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Marine macroalga-associated heterotrophic Bacillus velezensis: a novel antimicrobial agent with siderophore mode of action against drug-resistant nosocomial pathogens

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Abstract

Increased prevalence of microbial resistance and development of drug-resistant pathogens have triggered an urge among researchers to discover potential antimicrobial compounds, particularly from the marine habitat. The present study highlights the cultivable diversity and bioactivities of heterotrophic bacteria associated with marine macroalgae of southeast Indian coastal region. Culture-dependent isolation method resulted in 40 isolates, in which greater part of the isolates represented Gammaproteobacteria (62%) followed by that comprised of the phylum Firmicutes. One of the most active strains isolated from a macroalga, Laurencia papillosa, was characterized based on the integrated phenotypic and genotypic analysis as Bacillus velezensis MBTDLP1 MTCC 13048, with an inhibition zone of about 35 mm against methicillin-resistant Staphylococcus aureus (MRSA), was selected for bioprospecting studies. Type-I pks gene (MT394492) of 700 bp could be amplified from the heterotrophic B. velezensis. The bacterium exhibited siderophore production and possessed genes implicated in the biosynthesis of siderophore type of metabolites exhibiting 99% similarity with other GenBank sequences in BLAST search. B. velezensis exhibited promising anti-infective properties against methicillin-resistant Staphylococcus aureus (minimum inhibitory concentration 15 µg/mL), and the activities were positively correlated (r2 > 0.9) with iron-chelating activities. Chemical investigation of the organic extract of B. velezensis MBTDLP1 characterized a macrocyclic polyketide exhibiting prospective antibacterial potential against methicillin-resistant S. aureus (MIC 0.38 µg/mL), than that exhibited by positive control chloramphenicol (6.25 µg/mL). Significant antibacterial activity against drug-resistant bacteria combined with the presence of genes coding for bioactive secondary metabolites revealed that this marine symbiotic bacterium could be used against emerging antibiotic resistance.

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Acknowledgements

This work was funded by the Indian Council of Agricultural Research (ICAR) under the project titled as “Development of Bioactive Pharmacophores from Marine Organisms” (Grant Number MBT/HLT/SUB23). The research was partly funded by the College of Agriculture of Kerala Agricultural University, India under the B.Sc.–M.Sc. (Integrated) Biotechnology programme (Grant No. 2014-09-103). The authors thank the Director, Central Marine Fisheries Research Institute, Course Director [B.Sc.–M.Sc. (Integrated) Biotechnology programme] and Head, Department of Plant Biotechnology, College of Agriculture, Kerala Agricultural University, Thiruvanthapuram, for providing with necessary support. Thanks are due to the Head, Marine Biotechnology Division, Central Marine Fisheries Research Institute for facilitating the research activities.

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  1. Marine Biotechnology Division, Central Marine Fisheries Research Institute, P.B. No. 1603, Ernakulam North, Cochin, India

    Kajal Chakraborty, Aneetta Francis, Sumayya Asharaf, Vinaya Kizhakkepatt Kizhakkekalam & Silpa Kunnappilly Paulose

  2. Department of Plant Biotechnology, College of Agriculture, Kerala Agricultural University, Vellayani, Thiruvanthapuram, 695522, India

    Aneetta Francis

  3. Crustacean Fisheries Division, Central Marine Fisheries Research Institute, P.B. No. 1603, Ernakulam North, Cochin, India

    Rekha Devi Chakraborty

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  1. Kajal Chakraborty
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KC and AF conceived and designed research, acquired funds, and conducted experiments. KC, RDC, SA, and VKK analyzed data. KC, RDC, SKP, and VKK drafted the manuscript. All authors read and approved the manuscript.

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Correspondence to Kajal Chakraborty.

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Chakraborty, K., Francis, A., Chakraborty, R.D. et al. Marine macroalga-associated heterotrophic Bacillus velezensis: a novel antimicrobial agent with siderophore mode of action against drug-resistant nosocomial pathogens. Arch Microbiol 203, 5561–5575 (2021). https://doi.org/10.1007/s00203-021-02513-1

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