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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.

Plant endophytic bacteria have received special attention in recent decades for their ability to improve plant response to multiple stresses. A positive effect of endophytes on plant’s ability to cope with drought, salinity, nitrogen deficiency, and pathogens have already been demonstrated in numerous studies, and recently this evidence was consolidated in a meta-analysis of published data. Endophytic bacteria have also been implicated in increasing resistance to heavy metals in plants; despite the important biotechnological applications of such effect in heavy metal bioremediation and agriculture, efforts to systematically analyze studies in this field have been limited. In this study, we address this task with the objective of establishing whether the findings made for other types of stresses extend to the response to heavy metals. Specifically, we seek to establish if plant inoculation with plant-growth promoting endophytic bacteria have an impact on their tolerance to heavy metal stress? We carried out a meta-analysis of the effect size of inoculation with endophytic bacteria on the host plant biomass in response to heavy metal stress (aluminum, arsenic, cadmium, copper, chromium, manganese, nickel, lead, and zinc), which included 27 (from 76 published in the last 10 years) studies under controlled conditions that evaluated 19 host plants and 20 bacterial genera. Our results suggest that endophytic bacteria increase the biomass production of host plants subjected to different heavy metals, indicating their effectiveness in protecting plants from a wide range of metal toxicities. Stress mitigation by the bacteria was similar among the different plant groups with the exception of non-accumulating plants that benefit most from the symbiotic association. Host identity and heavy metal concentration seem to influence the effect of the bacteria. Our analysis revealed that bacterial consortia provide the greatest benefit although the most common biotechnological applications are not directed towards them, and support the value of endophytic bacteria as an alternative to mitigate heavy metal stress in a wide variety of hosts.