Theobroma cacao L. agricultural soils with natural low and high cadmium (Cd) in Santander (Colombia), contain a persistent shared bacterial composition shaped by multiple soil variables and bacterial isolates highly resistant to Cd concentrations

Curr Res Microb Sci. 2021 Nov 29;2:100086. doi: 10.1016/j.crmicr.2021.100086. eCollection 2021 Dec.

ABSTRACT

Heavy metals can be found in soil as natural components or as product of contaminations events; plants growing in soils are prone to bioaccumulate heavy metals on their biomass. Theobroma cacao L. can bioaccumulate cadmium (Cd) in the seed and could be in derived food products, it considered a human health risk; therefore, removal of Cd is desirable but not vet technically and economically feasible; only to avoid Cd in cocoa is by selecting lands plots exhibiting lower Cd concentrations in soils, imposing a serious limitation to farmers and regulators. The study of bacterial communities and isolation bacteria with tolerance and mechanisms to counteract the translocation of Cd to the parts of cocoa plant exhibits high relevance in Colombia economy and especially to companies producing chocolate and derivatives. Here, we explore bacterial communities associated with soils having relatively high natural Cd concentrations in a large agricultural cocoa plot located in the Santander region. We characterized the bacterial communities’ compositions by amplicon 16S rRNA sequencing from metagenomics soil DNA and by culturing-based enumeration and isolation approaches. Culture-dependent techniques allowed the isolation of bacteria tolerant to Cd concentration, complement the information for Colombia, and expand the number of strains characterized with adaptive capacity against Cd with tolerance in a concentration of 120 mg/L, which represents the first capacity for Exiguobacterium sp., Ralstonia sp., Serratia sp., Dermacoccus sp., Klebsiella sp., Lactococcus sp. and Staphylococcus sp. In addition to confirming that there is a greater diversity of Cd-tolerant bacteria present in soils of farms cultivated with cocoa in Colombia. As for the results of new generation sequencing, they revealed that, the alpha-diversity in bacterial composition, according to the ANOVA, there are statistically significant differences of the bacterial communities present in the samples. Regarding Pearson correlation analysis, it was found the Shannon Simpson indices, have a positive correlation against OM, C, pH, Mn, C.E.C.I., Ca, P and negatively correlated with S; respect to bacterial community structure, a principal component analysis, which revealed that independent of the concentration of Cd present in soil samples, separates them according to pH value. Phyla to high abundance relative in all samples were Proteobacteria, Acidobacteriota, Actinobacteriota, Verrucomicrobiota, Myxococcota, Chloroflexi, Plactomycetota, Bacteroidota, Gemmatimonadota, Nitrospirota, Firmicutes and NB1_J; the bacteria genera with higher relative abundance (>0.5%) Nitrospira, candidatus Udaeobacter, Haliangium, Cupriavidus, MND1, Bacillus, Kitasatospora, Niveibacterium, Acidothermus, Burkholderia, Acidibacter, Terrimonas, Gaiella, candidatus Solibacter, Kitasatospora, Sphingomonas, Streptomyces, this genus with a relationship with the Cd tolerance process. After it, redundancy analysis was performed between the variation of the bacterial communities identified by dependent and independent techniques and edaphic soil variables, where their positive correlation was found against K, OM, C, Ca, pH (p<0.01) and P, C.E.C.I (p<0.05). For soil samples, the bacterial genera that make up the core community were identified, which are present in all samples as Nitrospira sp., Cupriavidus sp., Burkholderia sp., Haliangium sp., candidatus Udaeobacter, MND1, Kitasatospora, Acidothermus, Acidibacter, Streptomyces, Gaiella, candidatus Solibacter and Terramonas; the genera identified has a different and fundamental role in ecosystem functioning. The combination of different approaches offers new clues regarding the assessment of bacterial communities in soils cultivated with cocoa in soils with elevated Cd content in Colombia, and the ecological role and interplay of soil components and bacterial communities that contribute to modulate the effect of bioaccumulation in products.

PMID:34927107 | PMC:PMC8649583 | DOI:10.1016/j.crmicr.2021.100086

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