Abstract

The effects of cadmium (Cd) contamination on the microbial community structure, soil physicochemistry and heavy metal resistome of a tropical agricultural soil were evaluated in field-moist soil microcosms. A Cd-contaminated agricultural soil (SL5) and an untreated control (SL4) were compared over a period of 5 weeks. Analysis of the physicochemical properties and heavy metals content of the two microcosms revealed a statistically significant decrease in value of the soil physicochemical parameters (P < 0.05) and concentration of heavy metals (Cd, Pb, Cr, Zn, Fe, Cu, Se) content of the agricultural soil in SL5 microcosm. Illumina shotgun sequencing of the DNA extracted from the two microcosms showed the predominance of the phyla, classes, genera and species of Proteobacteria (37.38%), Actinobacteria (35.02%), Prevotella (6.93%), and Conexibacter woesei (8.93%) in SL4, and Proteobacteria (50.50%), Alphaproteobacteria (22.28%), Methylobacterium (9.14%), and Methylobacterium radiotolerans (12,80%) in SL5, respectively. Statistically significant (P < 0.05) difference between the metagenomes was observed at genus and species delineations. Functional annotation of the two metagenomes revealed diverse heavy metal resistome for the uptake, transport, efflux and detoxification of various heavy metals. It also revealed the exclusive detection in SL5 metagenome of members of RND (resistance nodulation division) protein czcCBA efflux system (czcA, czrA, czrB), CDF (cation diffusion facilitator) transporters (czcD), and genes for enzymes that protect the microbial cells against cadmium stress (sodA, sodB, ahpC). The results obtained in this study showed that Cd contamination significantly affects the soil microbial community structure and function, modifies the heavy metal resistome, alters the soil physicochemistry and results in massive loss of some autochthonous members of the community not adapted to the Cd stress.

Highlights

  • Cadmium (Cd) is a highly toxic, carcinogenic heavy metal with an exceptionally high biological half-life (> 20 years) and propensity for accumulation in the food chain, drinking water and soil (Benavides et al 2005; Khan et al 2015; Fashola et al 2016)

  • Statistical analysis of the physicochemical parameters of the two metagenomes revealed that the difference is statistically significant (P < 0.05; P = 0.036)

  • While the concentrations of lead (0.02 ± 0.002 mg/kg), selenium (0.006 ± 0.001 mg/ kg), and Cd (0.15 ± 0.001 mg/kg) detected in the agricultural soil are considerably low, high concentrations of zinc, iron, copper, and chromium were detected in the agricultural soil SL4

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Summary

Introduction

Cadmium (Cd) is a highly toxic, carcinogenic heavy metal with an exceptionally high biological half-life (> 20 years) and propensity for accumulation in the food chain, drinking water and soil (Benavides et al 2005; Khan et al 2015; Fashola et al 2016). Cd toxicity to microbial cells is believed to be due to depletion of glutathione and sulfhydryl groups in proteins, interaction with nucleic acids, oxidative damage by production of reactive oxygen species, and inactivation of metalloproteins due to displacement of Zn and Fe ions (Vallee and Ulmer 1972; Stohs and Bagchi 1995; Fortuniak et al 1996; Stohs et al 2001; Banjerdkij et al 2005) This result in protein denaturation, cell membrane and nucleic acid disruption, and inhibition of transcription, cell division and enzyme activities (Fashola et al 2016). Cd cytotoxicity has been implicated in destruction of plant mitochondria as well as disruption of photosynthesis and transpiration (Imai and Siegel 1973; Toppi and Gabbrielli 1999; Lopez-Milla’n et al 2009; Mohamed et al 2012; Júnior et al 2014; Khan et al 2016a, b)

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