Assessment of hexavalent chromium (VI) biosorption competence of indigenous Aspergillus tubingensis AF3 isolated from bauxite mine tailing

Highlights

• Autochthonous Aspergillus tubingensis AF3 is an indigenous species from bauxite mine soil.

• Shows better resistance against Cr (1500 μg mL), Cu (600 μg mL), Pb (500 μg mL), and Zn (500 μg mL).

• Growth conditions (25 °C, pH 7.0, 0.5% of dextrose & 12 days) optimized for effective adsorption.

• Effectively reduced Cr as 74.4% than other metals and sequestered on mycelium surface.

• The cell wall of the chromium treated A. tubingensis AF3 contains primary amines and alkanes.

Abstract

The intention of this research was to find the most eminent metal tolerant and absorbing autochthonous fungal species from the waste dump of a bauxite mine. Out of the 4 (BI-1, BI-II, BI-III, and BI-IV) predominant isolates, BI-II had an excellent metal tolerance potential against most of the metals in the subsequent order: Cr(VI) (1500), Cu(II) (600), Pb(II) (500), and Zn(II) (500–1500 μg mL⁻¹). BI-II had shown tolerance to Cr(VI) up to 1500 mg L⁻¹. The excellent metal tolerant isolate was characterized and identified as Aspergillus tubingensis AF3 through 18S rRNA sequencing method and submitted to GenBank and received an accession number (MN901243). A. tubingensis AF3 had the efficiency to absorb Cr(VI) and Cu(II) at <70 & 46.3% respectively under the standard growth conditions. Under the optimized conditions (25 °C, pH 7.0, 0.5% of dextrose, and 12 days of incubation), A. tubingensis AF3 absorbed 74.48% of Cr(VI) in 12 days (reduction occurred as 822.3, 719.13, 296.66, and 255.2 mg L⁻¹ of Cr(VI) on the 3^rd, the 6^th, the 9^th and the 12^th day, respectively). The adsorbed metal was sequestered in the mycelia of the fungus in a precipitated form; it was confirmed by Scanning Electron Microscope (SEM) and Energy Dispersive X-ray analysis (EDX) analyses. The possible biosorption mechanisms were analyzed by Fourier-Transform Infrared Spectroscopy (FTIR) analysis, the results showed the presence of N–H primary amines (1649.98 cm⁻¹) and Alkanes (914.30 cm⁻¹) in the cell wall of the fungus, while being treated with Cr(VI) they supported and enhanced the Cr(VI) absorption. The entire results concluded that the biomass of A. tubingensis AF3 had the potential to absorb a high concentration of Cr(VI).

Introduction

In recent years, the environmental pollution caused by the modern industrialization has been creating a serious threat to both the prokaryotic and the eukaryotic organisms (Ryu et al., 2019). The heavy metals are a serious concern because of their toxicity in soil and their mobility from the surface of the water to the depth (Chen et al., 2019). The waste released from the mining and smelting industries cause soil and water pollution to the nearby sites and the water pools (Lavanya et al., 2019). The heavy metals are persisting in the form of cations or anions, mostly as salts or oxides and are crossing the permissible limits (Kim et al., 2017) as defined by the World Health Organization (WHO). Metals such as arsenic, copper, chromium, cadmium, mercury, nickel, lead, and zinc are considered as heavy metals. Among those, chromium (VI) is highly soluble in water, carcinogenic, highly toxic to humans and animals, and is largely exposed to the environment through industries such as leather, mining, steel, textile, etc. (Irazusta et al., 2018). The uptake of chromium leads to oxidative stress and DNA damage, which cause cancer cells and the death of the healthy cells (Pugazhendhi et al., 2018; Liu et al., 2020).

Numerous conventional methods, such as Bio piles, Bioventing, Bio slurping, chemical precipitation, electro dialysis, ion exchange, photo catalysis, stabilization, and nitrification have been used for the removal of metals from the contaminated soil and water resources (Banerjee et al., 2019). Though the said physicochemical methods are cost-effective, they cause secondary pollution during the treatment process (Javaid et al., 2011). Microorganisms are the best choice and they are capable of removing any kind of metal in a polluted environment (Lavanya et al., 2019). Generally, the microbes, which grow in such a metal polluted environment interact with the metals by different methods e.g. absorption, adsorption, biotransformation, bioleaching, and bioaccumulation (Liu et al., 2020). Adsorption is an effective method for the removal of contaminants from a polluted environment (Vale et al., 2016). The adsorption method is widely accepted for the following positive views such as the experimental setup is very simple, reproducible, a wide range of adsorbent materials, which are effective and cheap, can be used (Majumder et al., 2017). There are several absorbents available but nowadays, the attention has been directed towards biological adsorbents because of their easy availability and ecofriendly nature (Roy et al., 2020). Among the biological adsorbents, microorganisms have gained the attention of the researchers. In the extreme environmental conditions, nature allows only a specific set of strong microbial communities to live in the environment with acquired genetic resistance (Ryu et al., 2019; Liu et al., 2020). The researchers state that the microbes (fungi) are a potential biological candidate for the bioremediation of heavy metals due to their rapid hyphal growth, which provides a mechanical support to bind and degrade the contaminants’ large surface area to produce enzymes (Mukherjee et al., 2016; Pant et al., 2020) and other extracellular polymeric substances to degrade the pollutants (Pugazhendhi et al., 2018; Zhang et al., 2018). Several studies have been undertaken on the metal biosorption mechanism with the live and dead fungal biomass such as Aspergillus sp., Fusarium sp., Mucor sp., Rhizopus sp., Saccharomyces sp. etc. (Verma et al., 2016; Karthik et al., 2017b). The aforementioned studies showed that the living fungal biomass could take up the metal ions by the cell wall and extracellular substances and also could bioaccumulate the ions into the intracellular compounds (Mahapatra et al., 2020; Kieliszek et al., 2015); but in the case of dead biomass, the absorption took place only by the extracellular ways (Hu et al., 2019; Wang et al., 2019).

In particular, Aspergillus sp. was the most preferred organism by several researchers for the remediation of any pollutant that occurred in the environment because of its filamentous, ubiquitous, fast growing nature and it could be easily isolated from different ecological habitats (Ma et al., 2017; Wang et al., 2019). The Aspergillus species such as A. niger (Ghorai et al., 2013), A. fumigatus, A. flavus, etc. (Morales-Barrera and Cristiani-Urbina, 2008; Oladipo et al., 2016) were extensively studied for metal (Cd, Cu, Pb, As, Cr, and Fe) tolerance and removal purposes on a variety of environmentally polluted sites such as gold and gemstone mining (Owlad et al., 2009; Karthik et al., 2017a; Liu et al., 2020). This study is the foremost approach to assess indigenous fungi metal absorption competence isolated from the tailing of a bauxite mine, Kolli hills of Namakkal district of Tamil Nadu, India. According to the foresaid information, the work was designed to enumerate the metal tolerant and absorb predominant fungus species from bauxite mine tailing and assess its biosorption competence on the metal absorption (biosorption) process under optimized conditions (In-vitro).