Skip to main content
SpringerLink
Log in

Bacterial diversity of a floating vegetation (Phumdi) of Loktak Lake and its extracellular enzymes and bacterial antagonistic property

  • Original Paper
  • Published:
Archives of Microbiology Aims and scope Submit manuscript

Abstract

134 bacterial strains were isolated from phumdis of Loktak Lake. Through 16S rRNA sequencing, Bacillus sp. (23, 17.1%), Staphylococcus sp. (14, 10.4%), Pseudomonas sp. (11, 8.2%) and Acinetobacter sp. (8, 5.9%) were identified as the predominant bacterial taxa of Loktak Lake. B. pumulis (12, 8.9%), S. arlettae (4, 2.9%), P. knackmussii (6, 4.4%) are the leading species of Bacillus, Staphylococcus and Pseudomonas, respectively. Similarly, A. seifertii (2, 1.4%) and A. calcoaceticus (2, 1.4%) are the common species of Acinetobacter. 75 (55.9%) bacterial strains showed the ability to hydrolyze one or more extracellular enzymes tested. Among the extracellular enzymes produced by the bacterial isolates, the presence of elastase activity cannot be underestimated, since the enzyme is involved in the process of bacterial lung infection. Phosphate solubilizing activity could be seen in 11.1% of the bacterial isolates. 27 (20.1%) of the strains shown to have antagonistic activity against one or more tested pathogens. An isolate, MRC 52 showed antagonistic activity against eleven different pathogens including carbapenem resistant E. coli which was further subjected to extraction and identification of the biomolecule exerting the antimicrobial property. Based on GC–MS analysis, the bioactive compound was identified as phenyl ethyl alcohol.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

Data availability

The data sets generated during and/or analysed during the current study are available in the manuscript.

References

  • Adhikari NP, Adhikari S, Liu X et al (2019) Bacterial Diversity in Alpine Lakes: A Review from the Third Pole Region. J Earth Sci 30:387–396. https://doi.org/10.1007/s12583-018-1206-5

    Article  CAS  Google Scholar 

  • Agnieszka K, Maria SB (2013) Extracellular enzymatic activities in subsurface water of eutrophic Lake Chelmzynskie, Poland. J Freshw Ecol 4:517–527

    Google Scholar 

  • Ariffin H, Hassan MA, Shah UKM et al (2006) Production and characterization of cellulase by Bacillus pumilus EB3. Int J Eng Technol 3:47–53. https://doi.org/10.1263/jbb.106.231PMid:18929997

    Article  Google Scholar 

  • Bartosz K, Ryszard C, Tomasz K, Waldemar S et al (2019) Structural and functional microbial diversity along a eutrophication gradient of interconnected Lakes undergoing anthropopressure. Sci Rep 9:11144

    Article  Google Scholar 

  • Berrah G, Wkonetzka A (1962) Selective and reversible inhibition of the synthesis of bacterial deoxyribonucleic acid by phenethyl alcohol. J Bacteriol 83:738–744

    Article  CAS  Google Scholar 

  • Berrazeg M, Diene S, Medjahed L et al. (2014) New Delhi Metallo-beta-lactamase around the world: an eReview using Google Maps. Euro Surveill 19:pii20809. http://www.eurosurveillance.org/ViewArticle.aspx?ArticleId20809. doi:https://doi.org/10.2807/1560-7917.es2014.19.20.20809

  • Blanco JL, Hontecillas R, Bouza E et al (2002) Correlation between the elastase activity index and invasiveness of clinical isolates of Aspergillus fumigatus. J Clin Microbiol 40:1811–1813

    Article  CAS  Google Scholar 

  • Chen TC, Levin RE (1974) Taxonomic Significance of Phenethyl Alcohol Production by Achromobacter isolates from fishery sources. Appl Microbiol 28:681–687

    Article  CAS  Google Scholar 

  • Ciccarelli FD, Doerks T, von Mering C, Creevey CJ, Snel B, Bork P (2006) Toward automatic reconstruction of a highly resolved tree of life. Science 311(5765):1283–1287. https://doi.org/10.1126/science.1123061 (Erratum.In:Science.5;312(5774):697 PMID: 16513982)

    Article  CAS  PubMed  Google Scholar 

  • Corre J, Lucchini JJ, Mercier GM, Cremieux A (1990) Antibacterial activity of phenethyl alcohol and resulting membrane alterations. Res Microbiol 141:483–497. https://doi.org/10.1016/0923-2508(90)90074-Z

    Article  CAS  PubMed  Google Scholar 

  • Dana LD, Bauder JW (2011) A General Essay on Bioremediation of Contaminated Soil. Montana State University, Bozeman, Mont, USA

    Google Scholar 

  • Desjardine K, Pereira A, Wright H, Matainaho T, Kelly M, Andersen RJ (2007) Tauramamide, a lipopeptide antibiotic produced in culture by Brewibacillus laterosporus isolated from a marine habitat: structure elucidation and synthesis. J Nat Prod 70:1850–1853

    Article  CAS  Google Scholar 

  • Dua MAS, Sethunathan N, Johri A (2002) Biotechnology and bioremediation: successes and limitations. Appl Microbiol Biotechnol 59:143–152

    Article  CAS  Google Scholar 

  • El-Gendy MMA, Hawas UW, Jaspars M (2008) Novel bioactive metabolites from a marine derived bacterium Nocardia sp. ALAA 2000. J Antibiot 61:379–386. https://doi.org/10.1038/ja.2008.53

    Article  CAS  Google Scholar 

  • Ferdaouss E, Habil A, Saida A, Abderrazak R, Amin L, Mohammed B, Abdelhay A (2017) Screening of phosphate solubilizing bacterial isolates for improving growth of wheat. Eur J Biotechnol Biosci 6:07–11

    Google Scholar 

  • Fischbach MA, Walsh CT (2009) Antibiotics for emerging pathogens. Science 325:1089e93. https://doi.org/10.1126/science.1176667

    Article  CAS  Google Scholar 

  • Fraud S, Rees EL, Mahenthiralingam E, Russell AD, Maillard JY (2003) Aromatic alcohols and their effect on Gram-negative bacteria, cocci and mycobacteria. J Antimicrob Chemother 51:1435–1436. https://doi.org/10.1093/jac/dkg246

    Article  CAS  PubMed  Google Scholar 

  • Hilda R, Reynaldo F (1999) Phosphate solubilizing bacteria and their role in plant growth promotion. Biotechnol Adv 17:319–339

    Article  Google Scholar 

  • Kiersztyn B, Siuda W, Chrost RJ (2002) Microbial ectoenzyme activity: useful parameters for characterizing the trophic conditions of Lakes. Pol J Environ Stud 11:367–373

    CAS  Google Scholar 

  • Kumar S, Stecher G, Li M, Knyaz C, Tamura K (2018) MEGA X: Molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol 35:1547–1549. https://doi.org/10.1093/molbev/msy096

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kumar G, Lhingjakim KL, Uppada J, Ahamad S, Kumar D, Kashif GM, Sasikala C, Ramana CV (2021) Aquisphaera insulae sp. nov., a new member in the family Isosphaeraceae, isolated from the floating island of Loktak Lake and emended description of the genus Aquisphaera. Antonie Van Leeuwenhoek 114:1465–1477. https://doi.org/10.1007/s10482-021-01615-6 (Epub 2021 Jul 14 PMID: 34259976)

    Article  CAS  PubMed  Google Scholar 

  • Leung M (2004) Bioremediation: techniques for cleaning up a mess. J Biotechnol 2:18–22

    Google Scholar 

  • Lilley BO, Brewer JH (1953) The selective antibacterial action of phenethyl alcohol. J Am Pharm Assoc Sci Ed 42:6–8

    Article  CAS  Google Scholar 

  • Macherla VR, Liu J, Sunga M, White DJ, Grodberg J, Teisan S, Kin SL, Barbara CMP (2007) Lipoxazolidinones A, B, and C: antibacterial 4-Oxazolidinones from a marine actinomycete isolated from a Guam marine sediment. J Nat Prod 70:1454–1457

    Article  CAS  Google Scholar 

  • Magaldi S, Mata-Essayag S, Hartung de Capriles C (2004) Well diffusion for antifungal susceptibility testing. Int J Infect Dis 8:39–45

    Article  CAS  Google Scholar 

  • Massimiliano F, Anna MG, Belen JJ, Jesus GL (2007) Screening for extracellular enzyme activities by bacteria isolated from samples collected in the Tyrrhenian Sea. Ann Microbiol 57:93–99

    Article  Google Scholar 

  • Motsim B, Matiullah K, Asghari B et al (2019) Phosphorus and phosphate solubilizing bacteria: Keys for sustainable agriculture. Geomicrobiol J 36:904–916. https://doi.org/10.1080/01490451.2019.1654043

    Article  CAS  Google Scholar 

  • Muhire BM, Varsani A, Martin DP (2014) SDT: A Virus Classification Tool Based on Pairwise Sequence Alignment and Identity Calculation. PLoS ONE 9(9):e108277. https://doi.org/10.1371/journal.pone.0108277

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Newton RJ, Jones SE, Eiler A et al (2011) A guide to the natural history of freshwater Lake bacteria. Microbiol Mol Biol Rev: MMBR 75:14–49

    Article  CAS  Google Scholar 

  • Ngashangva N, Mukherjee P, Sharma KC, Kalita MC, Indira S (2021) Analysis of antimicrobial peptide metabolome of bacterial endophyte isolated from traditionally used medicinal plant Millettia pachycarpa benth. Front Microbiol 1(12):656896. https://doi.org/10.3389/fmicb.2021.656896 (PMID:34149644;PMCID:PMC8208310)

    Article  Google Scholar 

  • Payne DJ, Gwynn MN, Holmes DJ, Pompliano DL (2007) Drugs for bad bugs: confronting the challenges of antibacterial discovery. Nat Rev Drug Discov 6:29e40. https://doi.org/10.1038/nrd2201

    Article  CAS  Google Scholar 

  • Pikovskaya RI (1948) Mobilization of phosphorus in soil in connection with the vital activity of some microbial species. Mikrobiologiya 17:362–370

    CAS  Google Scholar 

  • Politano VT, Diener RM, Christian MS, Hoberman AM, Palmer A, Ritacco G, Adams TB, Api AM (2013) Oral and dermal developmental toxicity studies of phenylethyl alcohol in rats. Toxicol 32:32–38. https://doi.org/10.1177/1091581812461811

    Article  CAS  Google Scholar 

  • Puranik S, Pal RR, More RP, Purohit HJ (2016) Metagenomic approach to characterize soil microbial diversity of Phumdi at Loktak Lake. Water Sci Technol 74:2075–2086. https://doi.org/10.2166/wst.2016.370

    Article  PubMed  Google Scholar 

  • Sanchez M, Colom F (2010) Extracellular DNase activity of Cryptococcus neoformans and Cryptococcus gatti. Rev Iberoam Micol 27:10–13

    Article  Google Scholar 

  • Sanjotha G, Sudheer M (2016) Isolation, screening and characterization of phosphate solubilizing bacteria from Karwar costal region. Int J Res Stud Microbiol Biotechnol 2:1–6

    Google Scholar 

  • Sehnaz A, Sevtap A (2008) Investigation of extracellular elastase, acid proteinase and phospholipase activities as putative virulence factors in clinical isolates of Aspergillus species. J Basic Microbiol 48:331–337

    Article  Google Scholar 

  • Sharma J, Singh A, Kumar R, Mittal A (2006) Partial purification of an alkaline protease from a new strain of Aspergillus oryzae AW T20 and its enhanced stabilization in entrapped Ca – Alginate beads. The Int J Microbiol 2(2).

  • Silva MT, Sousa JCF, Macedo MAE, Polonia J, Ana MP (1976) Effects of phenethyl alcohol on Bacillus and Streptococcus. J Bacteriol 127:1359–1369

    Article  CAS  Google Scholar 

  • Simon S, Louis W (1967) Mechanism of action of phenethyl alcohol: Breakdown of the cellular permeability barrier. J Bacteriol 93:560–566

    Article  Google Scholar 

  • Stone MM, DeForest JL, Plante AF (2014) Changes in extracellular enzyme activity and microbial community structure with soil depth at the Luquillo Critical Zone Observatory. Soil Biol Biochem 75:237–247

    Article  CAS  Google Scholar 

  • Tamura Y, Suzuki S, Sawada T (1992) Role of elastase as a virulence factor in experimental Pseudomonas aeruginosa infection in mice. Microb Pathog 12:237–244

    Article  CAS  Google Scholar 

  • Tang X, Xie G, Shao K et al (2021) Aquatic Bacterial Diversity, Community Composition and Assembly in the Semi-Arid Inner Mongolia Plateau: Combined Effects of Salinity and Nutrient Levels. Microorganisms. 9(2):208. https://doi.org/10.3390/microorganisms9020208 (PMID: 33498349; PMCID: PMC7909399)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Trisuwan K, Rukachaisirikul V, Sukpondma Y, Phongpaichit S, Preedanon S, Sakayaroj J (2009) Lactone derivatives from the marine-derived fungus Penicillium sp. PSU-F44. Chem Pharm Bull 57:1100–1102. https://doi.org/10.1248/cpb.57.1100

    Article  CAS  Google Scholar 

  • Valan AM, Duraipandiyan V, Agastian P, Ignacimuthu S (2008) Antimicrobial activity of Streptomyces sp. ERI-26 recovered from Western Ghats of Tamil Nadu. J Mycol Med 18:147e53. https://doi.org/10.1016/j.mycmed.2008.07.004

    Article  Google Scholar 

  • Vidali M (2001) Bioremediation: an overview. Pure Appl Chem 7:1163–1172

    Article  Google Scholar 

  • Vijayshree SG, Shivaramu MS, Damare SR, Pujitha D, Meena RM, Shenoy BD (2019) Diversity and extracellular enzyme activities of heterotrophic bacteria from sediments of the Central Indian Ocean Basin. Sci Rep 9(1):9403. https://doi.org/10.1038/s41598-019-45792-x (PMID: 31253859; PMCID: PMC6599205)

    Article  CAS  Google Scholar 

  • Wang Y, Hua-Fang S, Yan H et al (2012) Comparison of the levels of bacterial diversity in freshwater, intertidal wetland, and marine sediments by using millions of Illumina Tags. Appl Environ Microbiol 78:8264–8271. https://doi.org/10.1128/AEM.01821-12

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wilson JRJ, Lyall J, Mcbride RJ, Murray JB, Smith G (1981) Partition coefficients of some aromatic alcohols in an n-heptane/water system and their relationship to minimum inhibitory concentration against Pseudomonas aeruginosa and Staphylococcus aureus. J Clin Hosp Phar 6:63–66

    CAS  Google Scholar 

  • Zhang B, He PJ, Lu F, Shao LM, Wang P (2007) Extracellular enzyme activities during regulated hydrolysis of high-solid organic wastes. Water Res 41:4468–4478

    Article  CAS  Google Scholar 

  • Zinger L, Linda AAZ, Jed AF, M. et al (2011) Global patterns of bacterial beta-diversity in seafloor and seawater ecosystems. PLoSOne 6:e24570. https://doi.org/10.1371/journal.pone.0024570

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We would like to thank the Department of Biotechnology (DBT), Govt. of India for the financial support. The authors also thank Prof. Khumanthem Sulochana Devi, Professor, Dept. of Microbiology, Regional Institute of Medical Sciences, Impha-795004, Manipur, India for providing clinical bacterial strains.

Funding

This work was supported by Department of Biotechnology (DBT), Ministry of Science and Technology, Govt. of India.

Author information

Authors and Affiliations

  1. Microbial Resources Division, Institute of Bioresources and Sustainable Development (IBSD), Takyelpat, Imphal, 795001, Manipur, India

    Jusna Nandeibam, Y Randhir Babu Singh, K Chandradev Sharma & S Indira Devi

  2. Phyto Pharmaceutical Laboratory, Institute of Bioresources and Sustainable Development (IBSD), Takyelpat, Imphal, 795001, Manipur, India

    Pulok Kumar Mukherjee

  3. Department of Microbiology, Regional Institute of Medical Sciences, Imphal, 795004, Manipur, India

    Kh. Ranjana Devi

Authors
  1. Jusna Nandeibam
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Y Randhir Babu Singh
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. K Chandradev Sharma
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Kh. Ranjana Devi
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Pulok Kumar Mukherjee
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. S Indira Devi
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

JN: isolation of bacteria, DNA extraction and 16S rRNA sequencing. RBSY: extracellular enzymes, antagonistic activity, analysis and interpretation of data, manuscript preparation. CSK: extraction of biomolecules and analysis. K.RD: concepts and guidance. IDS: concepts, analysis and interpretations, manuscript preparation. All authors read and approved the final manuscript.

Corresponding author

Correspondence to S Indira Devi.

Ethics declarations

Conflict of interests

The authors have no relevant financial or non-financial interests to disclose.

Ethics approval

This is an observational study. The Institute Research Ethics Committee (IBSD) has confirmed that no ethical approval is required.

Consent to participate

Not applicable, since no human participants was involve.

Consent to publish

Not applicable, since no human participants was involve.

Additional information

Communicated by Erko Stackebrandt.

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 32 KB)

Rights and permissions

Springer Nature or its licensor holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Nandeibam, J., Singh, Y.R.B., Sharma, K.C. et al. Bacterial diversity of a floating vegetation (Phumdi) of Loktak Lake and its extracellular enzymes and bacterial antagonistic property. Arch Microbiol 204, 657 (2022). https://doi.org/10.1007/s00203-022-03267-0

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s00203-022-03267-0

Keywords

Search

Navigation