Abstract
High concentrations of non-essential heavy metals/metalloids (arsenic, cadmium, and lead) in soils and irrigation water represent a threat to the environment, food safety, and human and animal health. Microbial bioremediation has emerged as a promising strategy to reduce the concentration of heavy metals in the environment due to the demonstrated ability of microorganisms, especially bacteria, to sequester and transform these compounds. Although several bacterial strains have been reported to be capable of remediation of soils affected by heavy metals, published information has not been comprehensively analyzed to date to recommend the most efficient microbial resources for application in bioremediation or bacterial-assisted phytoremediation strategies that may help improve plant growth and yield in contaminated soils. In this study, we critically analyzed eighty-five research articles published over the past 15 years, focusing on bacteria-assisted remediation strategies for the non-essential heavy metals, arsenic, cadmium, and lead, and selected based on four criteria: i) The bacterial species studied are part of a plant microbiome, i.e., they interact closely with a plant species ii) these same bacterial species exhibit plant growth-promoting characteristics, iii) bacterial resistance to the metal(s) is expressed in terms of the Minimum Inhibitory Concentration (MIC), and iv) metal resistance is related to biochemical or molecular mechanisms. A total of sixty-two bacterial genera, comprising 424 bacterial species/strains associated with fifty plant species were included in our analysis. Our results showed a close relationship between the tolerance level exhibited by the bacteria and metal identity, with lower MIC values found for cadmium and lead, while resistance to arsenic was widespread and significantly higher. In-depth analysis of the most commonly evaluated genera, Agrobacterium, Bacillus, Klebsiella, Enterobacter, Microbacterium, Pseudomonas, Rhodococcus, and Mesorhizobium showed significantly different tolerance levels among them and highlighted the deployment of different biochemical and molecular mechanisms associated with plant growth promotion or with the presence of resistance genes located in the cad and ars operons. In particular, the genera Klebsiella and Enterobacter exhibited the highest levels of cadmium and lead tolerance, clearly supported by molecular and biochemical mechanisms; they were also able to mitigate plant growth inhibition under phytotoxic metal concentrations. These results position Klebsiella and Enterobacter as the best potential candidates for bioremediation and bacteria-assisted phytoremediation strategies in soils contaminated with arsenic, cadmium, and lead.
Highlights
Soil pollution by heavy metals represents a threat to the environment and food security due to the fast growth of industry and agriculture, and the disruption of natural ecosystems by anthropogenic pressure linked to the growth of human populations (Sarwar et al, 2017)
This study aims to characterize and select genera associated with the plant microbiome with potential for bioremediation or bacteria-assisted phytoremediation strategies of soils contaminated with arsenic, cadmium, and lead, through a literature review and an analysis of the metal-tolerance level of bacteria in terms of the Minimum Inhibitory Concentration (MIC) and the biochemical and molecular mechanisms they use to deal with toxicity by these metals
Different factors affect the form and toxicity of metals, these include pH, the concentration of chelating agents, the concentration of inorganic anions, and competition from other cations; many natural and synthetic chelating agents can reduce the toxicity of heavy metals and it has been theorized that MIC values vary with the type of media used, since components of bacterial growth media can form a complex with heavy metals, remove them from solution, and reduce their concentrations in the media (Kumar et al, 2013; Aljerf and AlMasri, 2018)
Summary
Soil pollution by heavy metals represents a threat to the environment and food security due to the fast growth of industry and agriculture, and the disruption of natural ecosystems by anthropogenic pressure linked to the growth of human populations (Sarwar et al, 2017). The second group comprises arsenic, cadmium, lead, mercury, plutonium, tungsten, and vanadium; non-essential metals that constitute potent toxins and enter the cells/tissues thanks to their physicochemical properties, like ionic charge (Duce and Bush, 2010; Johri et al, 2010). The latter, deserve special attention since they do not have any essential function in living organisms, are highly toxic at low exposure levels, and are considered as the main threat to life forms (Atobatele and Olutona, 2015). The United States Agency for Toxic Substances and Disease Registry (ATSDR) lists more than 20 heavy metals with pronounced toxicity but four are of particular concern to human health; arsenic (As), lead (Pb), cadmium (Cd) and mercury (Hg); out of these four, arsenic is the most common cause of acute heavy metal poisoning and ranked number 1 on ATSDR’s “top 20 list”, lead is number 2 on the list and cadmium ranks in seventh place (Fay and Mumtaz, 1996; Flora et al, 2011); arsenic, cadmium and lead are objects of study in this paper
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