioaccumulation capacities. The toxic effects of selected heavy metals, on the morphology of isolates, were observed through scanning electron microscopy (SEM). Biology 2020, 9, x FOR PEER REVIEW 3 of 12 The toxic effects of selected heavy metals, on the morphology of isolates, were observed through scanning electron microscopy (SEM). Biology 2020, 9, 469 3 of 12 2. Materials and Methods 2. Materials and Methods 2.1. Sample Collection 2.1. Sample Collection To evaluateTo the evaluate tolerance the tolerance potential potential of different of different isolates isolates against against heavy heavy metals (Cr, (Cr, Cd, Cd, and and Pb), Pb), six soil samplessix soil were samples collected were collected from Nanjing from Nanjing mine mine (32°09 (32◦09′19.29019.29″ 00NN 118°56 118◦560′57.0457.0400″E) E) (Figure (Figure1). Soil 1). Soil samples weresamples taken were from taken the fromdepth the of depth 0~30 of cm 0~30 and cm andprocessed processed within within 8 8 h. h. After the the collection collection of soil of soil samples, thesesamples, were thesekept wereon dry kept ice on and dry ice further and further used used to isolate to isolate fungi. fungi. Figure 1. Location of studied area (Nanjing mine). 2.2. Processing of SoilFigure Samples 1. Location of studied area (Nanjing mine). Stones, coarse material, and other debris were removed. The air-dried soil samples were grounded 2.2. Processinginto of powderSoil Samples and sieved through a 2 mm sieve. The processed soils were used for heavy metal analysis. Stones, 2.3.coarse Heavy material, Metal Analysis and other debris were removed. The air-dried soil samples were grounded into powderFor this analysis,and sieved 0.5 g through of soil samples a 2 mm were sieve. weighted
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