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Pharmacological properties of some mangrove sediment-associated bacillus isolates

Archives of Microbiology volume 203, pages 67–76 (2021)Cite this article

Abstract

Mangrove sediment-associated bacteria are of significantly important in the field of medicine and pharmaceuticals as new promising sources of biologically active pharmacophores due to the extreme conditions, such as high salt concentration and soil anoxia. The sediment bacteria associated with Acanthus ilicifolius and Avicennia officinalis collected from the Mangalavanam mangrove ecosystem of the Kerala State of India were evaluated using various in vitro models for the assessment of their pharmacological properties. The bacteria exhibiting significant antioxidant and antimicrobial activities were isolated, identified, and characterized by the integrated microbiological, biochemical, and 16S rRNA sequencing. Among the varied bacteria isolated from mangrove sediments, Bacillus amyloliquefaciens MBMS5 (GenBank accession number MK765025) exhibited significant antimicrobial activities against various pathogenic bacteria, such as Aeromonas caviae, Vibrio parahemolyticus, and methicillin-resistant Staphylococcus aureus. The extracellular extracts of B. amyloliquefaciens MBMS5 exhibited potential antioxidant activity against free radical species coupled with anti-inflammatory property as displayed by the attenuation activity against pro-inflammatory 5-lipoxygenase.

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References

  • Abada E, Al-Fifi Z, Osman M (2019) Bioethanol production with carboxymethylcellulase of Pseudomonas poae using castor bean (Ricinus communis L.) cake. Saudi J Biol Sci 26(4):866–871

    CAS  Article  Google Scholar 

  • Amalaradjou M, Venkitanarayanan K (2014) Antibiofilm effect of octenidine hydrochloride on Staphylococcus aureus, MRSA and VRSA. Pathogens 3(2):404–416

    Article  Google Scholar 

  • Archer NK, Mazaitis MJ, Costerton JW, Leid JG, Powers ME, Shirtliff ME (2011) Staphylococcus aureus biofilms: properties, regulation, and roles in human disease. Virulence 2:445–459

    Article  Google Scholar 

  • Armstrong E, Yan L, Boyd KG, Wright PC, Burgess JG (2001) The symbiotic role of marine microbes on living surfaces. Hydrobiologia 461:37–40

    Article  Google Scholar 

  • Ayuso-Sacido A, Genilloud O (2005) New PCR primers for the screening of NRPS and PKS-I systems in actinomycetes: detection and distribution of these biosynthetic gene sequences in major taxonomic groups. Microb Ecol 49(1):10–24

    CAS  Article  Google Scholar 

  • Bandaranayake W (1995) Survey of mangrove plants from northern Australia for phytochemical constituents and UV-absorbing compounds. Curr Top Phytochem 14:69–78

    Google Scholar 

  • Baylac S, Racine P (2003) Inhibition of 5-lipoxygenase by essential oils and other natural fragrant extracts. Int J Aromather 13(2):138–142

    Article  Google Scholar 

  • Behera BC, Parida S, Dutta SK, Thatoi H (2014) Isolation and identification of cellulose degrading bacteria from mangrove soil of Mahanadi River Delta and their cellulase production ability. Am J Microbiol Res 2(1):41–46

    Article  Google Scholar 

  • Brand-Williams W, Cuvelier ME, Berset C (1995) Use of a free radical method to evaluate antioxidant activity. LWT-Food Sci Technol 28(1):25–30

    CAS  Article  Google Scholar 

  • Chakraborty K, Thilakan B, Raola VK (2014) Polyketide family of novel antibacterial 7-O-methyl-5′-hydroxy-3′-heptenoate–macrolactin from seaweed-associated Bacillus subtilis MTCC 10403. J Agric Food Chem 62(50):12194–12208

    CAS  Article  Google Scholar 

  • El-Helow ER (2001) Identification and molecular characterization of a novel Bacillus strain capable of degrading Tween-80. FEMS Microbiol Lett 196(2):119–122

    CAS  Article  Google Scholar 

  • Gilbert NC, Bartlett SG, Waight MT, Neau DB, Boeglin WE, Brash AR, Newcomer ME (2011) The structure of human 5-lipoxygenase. Science 331(6014):217–219

    CAS  Article  Google Scholar 

  • Goecke F, Labes A, Wiese J, Imhoff JF (2010) Chemical interactions between marine macroalgae and bacteria. Mar Ecol Prog Ser 409:267–300

    CAS  Article  Google Scholar 

  • Gram L, Melchiorsen J, Bruhn JB (2010) Antibacterial activity of marine culturable bacteria collected from a global sampling of ocean surface waters and surface swabs of marine organisms. Mar Biotechnol (NY) 12(4):439–451

    CAS  Article  Google Scholar 

  • Kimura M (1980) A simple method for estimating evolutionary rate of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16(2):111–120

    CAS  Article  Google Scholar 

  • Kizhakkekalam VK, Chakraborty K (2019) Pharmacological properties of marine macroalgae-associated heterotrophic bacteria. Arch Microbiol 201(4):505–518

    CAS  Article  Google Scholar 

  • Nandakumar R, Rush MC, Correa F (2007) Association of Burkholderia glumae and B. gladioli with panicle blight symptoms on rice in Panama. Plant Dis 91(6):767

    CAS  Article  Google Scholar 

  • Naragani K, Mangamuri U, Muvva V, Poda S, Munaganti RK (2016) Antimicrobial potential of Streptomyces cheonanensis VUK-a from mangrove origin. Int J Pharm Pharm Sci 8(3):53–57

    CAS  Google Scholar 

  • National Research Council (1999) From monsoons to microbes: understanding the ocean’s role in human health. The National Academics Press, Washington, DC. https://doi.org/10.7226/6368

    Book  Google Scholar 

  • Nei M, Kumar S (2000) Molecular evolution and phylogenetics. Oxford University Press, New York, p 348 (ISBN: 9780195135855)

    Google Scholar 

  • Okamura M, Shimazaki K, Nakata T, Chida N, Miyatake T, Maemoku H, Tsutsumi H, Nakamura T, Yamaguchi C, Ogawa M (1993) Submarine active faults in the northwestern part of Beppu Bay, Japan-on a new technique for submarine active fault survey. Mem Geol Soc Jpn 40:65–74

    Google Scholar 

  • Penesyan A, Kjelleberg S, Egan S (2010) Development of novel drugs from marine surface associated microorganisms. Mar Drugs 8(3):438–459

    CAS  Article  Google Scholar 

  • Prathiba S, Jayaraman G (2018) Evaluation of the anti-oxidant property and cytotoxic potential of the metabolites extracted from the bacterial isolates from mangrove forest and saltern regions of South India. Prep Biochem Biotechnol 48(8):750–758

    CAS  Article  Google Scholar 

  • Re R, Pellegrini N, Proteggente A, Pannala A, Yang M, Rice-Evans C (1999) Antioxidant activity applying an improved ABTS radical cation decolorization assay. Free Radic Biol Med 26(9–10):1231–1237

    CAS  Article  Google Scholar 

  • Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4(4):406–425

    CAS  Google Scholar 

  • Schirmer A, Gadkari R, Reeves CD, Ibrahim F, DeLong EF, Hutchinson CR (2005) Metagenomic analysis reveals diverse polyketide synthase gene clusters in microorganisms associated with the marine sponge Discodermia dissoluta. Appl Environ Microbiol 71(8):4840–4849

    CAS  Article  Google Scholar 

  • Scott J (2004) Pathophysiology and biochemistry of cardiovascular disease. Curr Opin Genet Dev 14(3):271–279

    CAS  Article  Google Scholar 

  • Ser HL, Palanisamy UD, Yin WF, Chan KG, Goh BH, Lee LH (2016) Streptomyces malaysiense sp. nov.: a novel Malaysian mangrove soil actinobacterium with antioxidative activity and cytotoxic potential against human cancer cell lines. Sci Rep 6:24247

    CAS  Article  Google Scholar 

  • Shahidi F (2000) Antioxidants in food and food antioxidants. Nahrung 44(3):158–163

    CAS  Article  Google Scholar 

  • Sostres C, Gargallo CJ, Arroyo MT, Lanas A (2010) Adverse effects of non-steroidal anti-inflammatory drugs (NSAIDs, aspirin and coxibs) on upper gastrointestinal tract. Best Pract Res Clin Gastroenterol 24(2):121–132

    CAS  Article  Google Scholar 

  • Suganthi C, Mageswari A, Karthikeyan S, Anbalagan M, Sivakumar A, Gothandam KM (2013) Screening and optimization of protease production from a halotolerant Bacillus licheniformis isolated from saltern sediments. J Genet Eng Biotechnol 11(1):47–52

    Article  Google Scholar 

  • Sun W, Wu W, Liu X, Zaleta-Pinet DA, Clark BR (2019) Bioactive compounds isolated from marine-derived microbes in China: 2009–2018. Mar Drugs 17(6):339

    CAS  Article  Google Scholar 

  • Tabbene O, Gharbi D, Slimene IB, Elkahoui S, Alfeddy MN, Cosette P, Mangoni ML, Jouenne T, Limam F (2012) Antioxidative and DNA protective effects of bacillomycin D-like lipopeptides produced by b-38 strain. Appl Biochem Biotechnol 168(8):2245–2256

    CAS  Article  Google Scholar 

  • Tamehiro N, Okamoto-Hosoya Y, Okamoto S, Ubukata M, Hamada M, Naganawa H, Ochi K (2002) Bacilysocin, a novel phospholipid antibiotic produced by Bacillus subtilis 168. Antimicrob Agents Chemother 46(2):315–320

    CAS  Article  Google Scholar 

  • Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30(12):2725–2729

    CAS  Article  Google Scholar 

  • Tang JS, Zhao F, Gao H, Dai Y, Yao ZH, Hong K, Li J, Ye WC, Yao XS (2010) Characterization and online detection of surfactin isomers based on HPLC-MS(n) analyses and their inhibitory effects on the overproduction of nitric oxide and the release of TNF-α and IL-6 in LPS-induced macrophages. Mar Drugs 8(10):2605–2618

    CAS  Article  Google Scholar 

  • Thilakan B, Chakraborty K, Chakraborty RD (2016) Antimicrobial properties of cultivable bacteria associated with seaweeds in the Gulf of Mannar on the southeast coast of India. Can J Microbiol 62(8):668–681

    CAS  Article  Google Scholar 

  • Thongjun J, Tansila N, Panthong K, Tanskul S, Nishibuchi M, Vuddhakul V (2016) Inhibitory potential of biosurfactants from Bacillus amyloliquefaciens derived from mangrove soil against Vibrio parahaemolyticus. Ann Microbiol 66(3):1257–1263

    CAS  Article  Google Scholar 

  • Thoppil RJ, Bishayee A (2011) Terpenoids as potential chemopreventive and therapeutic agents in liver cancer. World J Hepatol 3(9):228–249

    Article  Google Scholar 

  • Velho-Pereira S, Parvatkar P, Furtado I (2015) Evaluation of antioxidant producing potential of halophilic bacterial bionts from marine invertebrates. Indian J Pharm Sci 77(2):183–189

    CAS  Article  Google Scholar 

  • Yasmeen S, Muvva V, Munaganti RK (2016) Isolation and characterization of bioactive Streptomyces from mangrove ecosystem of Machilipatnam, Krishna district, Andhra Pradesh. Asian J Pharm Clin Res 9(3):258–263

    CAS  Google Scholar 

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Acknowledgements

This work was 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 are thankful to Indian Council of Agricultural Research (ICAR), New Delhi for providing facilities to carry out the work. 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, Thiruvananthapuram, 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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Author notes

  1. Lakshmi Rajan and Kajal Chakraborty contributed equally.

Authors and Affiliations

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

    Lakshmi Rajan & Kajal Chakraborty

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

    Lakshmi Rajan

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

    Rekha Devi Chakraborty

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  1. Lakshmi Rajan
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  2. Kajal Chakraborty
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  3. Rekha Devi Chakraborty
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Correspondence to Kajal Chakraborty.

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Human and animal rights statement

This article does not contain any studies with human participants or animals performed by any of the authors. Appropriate permissions were obtained from the responsible authorities for collecting mangrove sediments in the Mangalavanam Mangrove Ecosystem and Bird Sanctuary located in Kochi, Kerala at 9° 54′ N 76° 18′ E.

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Rajan, L., Chakraborty, K. & Chakraborty, R.D. Pharmacological properties of some mangrove sediment-associated bacillus isolates. Arch Microbiol 203, 67–76 (2021). https://doi.org/10.1007/s00203-020-01999-5

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  • DOI: https://doi.org/10.1007/s00203-020-01999-5

Keywords

  • Mangrove sediment-associated bacteria
  • Bacillus amyloliquefaciens MBMS5
  • Pharmacological properties
  • Antimicrobial
  • Antioxidant and anti-inflammatory activities