Volume 40 Issue 4
Jun.  2021
Turn off MathJax
Article Contents
Mohammad Abdulaziz Ba-akdah, Sathianeson Satheesh. Characterization and antifouling activity analysis of extracellular polymeric substances produced by an epibiotic bacterial strain Kocuria flava associated with the green macroalga Ulva lactuca[J]. Acta Oceanologica Sinica, 2021, 40(4): 107-115. doi: 10.1007/s13131-020-1694-x
Citation: Mohammad Abdulaziz Ba-akdah, Sathianeson Satheesh. Characterization and antifouling activity analysis of extracellular polymeric substances produced by an epibiotic bacterial strain Kocuria flava associated with the green macroalga Ulva lactuca[J]. Acta Oceanologica Sinica, 2021, 40(4): 107-115. doi: 10.1007/s13131-020-1694-x

Characterization and antifouling activity analysis of extracellular polymeric substances produced by an epibiotic bacterial strain Kocuria flava associated with the green macroalga Ulva lactuca

doi: 10.1007/s13131-020-1694-x
Funds:  The Deanship of Scientific Research of King Abdulaziz University under contract No. G-153-150-39.
More Information
  • Corresponding author: e-mail: ssathianeson@kau.edu.sa; satheesh_s2005@yahoo.co.in
  • Received Date: 2019-08-30
  • Accepted Date: 2020-02-22
  • Available Online: 2021-04-01
  • Publish Date: 2021-06-03
  • Extracellular polymeric substances (EPS) are present externally to the microorganisms and play an important role in attachment and biofilm formation. These polymers possess antibacterial and antifouling activities. In this study, the antifouling activity of EPS produced by an epibiotic bacterium associated with macroalga Ulva lactuca was assessed against fouling bacteria and barnacle larvae. Results indicate that the EPS isolated from the epibiotic bacterium inhibits the biofilm formation of the bacteria without much antibacterial activity. Also, the EPS reduced the settlement of barnacle larvae on the hard substrate under laboratory conditions. The epibiotic bacterium was identified as Kocuria flava based on 16S rRNA gene sequencing. The EPS was further analysed using Fourier transform infrared (FT-IR), nuclear magnetic resonance (NMR) and X-ray diffraction (XRD) to understand the biochemical composition. NMR analysis revealed the presence of polysaccharides, proteins, acetyl amine and succinyl groups. Scanning electron microscope analysis indicated that the EPS consisted of aggregated and irregular sphere-shaped particles.
  • loading
  • [1]
    Almeida J R, Correia-da-Silva M, Sousa E, et al. 2017. Antifouling potential of nature-inspired sulfated compounds. Scientific Reports, 7: 42424. doi: 10.1038/srep42424
    [2]
    Angelina, Vijayendra S V N. 2015. Microbial biopolymers: the exopolysaccharides. In: Kalia V C, ed. Microbial Factories. New Delhi: Springer, 113–125
    [3]
    Badireddy A R, Korpol B R, Chellam S, et al. 2008. Spectroscopic characterization of extracellular polymeric substances from Escherichia coli and Serratia marcescens: suppression using sub-inhibitory concentrations of bismuth thiols. Biomacromolecules, 9(11): 3079–3089. doi: 10.1021/bm800600p
    [4]
    Balqadi A A, Salama A J, Satheesh S. 2018. Microfouling development on artificial substrates deployed in the central Red Sea. Oceanologia, 60(2): 219–231. doi: 10.1016/j.oceano.2017.10.006
    [5]
    Bérdy J. 2005. Bioactive microbial metabolites. The Journal of Antibiotics, 58(1): 1–26. doi: 10.1038/ja.2005.1
    [6]
    Bibi F, Naseer M I, Hassan A M, et al. 2018. Diversity and antagonistic potential of bacteria isolated from marine grass Halodule uninervis. 3 Biotech, 8(1): 48. doi: 10.1007/s13205-017-1066-1
    [7]
    Brian-Jaisson F, Molmeret M, Fahs A, et al. 2016. Characterization and anti-biofilm activity of extracellular polymeric substances produced by the marine biofilm-forming bacterium Pseudoalteromonas ulvae strain TC14. Biofouling, 32(5): 547–560. doi: 10.1080/08927014.2016.1164845
    [8]
    Camacho-Chab J C, Lango-Reynoso F, Castañeda-Chávez M D R, et al. 2016. Implications of extracellular polymeric substance matrices of microbial habitats associated with coastal aquaculture systems. Water, 8(9): 369. doi: 10.3390/w8090369
    [9]
    Caruso C, Rizzo C, Mangano S, et al. 2018. Production and biotechnological potential of extracellular polymeric substances from sponge-associated Antarctic bacteria. Applied and Environmental Microbiology, 84(4): e01624–17. doi: 10.1128/AEM.01624-17
    [10]
    Casillo A, Lanzetta R, Parrilli M, et al. 2018. Exopolysaccharides from marine and marine extremophilic bacteria: structures, properties, ecological roles and applications. Marine Drugs, 16(2): 69. doi: 10.3390/md16020069
    [11]
    Coffey B M, Anderson G G. 2014. Biofilm formation in the 96-well microtiter plate. In: Filloux A, Ramos JL, eds. Pseudomonas Methods and Protocols. New York: Humana Press, 631–641, doi: 10.1007/978-1-4939-0473-0_48
    [12]
    Costerton J W, Lewandowski Z, Caldwell D E, et al. 1995. Microbial biofilms. Annual Review of Microbiology, 49: 711–745. doi: 10.1146/annurev.mi.49.100195.003431
    [13]
    De Siqueira Melo R, Brasil S L D C, De Carvalho L J, et al. 2016. Assessment of the antifouling effect of exopolysaccharides incorporated into copper oxide-based organic paint. International Journal of Electrochemical Science, 11(9): 7750–7763
    [14]
    Decho A W. 1990. Microbial exopolymer secretions in ocean environments: their role(s) in food webs and marine processes. Oceanography and Marine Biology, 28: 73–153
    [15]
    Delbarre-Ladrat C, Sinquin C, Lebellenger L, et al. 2014. Exopolysaccharides produced by marine bacteria and their applications as glycosaminoglycan-like molecules. Frontiers in Chemistry, 2: 85. doi: 10.3389/fchem.2014.00085
    [16]
    Dogan N M, Doganli G A, Dogan G, et al. 2015. Characterization of extracellular polysaccharides (EPS) produced by thermal Bacillus and determination of environmental conditions affecting exopolysaccharide production. International Journal of Environmental Research, 9(3): 1107–1116. doi: 10.22059/IJER.2015.998
    [17]
    Dubois M, Gilles K, Hamilton J K, et al. 1951. A colorimetric method for the determination of sugars. Nature, 168(4265): 167. doi: 10.1038/168167a0
    [18]
    Elbendary A A, Hessain A M, El-Hariri M D, et al. 2018. Isolation of antimicrobial producing Actinobacteria from soil samples. Saudi Journal of Biological Sciences, 25(1): 44–46. doi: 10.1016/j.sjbs.2017.05.003
    [19]
    Flemming H C, Neu T R, Wozniak D J. 2007. The EPS matrix: the “house of biofilm cells”. Journal of Bacteriology, 189(22): 7945–7947. doi: 10.1128/JB.00858-07
    [20]
    Gonzalez-Gil G, Thomas L, Emwas A H, et al. 2015. NMR and MALDI-TOF MS based characterization of exopolysaccharides in anaerobic microbial aggregates from full-scale reactors. Scientific Reports, 5: 14316. doi: 10.1038/srep14316
    [21]
    Gu Di, Jiao Yingchun, Wu Jianan, et al. 2017. Optimization of EPS production and characterization by a halophilic bacterium, Kocuria rosea ZJUQH from Chaka Salt Lake with response surface methodology. Molecules, 22(5): 814. doi: 10.3390/molecules22050814
    [22]
    He Jinzhe, Zhang Anqiang, Ru Qiaomei, et al. 2014. Structural characterization of a water-soluble polysaccharide from the fruiting bodies of Agaricus bisporus. International Journal of Molecular Sciences, 15(1): 787–797. doi: 10.3390/ijms15010787
    [23]
    Hwang G, Kang S, El-Din M G, et al. 2012. Impact of an extracellular polymeric substance (EPS) precoating on the initial adhesion of Burkholderia cepacia and Pseudomonas aeruginosa. Biofouling, 28(6): 525–538. doi: 10.1080/08927014.2012.694138
    [24]
    Jiang Peng, Li Jingbao, Han Feng, et al. 2011. Antibiofilm activity of an exopolysaccharide from marine bacterium Vibrio sp. QY101. PLoS One, 6(4): e18514. doi: 10.1371/journal.pone.0018514
    [25]
    Jiao Yongqin, Cody G D, Harding A K, et al. 2010. Characterization of extracellular polymeric substances from acidophilic microbial biofilms. Applied and Environmental Microbiology, 76(9): 2916–2922. doi: 10.1128/AEM.02289-09
    [26]
    Kanamarlapudi S L R K, Muddada S. 2017. Characterization of exopolysaccharide produced by Streptococcus thermophilus CC30. BioMed Research International, 2017: 4201809. doi: 10.1155/2017/4201809
    [27]
    Kavita K, Mishra A, Jha B. 2011. Isolation and physico-chemical characterisation of extracellular polymeric substances produced by the marine bacterium Vibrio parahaemolyticus. Biofouling, 27(3): 309–317. doi: 10.1080/08927014.2011.562605
    [28]
    Kavita K, Singh V K, Mishra A, et al. 2014. Characterisation and anti-biofilm activity of extracellular polymeric substances from Oceanobacillus iheyensis. Carbohydrate Polymers, 101: 29–35. doi: 10.1016/j.carbpol.2013.08.099
    [29]
    Lee M E, Lee H D, Suh H H. 2015. Production and characterization of extracellular polysaccharide produced by Pseudomonas sp. GP32. Journal of Life Science, 25(9): 1027–1035. doi: 10.5352/JLS.2015.25.9.1027
    [30]
    Lembre P, Lorentz C, Di Martino P. 2012. Exopolysaccharides of the biofilm matrix: a complex biophysical world. In: Karunaratne D N, ed. The Complex World of Polysaccharides. Croatia: IntechOpen, 371–392, doi: 10.5772/51213
    [31]
    Liu F C, Su C R, Wu T Y, et al. 2011. Efficient 1H-NMR quantitation and investigation of N-acetyl-D-glucosamine (GlcNAc) and N,N′-diacetylchitobiose (GlcNAc)2 from chitin. International Journal of Molecular Sciences, 12(9): 5828–5843. doi: 10.3390/ijms12095828
    [32]
    Mallick I, Bhattacharyya C, Mukherji S, et al. 2018. Effective rhizoinoculation and biofilm formation by arsenic immobilizing halophilic plant growth promoting bacteria (PGPB) isolated from mangrove rhizosphere: a step towards arsenic rhizoremediation. Science of the Total Environment, 610–611: 1239–1250. doi: 10.1016/j.scitotenv.2017.07.234
    [33]
    Maréchal J P, Hellio C. 2009. Challenges for the development of new non-toxic antifouling solutions. International Journal of Molecular Sciences, 10(11): 4623–4637. doi: 10.3390/ijms10114623
    [34]
    More T T, Yadav J S S, Yan S, et al. 2014. Extracellular polymeric substances of bacteria and their potential environmental applications. Journal of Environmental Management, 144: 1–25. doi: 10.1016/j.jenvman.2014.05.010
    [35]
    Palomo S, González I, De La Cruz M, et al. 2013. Sponge-derived Kocuria and Micrococcus spp. as sources of the new thiazolyl peptide antibiotic kocurin. Marine Drugs, 11(4): 1071–1086. doi: 10.3390/md11041071
    [36]
    Powell L C, Pritchard M F, Ferguson E L, et al. 2018. Targeted disruption of the extracellular polymeric network of Pseudomonas aeruginosa biofilms by alginate oligosaccharides. NPJ Biofilms and Microbiomes, 4: 13. doi: 10.1038/s41522-018-0056-3
    [37]
    Pradeepa, Shetty A D, Matthews K, et al. 2016. Multidrug resistant pathogenic bacterial biofilm inhibition by Lactobacillus plantarum exopolysaccharide. Bioactive Carbohydrates and Dietary Fibre, 8(1): 7–14. doi: 10.1016/j.bcdf.2016.06.002
    [38]
    Qian Peiyuan, Chen Lianguo, Xu Ying. 2013. Mini-review: molecular mechanisms of antifouling compounds. Biofouling, 29(4): 381–400. doi: 10.1080/08927014.2013.776546
    [39]
    Rajasree V, Sunjaiy Shankar C V, Satheesh S, et al. 2014. Biofilm inhibitory activity of extracellular polymeric substance produced by Exiguobacterium sp. associated with the polychaete Platynereis dumerilii. Thalassas, 30(2): 13–19
    [40]
    Rani R P, Anandharaj M, Sabhapathy P, et al. 2017. Physiochemical and biological characterization of novel exopolysaccharide produced by Bacillus tequilensis FR9 isolated from chicken. International Journal of Biological Macromolecules, 96: 1–10. doi: 10.1016/j.ijbiomac.2016.11.122
    [41]
    Ricou P, Pinel E, Juhasz N. 2005. Temperature experiments for improved accuracy in the calculation of polyamide-11 crystallinity by X-ray diffraction. In: International Centre for Diffraction Data, ed. Advances in X-ray Analysis, Vol 48. Newtown, Pennsylvania, USA: International Centre for Diffraction Data, 171–175
    [42]
    Salama A J, Satheesh S, Balqadi A A. 2018. Antifouling activities of methanolic extracts of three macroalgal species from the Red Sea. Journal of Applied Phycology, 30(3): 1943–1953. doi: 10.1007/s10811-017-1345-6
    [43]
    Satheesh S, Ba-akdah M A, Al-Sofyani A A. 2016. Natural antifouling compound production by microbes associated with marine macroorganisms—A review. Electronic Journal of Biotechnology, 21: 26–35. doi: 10.1016/j.ejbt.2016.02.002
    [44]
    Satheesh S, Soniamby A R, Shankar C V S, et al. 2012. Antifouling activities of marine bacteria associated with sponge (Sigmadocia sp.). Journal of Ocean University of China, 11(3): 354–360. doi: 10.1007/s11802-012-1927-5
    [45]
    Sayem S A, Manzo E, Ciavatta L, et al. 2011. Anti-biofilm activity of an exopolysaccharide from a sponge-associated strain of Bacillus licheniformis. Microbial Cell Factories, 10: 74. doi: 10.1186/1475-2859-10-74
    [46]
    Schultz M P, Bendick J A, Holm E R, et al. 2011. Economic impact of biofouling on a naval surface ship. Biofouling, 27(1): 87–98. doi: 10.1080/08927014.2010.542809
    [47]
    Shiyamala D S, Priya P, Sahadevan R. 2014. Pyrrolo [1, 2-A] Pyrazine-1,4-dione, hexahydro-3-(2-methylpropyl)- and phenol, 2,4-Bis (1,1-dimethy ethyl) novel antibacterial metabolites from a marine Kocuria sp. SRS88: optimization and its application in medical cotton gauze cloth against bacterial wound pathogens. International Journal of Pharmaceutical Research and Development, 6(2): 44–55
    [48]
    Solmaz K B, Ozcan Y, Mercan Dogan N, et al. 2018. Characterization and production of extracellular polysaccharides (EPS) by Bacillus pseudomycoides U10. Environments, 5(6): 63. doi: 10.3390/environments5060063
    [49]
    Sutherland I W. 2001. Biofilm exopolysaccharides: a strong and sticky framework. Microbiology, 147(1): 3–9. doi: 10.1099/00221287-147-1-3
    [50]
    Thomas K V, Brooks S. 2010. The environmental fate and effects of antifouling paint biocides. Biofouling, 26(1): 73–88. doi: 10.1080/08927010903216564
    [51]
    Tian Yu. 2008. Behaviour of bacterial extracellular polymeric substances from activated sludge: a review. International Journal of Environment and Pollution, 32(1): 78–89. doi: 10.1504/IJEP.2008.016900
    [52]
    Viju N, Satheesh S, Punitha S M J. 2016. Antibiofilm and antifouling activities of extracellular polymeric substances isolated from the bacteria associated with marine gastropod Turbo sp. Oceanological and Hydrobiological Studies, 45(1): 11–19. doi: 10.1515/ohs-2016-0002
    [53]
    Vliegenthart J F G, van Halbeek H, Dorland L. 1981. The applicability of 500-mhz high-resolution 1H-NMR spectroscopy for the structure determination of carbohydrates derived from glycoproteins. Pure and Applied Chemistry, 53(1): 45–77. doi: 10.1351/pac198153010045
    [54]
    Wang Chunlei, Fan Qiuping, Zhang Xiaofei, et al. 2018. Isolation, characterization, and pharmaceutical applications of an exopolysaccharide from Aerococcus Uriaeequi. Marine Drugs, 16(9): 337. doi: 10.3390/md16090337
    [55]
    Wang Kailing, Wu Zehong, Wang Yu, et al. 2017. Mini-review: antifouling natural products from marine microorganisms and their synthetic analogs. Marine Drugs, 15(9): 266. doi: 10.3390/md15090266
    [56]
    Wang Ji, Zhao Xiao, Tian Zheng, et al. 2015. Characterization of an exopolysaccharide produced by Lactobacillus plantarum YW11 isolated from Tibet Kefir. Carbohydrate Polymers, 125: 16–25. doi: 10.1016/j.carbpol.2015.03.003
    [57]
    Wu Shimei, Liu Geihua, Jin Wengyuan, et al. 2016. Antibiofilm and anti-infection of a marine bacterial exopolysaccharide against Pseudomonas aeruginosa. Frontiers in Microbiology, 7: 102. doi: 10.3389/fmicb.2016.00102
    [58]
    Yadav V, Prappulla S G, Jha A, et al. 2011. A novel exopolysaccharide from probiotic Lactobacillus fermentum CFR 2195: Production, purification and characterization. Biotechnology and Bioengineering, 1(4): 415–421
    [59]
    Yang L H, Miao Li, Lee O O, et al. 2007. Effect of culture conditions on antifouling compound production of a sponge-associated fungus. Applied Microbiology and Biotechnology, 74(6): 1221–1231. doi: 10.1007/s00253-006-0780-0
    [60]
    Yildiz H, Karatas N. 2018. Microbial exopolysaccharides: resources and bioactive properties. Process Biochemistry, 72: 41–46. doi: 10.1016/j.procbio.2018.06.009
    [61]
    Zhang Li, Liu Chunhong, Li Da, et al. 2013. Antioxidant activity of an exopolysaccharide isolated from Lactobacillus plantarum C88. International Journal of Biological Macromolecules, 54: 270–275. doi: 10.1016/j.ijbiomac.2012.12.037
  • 加载中

Catalog

    通讯作者: 陈斌, bchen63@163.com
    • 1. 

      沈阳化工大学材料科学与工程学院 沈阳 110142

    1. 本站搜索
    2. 百度学术搜索
    3. 万方数据库搜索
    4. CNKI搜索

    Figures(7)  / Tables(2)

    Article Metrics

    Article views (821) PDF downloads(17) Cited by()
    Proportional views
    Related

    /

    DownLoad:  Full-Size Img  PowerPoint
    Return
    Return