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Inducible boron resistance via active efflux in Lysinibacillus and Enterococcus isolates from boron-contaminated agricultural soil

Abstract

Phylogenetically diverse bacteria tolerate high boron concentrations while others require it for metabolic purposes despite the metalloid being toxic beyond a threshold. Boron resistance and plant growth promoting attributes of two bacterial strains, Lysinibacillus sp. OL1 and a novel Enterococcus sp. OL5, isolated from boron-fertilizer-amended cauliflower fields were investigated in this study. OL1 and OL5 grew efficiently in the presence of 210–230 mM boron, and resistance was found to be inducible by small amounts of the element: 5 to 50 mM boron pre-exposure progressively shortened the lag phase of growth in the presence of 200 mM boron. Intracellular boron accumulation was also found to be regulated by the level of pre-exposure: no induction or induction by small amounts led to higher levels of intracellular accumulation, whereas induction by high concentrations led to lower accumulation. These data, in the context of the strains’ overall resistance towards 200 mM boron, indicated that induction by higher boron concentrations turned potential efflux mechanisms on, while resistance was eventually achieved by continuous cellular entry and exit of the ions. Involvement of solute efflux in boron resistance was corroborated by the genome content of the isolates (genes encoding proteins of the ATP-binding cassette, major facilitator, small multidrug resistance, multi antimicrobial extrusion, and resistance-nodulation-cell division, family/superfamily). Bacteria such as OL1 and OL5, which resist boron via influx-efflux, potentially lower boron bioavailability, and therefore toxicity, for the soil microbiota at large. These bacteria, by virtue of their plant-growth-promoting attributes, can also be used as biofertilizers.

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Acknowledgements

Authors sincerely thank the Department of Science and Technology (DST), Government of India as one of the author; Subhajit Sen received research grants through INSPIRE Fellowship vide sanction order DST/INSPIRE Fellowship/2016/IF160786. Nibendu Mondal received fellowships from Science and Engineering Research Board, Government of India and Bose Institute.

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Correspondence to Ranadhir Chakraborty.

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Sen, S., Mondal, N., Ghosh, W. et al. Inducible boron resistance via active efflux in Lysinibacillus and Enterococcus isolates from boron-contaminated agricultural soil. Biometals 35, 215–228 (2022). https://doi.org/10.1007/s10534-021-00359-0

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  • DOI: https://doi.org/10.1007/s10534-021-00359-0

Keywords

  • Boron resistance
  • Influx/efflux mechanism
  • Enterococcus
  • Lysinibacillus
  • Genome analysis