Abstract
Purpose
The marine environment harbours diverse bacterial species which can be exploited for the production of valuable compounds such as exopolysaccharides (EPS) which hold promises for biotechnological applications. The coastal waters of Mauritius is a relatively underexplored marine environment and in this study, isolated bacterial species were tested for the production of EPS exhibiting antibacterial properties against human bacterial pathogens from the genera Acinetobacter, Bacillus, Campylobacter, Enterobacter, Enterococcus, Escherichia, Proteus, Pseudomonas, Salmonella, Streptococcus and Staphylococcus.
Methods
Bacteria were first isolated from seawater samples. Using the disc diffusion method, their EPS were tested for antibacterial effects through two screenings, with each involving a different set of arbitrarily chosen group of pathogens. The microorganisms producing antibacterial EPS were subsequently identified by morphological, biochemical and 16S rRNA-based phylogenetic analyses. Those EPS exhibiting broadest antibacterial activities were eventually characterised by Fourier-transform infrared spectroscopy (FTIR) and thin-layer chromatography (TLC).
Results
Eight EPS were found to display antibacterial effects against more than half of the pathogens and the microorganisms producing them were identified as Bacillus, Halomonas, Psychrobacter and Alcaligenes species. However, only two of these EPS were found to be the most active, with their MIC values ranging between 62.5 and 500 μg/ml. FTIR and TLC analyses revealed the presence of carboxyl, hydroxyl and amide as well as sulphate for the EPS, with glucose or fructose being the main sugar.
Conclusion
The results suggest that Mauritius seawater can be a source of biotechnologically useful microorganisms, producing EPS having potential as antimicrobial agents. DNA sequence data also suggest possible novel bacterial species.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Change history
03 July 2019
In the above-mentioned paper, the wrong figure was provided for figure 6.
References
Al-Nahas MO, Darwish MM, Ali AE, Amin MA (2011) Characterization of an exopolysaccharide-producing marine bacterium, isolate Pseudoalteromonas sp. AM. Afr J Microbiol Res 5(22):3823–3831. https://doi.org/10.5897/AJMR11.757
Balouiri M, Sadiki M, Ibnsouda SK (2016) Methods for in vitro evaluating antimicrobial activity: a review. J Pharm Anal 6(2):71–79. https://doi.org/10.1016/j.jpha.2015.11.005
Balzaretti S, Taverniti V, Guglielmetti S, Fiore W, Minuzzo M, Ngo HN, Ngere JB, Sadiq S, Humphreys PN, Laws AP (2017) A novel rhamnose-rich heteroexopolysaccharide isolated from Lactobacillus paracasei DG activates THP-1 human monocytic cells. Appl Environ Microbiol 83(3):e02702–e02716. https://doi.org/10.1128/AEM.02702-16
Bragadeeswaran S, Jeevapriya R, Prabhu K, Rani SS, Priyadharsini S, Balasubramanian T (2011) Exopolysaccharide production by Bacillus cereus GU812900, a fouling marine bacterium. Afr J Microbiol Res 5(24):4124–4132. https://doi.org/10.5897/AJMR11.375
Brown L, Wolf JM, Rosales RP, Casadevall A (2015) Through the wall: extracellular vesicles in Gram-positive bacteria, mycobacteria and fungi. Nature Rev Microbiol 13(10):620–630. https://doi.org/10.1038/nrmicro3480
Byun BY, Lee S, Mah J (2014) Antipathogenic activity and preservative effect of levan (β-2,6-fructan), a multifunctional polysaccharide. Food Sci Technol 49:238–245. https://doi.org/10.1111/ijfs.12304
Ceuppens S, Boon N, Uyttendaele M (2013) Diversity of Bacillus cereus group strains is reflected in their broad range of pathogenicity and diverse ecological lifestyles. FEMS Microbiol Ecol 84(3):433–450. https://doi.org/10.1111/1574-6941.12110
Chalkiadakis E, Dufourcq R, Schmitt S, Brandily C, Kervarec N, Coatanea D, Amir H, Loubersac L, Chanteau S, Guezennec J, Rouzeyrol M, Colin C (2013) Partial characterization of an exopolysaccharide secreted by a marine bacterium, Vibrio neocaledonicus sp. nov., from New Caledonia. J Appl Microbiol 114(6):1702–1712. https://doi.org/10.1111/jam.12184
Chen M, Liang P (2017) Synthesis and antibacterial activity of quaternized curdlan. Polym Bulletin 74(10):4251–4266. https://doi.org/10.1007/s00289-017-1951-0
Choma A, Wiater A, Komaniecka I, Paduch R, Pleszczynska M, Szczodrak J (2013) Chemical characterization of a water insoluble (1→3)-α-D-glucan from an alkaline extract of Aspergillus wentii. Carbohydrates Pol 91(2):603–608. https://doi.org/10.1016/j.carbpol.2012.08.060
Chun J, Oren A, Ventosa A, Christensen H, Arahal DR, da Costa MS, Rooney AP, Yi H, Xu X, Meyer S, Trujillo ME (2018) Proposed minimal standards for the use of genome data for the taxonomy of prokaryotes. I J Syst Evol Microbiol 68:461–466. https://doi.org/10.1099/ijsem.0.002516
Cojoc R, Merciu S, Oancea P, Pincu E, Dumitru L, Enache M (2009) Highly thermostable exopolysaccharide produced by the moderately halophilic bacterium isolated from a man-made young salt lake in Romania. Polish J Microbiol 58(4):289–294 ISSN: 1733-1331
Collin C, Gueguen Y, Bachere E, Kouzayha A, Saulnier D, Gayet N, Guezennec J (2015) Use of natural antimicrobial peptides and bacterial biopolymers for cultured pearl production. Mar Drugs 13:3732–3744. https://doi.org/10.3390/md13063732
Dakheel KH, Rahim RA, Neela VK, Al-Obaidi JR, Hun TG, Yusoff K (2016) Methicillin-resistant Staphylococcus aureus biofilms and their influence on bacterial adhesion and cohesion. Biomed Res Int 2016:4708425. https://doi.org/10.1155/2016/4708425
Darriba D, Taboada GL, Doallo R, Posada D (2012) jModelTest 2: more models, new heuristics and parallel computing. Nat Methods 9(8):772. https://doi.org/10.1038/nmeth.2109
Debbab A, Aly AH, Lin WH, Proksch P (2010) Bioactive compounds from marine bacteria and fungi. Microb Biotechnol 3(5):544–563. https://doi.org/10.1111/j.1751-7915.2010.00179.x
Dinić M, Pecikoza U, Djokić J, Stepanović-Petrović R, Milenković M, Stevanović M, Filipović N, Begović J, Golić N, Lukić J (2018) Exopolysaccharide produced by probiotic strain Lactobacillus paraplantarum BGCG11 reduces inflammatory hyperalgesia in rats. Front Pharmacol 9(1). https://doi.org/10.3389/fphar.2018.00001
Du B, Yang Y, Bian Z, Xu B (2017) Characterization and anti-inflammatory potential of an exopolysaccharide from submerged mycelial culture of Schizophyllum commune. Front Pharmacol 8(252). https://doi.org/10.3389/fphar.2017.00252
Dubois M, Gilles KA, Hamilton JK, Rebers PA, Smith F (1956) Calorimetric method for determination of sugars and related substances. Anal Chem 28(3):350–356. https://doi.org/10.1021/ac60111a017
El Essawy AK, Abu Shady HM, Abu El Kher AM, Helal MM (2016) Antimicrobial, anticoagulation, fibrinolytic and prebiotic activities of exopolysaccharide produced by marine Klebsiella Sp. Egypt. J Exp Biol (Bot) 12(2):267–274. ISSN: 2090 – 0503. https://doi.org/10.5455/egyjebb.20161115114843
El-Deeb NM, Yassin AM, Al-Madboly LA, El-Hawiet A (2018) A novel purified Lactobacillus acidophilus 20079 exopolysaccharide, LA-EPS-20079, molecularly regulates both apoptotic and NF-κB inflammatory pathways in human colon cancer. Microb Cell Factories 17:29. https://doi.org/10.1186/s12934-018-0877-z
El-Naggar ME, Abdelgawad AM, Salas C, Rojas OJ (2016) Curdlan in fibers as carriers of tetracycline hydrochloride: controlled release and antibacterial activity. Carbohydr Polym 154(10):194–203. https://doi.org/10.1016/j.carbpol.2016.08.042
Eloff JN (1998) A sensitive and quick microplate method to determine the minimal inhibitory concentration of plant extracts for bacteria. Planta Med 64(8):711–713. https://doi.org/10.1055/s-2006-957563
Felsenstein J (1981) Evolutionary trees from DNA sequences: a maximum likelihood approach. J Mol Evol 17(6):368–376. https://doi.org/10.1007/BF01734359
Fitch WM (1971) Toward defining the course of evolution: minimum change for a specific tree topology. Syst Biol 20(4):406–416. https://doi.org/10.1093/sysbio/20.4.406
Frank JA, Reich CI, Sharma S, Weisbaum JS, Wilson BA, Olsen GJ (2008) Critical evaluation of two primers commonly used for amplification of bacterial 16S rRNA genes. Appl Environ Microbiol 74(8):2461–2470
Ghalem BR (2017) Antioxidant and antimicrobial activities of exopolysaccharides from yoghurt starter. Adv Biochem 5(5):97–101. https://doi.org/10.11648/j.ab.20170505.13
Goy RC, Britto D, Assis OBG (2009) A review of the antimicrobial activity of chitosan. Polímeros 19(3):241–247 ISSN 1678-5169
Gugliandolo C, Spanò A, Lentini V, Arena A, Maugeri TL (2014) Antiviral and immunomodulatory effects of a novel bacterial exopolysaccharide of shallow marine vent origin. J Appl Microbiol 116(4):1028–1034. https://doi.org/10.1111/jam.12422
Guindon S, Gascuel O (2003) A simple, fast and accurate method to estimate large phylogenies by maximum-likelihood. Syst Biol 52(5):696–704. https://doi.org/10.1080/10635150390235520
Guinebretière MH, Auger S, Galleron N, Contzen M, Sarrau B, De Buyser ML, Lamberet G, Fagerlund A, Granum PE, Lereclus D, De Vos P, Nguyen-The C, Sorokin A (2013) Bacillus cytotoxicus sp. nov. is a novel thermotolerant species of the Bacillus cereus group occasionally associated with food poisoning. I J Syst Evol Microbiol 63:31–40. https://doi.org/10.1099/ijs.0.030627-0
Gupta P, Diwan B (2017) Bacterial exopolysaccharide mediated heavy metal removal: a review on biosynthesis, mechanism and remediation strategies. Biotechnol Rep (Amst) 13:58–71. https://doi.org/10.1016/j.btre.2016.12.006
Heymann D, Velasco C, Chesneau J, Ratiskol J, Sinquin C, Jouault S (2016) Anti-metastatic properties of a marine bacterial exopolysaccharide-based derivative designed to mimic glycosaminoglycans. Molecules 21(3):309. https://doi.org/10.3390/molecules21030309
Holt JG, Krieg NR, Sneath PHA, Staley JT, Williams ST (1994) Bergey’s manual® of determinative bacteriology, 9th edn. Williams & Wilkins, Maryland
Im S, Wang W, Lee C, Lee YN (2010) Activation of macrophages by exopolysaccharide produced by MK1 bacterial strain isolated from Neungee mushroom, Sarcodon aspratus. Immune Netw 10(6):230–238. https://doi.org/10.4110/in.2010.10.6.230
Janda JM, Abbott SL (2007) 16S rRNA gene sequencing for bacterial identification in the diagnostic laboratory: pluses, perils, and pitfalls. J Clin Microbiol 45(9):2761–2764. https://doi.org/10.1128/JCM.01228-07
Jeong D, Kim D, Kang I, Kim H, Song K, Kim H, Seo K (2017) Characterization and antibacterial activity of a novel exopolysaccharide produced by Lactobacillus kefiranofaciens DN1 isolated from kefir. Food Control 78:436–442. https://doi.org/10.1016/j.foodcont.2017.02.033
Jesus Raposo MF, Morais RMSC, Morais AMMB (2013) Bioactivity and applications of sulphated polysaccharides from marine microalgae. Mar Drugs 11(1):233–252. https://doi.org/10.3390/md11010233
Ji C, Ji Y, Meng D (2013) Sulfated modification and anti-tumor activity of laminarin. Exp Ther Med 6(5):1259–1264. https://doi.org/10.3892/etm.2013.1277
Jones KM (2012) Increased production of the exopolysaccharide Succinoglycan enhances Sinorhizobium meliloti 1021 symbiosis with the host plant Medicago truncatula. J Bacteriol 194(16):4322–4331. https://doi.org/10.1128/JB.00751-12
Kalyanasundaram GT, Doble M, Gummadi SN (2012) Production and downstream processing of (1→3)-β-D-glucan from mutant strain of Agrobacterium sp. ATCC 31750. AMB Express 2:31. https://doi.org/10.1186/2191-0855-2-31
Kämpfer P, Jerzak L, Wilharm G, Golke J, Busse H, Glaeser HP (2015) Psychrobacter ciconiae sp. nov., isolated from white storks (Ciconia ciconia). I J Syst Evol Microbiol 65:772–777. https://doi.org/10.1099/ijs.0.000013
Karlapudi AP, Kodali VP, Kota KP, Shaik SS, Kumar NSS, Dirisala VR (2016) Deciphering the effect of novel bacterial exopolysaccharide-based nanoparticle cream against Propionibacterium acnes. 3 Biotech 6(1):35. https://doi.org/10.1007/s13205-015-0359-5
Khalil ES, Manap MY, Mustafa S, Amid M, Alhelli AM, Aljoubori A (2018) Probiotic characteristics of exopolysaccharides-producing Lactobacillus isolated from some traditional Malaysian fermented foods. CyTA J Food 16(1):287–298. https://doi.org/10.1080/19476337.2017.1401007
Kielak AM, Castellane TCL, Campanharo JC, Colnago LA, Costa OYA, Corradi da Silva ML, Veen JA, Lemos EGM, Kuramae EE (2017) Characterisation of novel Acidobacteria exopolysaccharides with potential industrial and ecological applications. Sci Rep 7(41193). https://doi.org/10.1038/srep41193
Kim M, Oh H, Park S, Chun J (2014) Towards a taxonomic coherence between average nucleotide identity and 16S rRNA gene sequence similarity for species demarcation of prokaryotes. I J Syst Evol Microbiol 64:346–351. https://doi.org/10.1099/ijs.0.059774-0
Kimura M (1980) A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16(2):111–120. https://doi.org/10.1007/BF01731581
Kong M, Chen XG, Xing K, Park HJ (2010) Antimicrobial properties of chitosan and mode of action: a state of the art review. I J Food Microbiol 144(1):51–63. https://doi.org/10.1016/j.ijfoodmicro.2010.09.012
Ladrat C, Sinquin C, Lebellenger L, Zykwinska A, Joualt S (2014) Exopolysaccharides produced by marine bacteria and their applications as glycosaminoglycan-like molecules. Front Chem 2:85. https://doi.org/10.3389/fchem.2014.00085
Laurienzo P (2010) Marine polysaccharides in pharmaceutical applications: an overview. Mar Drugs 8(9):2435–2465. https://doi.org/10.3390/md8092435
Liu S, Chen X, He H, Zhang X, Xie B, Yu Y, Chen B, Zhou B, Zhang Y (2013) Structure and ecological roles of a novel exopolysaccharide from the Arctic Sea ice bacterium Pseudoalteromonas sp. strain SM20310. Appl Environ Microbiol 79(1):224–230. https://doi.org/10.1128/AEM.01801-12
Lowry OH, Rosbrough NJ, Farr AL, Randall RJ (1951) Protein measurement with the Folin phenol reagent. J Biol Chem 193(1):265–275
Manca MC, Lama L, Improta R, Esposito E, Gambacorta A, Nicolaus B (1996) Chemical composition of two exopolysaccharides from Bacillus thermoantarcticus. Appl Environ Microbiol 62(9):3265–3269
Morsy MK, Sharoba AM, Khalaf HH, El-Tanahy HH, Cutter CN (2015) Efficacy of antimicrobial pullulan-based coating to improve internal quality and shelf-life of chicken eggs during storage. J Food Sci 80(5):1066–1074. https://doi.org/10.1111/1750-3841.12855
Moscovici M (2015) Present and future medical applications of microbial exopolysaccharides. Front Microbiol 6(1012). https://doi.org/10.3389/fmicb.2015.01012
Neopane P, Nepal HP, Shrestha R, Uehara O, Abiko Y (2018) In vitro biofilm formation by Staphylococcus aureus isolated from wounds of hospital-admitted patients and their association with antimicrobial resistance. Int J Gen Med 11:25–32. https://doi.org/10.2147/IJGM.S153268
Nichols CAM, Guezennec J, Bowman JP (2005) Bacterial exopolysaccharides from extreme marine environments with special consideration of the southern ocean, sea ice, and deep-sea hydrothermal vents: a review. Mar Biotechnol 7(4):253–271. https://doi.org/10.1007/s10126-004-5118-2
Nwodo UU, Green E, Okoh AI (2012) Bacterial exopolysaccharides: functionality and prospects. Int J Mol Sci 13(11):14002–14015. https://doi.org/10.3390/ijms131114002
Okinaka RT, Keim P (2016) The phylogeny of Bacillus cereus sensu lato. Microbiol Spectr 4(1). https://doi.org/10.1128/microbiolspec.TBS-0012-2012
Ordóñez E, Rupérez P (2011) FTIR-ATR spectroscopy as a tool for polysaccharide identification in edible brown and red seaweeds. Food Hydrocoll 25(6):1514–1520. https://doi.org/10.1016/j.foodhyd.2011.02.009
Panthavee W, Noda M, Danshiitsoodol N, Kumagai T, Sugiyama M (2017) Characterization of exopolysaccharides produced by thermophilic lactic acid bacteria isolated from tropical fruits of Thailand. Biol Pharm Bull 40(5):621–629. https://doi.org/10.1248/bpb.b16-00856
Pawar ST, Bhosale AA, Gawade TB, Nale TR (2013) Isolation, screening and optimization of exopolysaccharide producing bacterium from saline soil. J Microbiol Biotechnol Res 3(3):24–31 ISSN 2231-3168
Philippis R, Colica G, Micheletti E (2011) Exopolysaccharide-producing cyanobacteria in heavy metal removal from water: molecular basis and practical applicability of the biosorption process. Appl Microbiol Biotechnol 92(4):697–708. https://doi.org/10.1007/s00253-011-3601-z
Poli A, Anzelmo G, Fiorentino G, Nicolaus B, Tommonaro G, Di Donato P (2011) Polysaccharides from wastes of vegetable industrial processing: new opportunities for their eco-friendly re-use. In: Elnashar M (ed) Biotechnology of Polymers. InTech, London, pp 33–56
Prochnow A, Clauson M, Hong J, Murphy AB (2016) Gram positive and gram negative bacteria differ in their sensitivity to cold plasma. Sci Rep 6(38610). doi:10.1038/srep38610
Qiu D, Huang Z, Zhou T, Shen C, Hider RC (2011) In vitro inhibition of bacterial growth by iron chelators. FEMS Microbiol Lett 314(2):107–111. https://doi.org/10.1111/j.1574-6968.2010.02153.x
Raveendran S, Poulose AC, Yoshida Y, Maekawa T, Kumar DS (2013) Bacterial exopolysaccharide based nanoparticles for sustained drug delivery cancer chemotherapy and bioimaging. Carbohydrate Pol 91(1):22–32. https://doi.org/10.1016/j.carbpol.2012.07.079
Reichert M, Bergmann SM, Hwang J, Buchholz R, Lindenberger C (2017) Antiviral activity of exopolysaccharides from Arthrospira platensis against koi herpesvirus. J Fish Dis 40(10):1441–1450. https://doi.org/10.1111/jfd.12618
Romanenko LA, Schumann P, Rohde M, Lysenko AM, Mikhailov VV, Stackebrandt E (2002) Psychrobacter submarinus sp. nov. and Psychrobacter marincola sp. nov., psychrophilic halophiles from marine environments. I. J Syst Evol Microbiol 52:1291–1297. https://doi.org/10.1099/ijs.0.02087-0
Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4(4):406–425. https://doi.org/10.1093/oxfordjournals.molbev.a040454
Sajna KV, Sukumaran RK, Gottomukkala JD, Jayamurthy H, Dhar KS, Pandey A (2013) Studies on structural and physical characteristics of a novel exopolysaccharide from Pseudozyma sp. NII 08165. I J Biol Macromol 59:84–89. https://doi.org/10.1016/j.ijbiomac.2013.04.025
Sardari RRR, Kulcinskaja E, Ron EYC, Björnsdóttirc S, Friðjónsson OH, Hreggviðsson GO, Karlsson EN (2017) Evaluation of the production of exopolysaccharides by two strains of the thermophilic bacterium Rhodothermus marinus. Carbohydrate Pol 156:1–8. https://doi.org/10.1016/j.carbpol.2016.08.062
Sardi JCO, Polaquini CR, Freires IA, Galvão LCC, Lazarini JG, Torrezan GS, Regasini LO, Rosalen PL (2017) Antibacterial activity of diacetylcurcumin against Staphylococcus aureus results in decreased biofilm and cellular adhesion. J Med Microbiol 66:816–824. https://doi.org/10.1099/jmm.0.00049
Schmidt TR, Scott EJ, Dyer DW (2011) Whole-genome phylogenies of the family Bacillaceae and expansion of the sigma factor gene family in the Bacillus cereus species-group. BMC Genomics 12(430). https://doi.org/10.1186/1471-2164-12-430
Sebat JL, Paszczynski AJ, Cortese MS, Crawford RL (2001) Antimicrobial properties of pyridine-2, 6-dithiocarboxylic acid, a metal chelator produced by Pseudomonas spp. Appl Environ Microbiol 67(9):3934–3942. https://doi.org/10.1128/AEM.67.9.3934-3942.2001
Sezer AD, Kazak SH, Rayaman E, Cevikbas A, Öner ET, Akbuğa J (2017) Development and characterization of vancomycin-loaded levan-based microparticular system for drug delivery. Pharm Dev Technol 22(5):627–634. https://doi.org/10.3109/10837450.2015.1116564
Silhavy TJ, Kahne D, Walker S (2010) The bacterial cell envelope. Cold Spring Harb Perspect Biol 2(5). https://doi.org/10.1101/cshperspect.a000414
Singha TK (2012) Microbial extracellular polymeric substances: production, isolation and applications. IOSR J Pharm 2(2):276–281. http://www.iosrphr.org/papers/v2i2/ZC022276281.pdf. Accessed 16 December 2018. https://doi.org/10.9790/3013-0220276281
Smibert RM, Krieg NR (1994) Phenotypic characterization. In: Gerhardt P, Murray R, Wood W, Krieg N (eds) Methods for general and molecular bacteriology. ASM Press, Washington DC, pp 607–654
Soria-Mercado IE, Villareal-Gomez LJ, Rivas GG, Sanchez NEA (2012) Bioactive compounds from bacteria associated to marine algae. In: Sammour RH (ed) Biotechnology - molecular studies and novel applications for improved quality of human life. In-Tech, London, pp 25–44
Sun M, Zhao F, Shi M, Zhang X, Zhou B, Zhang Y, Chen X (2015) Characterization and biotechnological potential analysis of a new exopolysaccharide from the Arctic marine bacterium Polaribacter sp. SM1127. Sci Rep 5:18435. https://doi.org/10.1038/srep18435
Swofford DL (2002) PAUP*. Phylogenetic analysis using parsimony (*and other methods). Version 4, Sinauer Associates, Sunderland Massachusetts
Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22(22):4673–4680. https://doi.org/10.1093/nar/22.22.4673
Trinetta V, Cutter CN (2016) Pullulan: a suitable biopolymer for antimicrobial food packaging applications. In: Barros-Velázquez J (ed) Antimicrobial food packaging. Academic Press, Waltham MA, pp 385–397
Vu B, Chen M, Crawford RJ, Ivanova EP (2009) Bacterial extracellular polysaccharides involved in biofilm formation. Molecules 14(7):2535–2554. https://doi.org/10.3390/molecules14072535
Vuyst L, Vanderveken F, Van de Ven S, Degeest V (1998) Production by and isolation of exopolysaccharides from Streptococcus thermophilus grown in a milk medium and evidence for their growth-associated biosynthesis. J Appl Microbiol 84:1059–1068. https://doi.org/10.1046/j.1365-2672.1998.00445.x
Wang Y, Cai H, Chi C, Lu A, Lin X, Jiang Z, Wu X (2007) Halomonas shengliensis sp. nov., a moderately halophilic, denitrifying, crude-oil-utilizing bacterium. I J Syst Evol Microbiol 57:1222–1226. https://doi.org/10.1099/ijs.0.64973-0
Wen L, Xu Y, Wei Q, Chen W, Chen G (2018) Modeling and optimum extraction of multiple bioactive exopolysaccharide from an endophytic fungus of Crocus sativus L. Pharmacogn Mag 14(53):36–43. https://doi.org/10.4103/pm.pm_96_17
Wilson K (2003) Preparation of genomic DNA from bacteria. In: Ausubel FM, Brent R, Kingston RE, Moore DD, Seidman JG, Smith JA, Struhl K (eds) Current protocols in molecular biology. John Wiley & Sons Inc., Somerset NJ, pp 2.4.1–2.4.5
Wilson GS, Raftos DA, Nair SV (2011) Antimicrobial activity of surface attached marine bacteria in biofilms. Microbiol Res 166(6):437–448. https://doi.org/10.1016/j.micres.2010.08.003
Woo PCY, Teng JLL, Wu JKL, Leung FPS, Tse H, Fung AMY, Lau SKP, Yuen K (2009) Guidelines for interpretation of 16S rRNA gene sequence-based results for identification of medically important aerobic gram-positive bacteria. J Med Microbiol 58(Pt 8):1030–1036. https://doi.org/10.1099/jmm.0.008615-0
Wu S, Liu G, Jin W, Xiu P, Sun C (2016) Antibiofilm and anti-infection of a marine bacterial exopolysaccharide against Pseudomonas aeruginosa. Front Microbiol 7:102. https://doi.org/10.3389/fmicb.2016.00102
Yadav V, Prappulla SG, Jha A, Poonia A (2011) A novel exopolysaccharide from probiotic Lactobacillus fermentum CFR 2195: production, purification and characterization. Biotechnol Bioinf Bioeng 1(4):415–421 ISSN 2249-9075
Yang W, Pei F, Shi Y, Zhao L, Fang Y, Hu Q (2012) Purification, characterization and anti-proliferation activity of polysaccharides from Flammulina velutipes. Carbohydrates Pol 88(2):474–480. https://doi.org/10.1016/j.carbpol.2011.12.018
Yoon SH, Ha SM, Kwon S, Lim J, Kim Y, Seo H, Chun J (2017) Introducing EzBioCloud: a taxonomically united database of 16S rRNA and whole genome assemblies. Int J Syst Evol Microbiol 67:1613–1617
Zahner V, Silva ACTC, Moraes GP, McIntosh D, Filippis I (2013) Extended genetic analysis of Brazilian isolates of Bacillus cereus and Bacillus thuringiensis. Mem Inst Oswaldo Cruz 108(1):65–72. https://doi.org/10.1590/S0074-02762013000100011
Zeng Y, Yu Y, Liu Y, Li H (2016) Psychrobacter glaciei sp. nov., isolated from the ice core of an Arctic glacier. I J Syst Evol Microbiol 66:1792–1798. https://doi.org/10.1099/ijsem.0.000939
Zhang Z, Zhou Z, Li Y, Zhou L, Ding Q, Xu L (2016) Isolated exopolysaccharides from Lactobacillus rhamnosus GG alleviated adipogenesis mediated by TLR2 in mice. Sci Rep 6:36083. https://doi.org/10.1038/srep36083
Zheng LH, Wang YJ, Sheng J, Wang F, Zheng Y, Lin XK, Sun M (2011) Antitumor peptides from marine organisms. Mar Drugs 9:1840–1859. https://doi.org/10.3390/md9101840
Zhou X, Hong T, Yu Q, Nie S, Gong D, Xiong T, Xie M (2017) Exopolysaccharides from Lactobacillus plantarum NCU116 induce c-Jun dependent Fas/Fasl-mediated apoptosis via TLR2 in mouse intestinal epithelial cancer cells. Sci Rep 7:14247. https://doi.org/10.1038/s41598-017-14178-2
Acknowledgements
The authors wish to thank the Faculty of Agriculture, Faculty of Science, CBBR and University of Mauritius for supporting this study. The support of the technical staff of the Department of Agriculture & Food Science as well as the Department of Chemistry is gratefully acknowledged.
Funding
This work was supported by a grant from the University of Mauritius (grant number Q0117).
Author information
Authors and Affiliations
Corresponding authors
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Research involving human participants and/or animals
This article does not contain any studies with human participants or animals performed by any of the authors.
Informed consent
N/A
Additional information
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
ESM 1
(DOCX 567 kb)
Rights and permissions
About this article
Cite this article
Aullybux, A.A., Puchooa, D., Bahorun, T. et al. Phylogenetics and antibacterial properties of exopolysaccharides from marine bacteria isolated from Mauritius seawater. Ann Microbiol 69, 957–972 (2019). https://doi.org/10.1007/s13213-019-01487-2
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s13213-019-01487-2