Arbuscular Mycorrhizal Fungi, Bacillus cereus, and Candida parapsilosis from a Multicontaminated Soil Alleviate Metal Toxicity in Plants

Abstract

We investigated if the limited development of Trifolium repens growing in a heavy metal (HM) multicontaminated soil was increased by selected native microorganisms, bacteria (Bacillus cereus (Bc)), yeast (Candida parapsilosis (Cp)), or arbuscular mycorrhizal fungi (AMF), used either as single or dual inoculants. These microbial inoculants were assayed to ascertain whether the selection of HM-tolerant microorganisms can benefit plant growth and nutrient uptake and depress HM acquisition. The inoculated microorganisms, particularly in dual associations, increased plant biomass by 148% (Bc), 162%, (Cp), and 204% (AMF), concomitantly producing the highest symbiotic (AMF colonisation and nodulation) rates. The lack of AMF colonisation and nodulation in plants growing in this natural, polluted soil was compensated by adapted microbial inoculants. The metal bioaccumulation abilities of the inoculated microorganisms and particularly the microbial effect on decreasing metal concentrations in shoot biomass seem to be involved in such effects. Regarding microbial HM tolerance, the activities of antioxidant enzymes known to play an important role in cell protection by alleviating cellular oxidative damage, such as superoxide dismutase, catalase, glutathione reductase, and ascorbate peroxidase, were here considered as an index of microbial metal tolerance. Enzymatic mechanisms slightly changed in the HM-adapted B. cereus or C. parapsilosis in the presence of metals. Antioxidants seem to be directly involved in the adaptative microbial response and survival in HM-polluted sites. Microbial inoculations showed a bioremediation potential and helped plants to develop in the multicontaminated soil. Thus, they could be used as a biotechnological tool to improve plant development in HM-contaminated environments.