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Extracellular Polysaccharide Production by Bacteria as a Mechanism of Toxic Heavy Metal Biosorption and Biosequestration in the Marine Environment

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Marine Pollution and Microbial Remediation

Abstract

Marine environments are one of the most diverse environments owing to their vast natural resource of imperative functional molecules. Interestingly, marine bacteria offer a great diversity of polysaccharides which could play an important role in biotechnology and industry. Among the various bioactive compounds, marine exopolymers are attracting major interest and attention due to their structural and functional diversity. Bacterial exopolysaccharides (EPSs) contain ionizable functional groups, which enable them to bind and sequestrate toxic heavy metal ions. Due to their biodegradability and safety of the environment, biosorption of heavy metals by these biopolymers has attracted considerable attention as promising alternatives capable to compete with expensive, inefficient and conventional technologies, including chemical precipitation, adsorption on activated carbon, membrane separations, ion exchange and solvent extraction methods. This review particularly emphasizes on utilization of marine bacteria in the field of bioremediation and understanding the mechanism behind acquiring the characteristic feature of adaptive responses. Fundamental insights regarding metals in relation to metal-binding proteins/peptides for immobilization, information regarding genetic engineering for enzymes involved in metal transformation and strategies that can be employed to overcome the bottlenecks associated with microbial-based remediation are highlighted in this review. The important engineering properties based on structural characteristics such as adsorption, biodegradability and hydrophilicity/hydrophobicity of EPS matrix are also discussed. A thorough understanding of microbes that produce exopolysaccharides for metal biosequestration and biosorption would solve several problems in bioremediation process.

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References

  • Abd-Elnaby H, Abou-Elela GM, El-Sersy NA (2013) Cadmium resisting bacteria in Alexandria Eastern Harbor (Egypt) and optimization of cadmium bioaccumulation by Vibrio harveyi. Afr J Biotechnol 10(17):3412–3423

    Google Scholar 

  • Al-Horani RA, Desai UR (2010) Chemical sulfation of small molecules—advances and challenges. Tetrahedron 66(16):2907–2918

    Article  CAS  Google Scholar 

  • Arena A (2004) Exopolysaccharides from marine thermophilic bacilli induce a Th1 cytokine profile in human PBMC. Eur Congr Clin Microbiol Infect Dis 14:1317

    Google Scholar 

  • Arias S, Del Moral A, Ferrer MR, Tallon R, Quesada E, Bejar V (2003) Mauran, an exopolysaccharide produced by the halophilic bacterium Halomonas maura, with a novel composition and interesting properties for biotechnology. Extremophiles 7:319–326

    Article  CAS  Google Scholar 

  • Baptista MS, Vasconcelos MT (2006) Cyanobacteria metal interactions: requirements, toxicity, and ecological implications. Crit Rev Microbiol 32(3):127–137

    Article  CAS  Google Scholar 

  • Barnett JP, Scanlan DJ, Blindauer CA (2014) Identification of major zinc-binding proteins from a marine cyanobacterium: insight into metal uptake in oligotrophic environments. Metallomics 6(7):1254–1268

    Article  CAS  Google Scholar 

  • Bautista BET, Wikieł AJ, Datsenko I, Vera M, Sand W, Seyeux A, Marcus P (2015) Influence of extracellular polymeric substances (EPS) from Pseudomonas NCIMB 2021 on the corrosion behaviour of 70Cu–30Ni alloy in seawater. J Electroanal Chem 737:184–197

    Article  CAS  Google Scholar 

  • Beech IB, Cheung CWS (1995) Interactions of exopolymers produced by sulphate reducing bacteria with metal ions. Int Biodeterior Biodegrad 35:59–72

    Article  CAS  Google Scholar 

  • Bhaskar PV, Bhosle NB (2006) Bacterial extracellular polymeric substances (EPS) a carrier of heavy metals in the marine food-chain. Environ Int 32:192–198

    Article  CAS  Google Scholar 

  • Bhaskar PV, Grossart HP, Bhosle NB, Simon M (2005) Production of macroaggregates from dissolved exopolymeric substances (EPS) of bacterial and diatom origin. FEMS Microbiol Ecol 53(2):255–264

    Article  CAS  Google Scholar 

  • Blindauer CA, Harrison MD, Robinson AK, Parkinson JA, Bowness PW, Sadler PJ, Robinson NJ (2002) Multiple bacteria encode metallothioneins and SmtA‐like zinc fingers. Mol Microbiol 45(5):1421–1432

    Article  CAS  Google Scholar 

  • Bouchotroch S, Quesada E, Izquierdo I, Rodriguez M, Bejar V (2000) Bacterial exopolysaccharides produced by newly discovered bacteria belonging to the genus Halomonas, isolated from hypersaline habitats in Morocco. J Ind Microbiol Biotechnol 24:374–378

    Article  CAS  Google Scholar 

  • Braissant O, Decho AW, Dupraz C, Glunk C, Przekop KM, Visscher PT (2007) Exopolymeric substances of sulfate-reducing bacteria: interactions with calcium at alkaline pH and implication for formation of carbonate minerals. Geobiology 5:401–411

    Article  CAS  Google Scholar 

  • Bramhachari PV, Dubey SK (2006) Isolation and characterization of exopolysaccharide produced by Vibrio harveyi strain VB23. Lett Appl Microbiol 43(5):571–577

    Article  CAS  Google Scholar 

  • Bramhachari PV, Kavi Kishor PB, Ramadevi R, Kumar R, Rao BR, Dubey SK (2007) Isolation and characterization of mucous exopolysaccharide produced by Vibrio furnissii VB0S3. J Microbiol Biotechnol 17:44–51

    CAS  Google Scholar 

  • Brim H, McFarlan SC, Fredrickson JK, Minton KW, Zhai M, Wackett LP, Daly MJ (2000) Engineering Deinococcus radiodurans for metal remediation in radioactive mixed waste environments. Nat Biotechnol 18:85–90

    Article  CAS  Google Scholar 

  • Cambon-Bonavita MA, Raguenes G, Jean J, Vincent P, Guezennec J (2002) A novel polymer produced by a bacterium isolated from a deep-sea hydrothermal vent polychaete annelid. J Appl Microbiol 93:310–315

    Article  CAS  Google Scholar 

  • Campbell LM, Norstrom RJ, Hobson KA, Muir DC, Backus S, Fisk AT (2005) Mercury and other trace elements in a pelagic Arctic marine food web (Northwater Polynya, Baffin Bay). Sci Total Environ 351:247–263

    Article  CAS  Google Scholar 

  • Cao B, Ahmed B, Kennedy DW, Wang Z, Shi L, Marshall MJ, Beyenal H (2011) Contribution of extracellular polymeric substances from Shewanella sp. HRCR-1 biofilms to U (VI) immobilization. Environ Sci Technol 45(13):5483–5490

    Article  CAS  Google Scholar 

  • Chakraborty J, Das S (2014) Characterization and cadmium-resistant gene expression of biofilm-forming marine bacterium Pseudomonas aeruginosa JP-11. Environ Sci Pollut Res 21(24):14188–14201

    Article  CAS  Google Scholar 

  • Chen W, Bruhlmann F, Richins RD, Mulchandani A (1999) Engineering of improved microbes and enzymes for bioremediation. Curr Opin Biotechnol 10:137–141

    Article  CAS  Google Scholar 

  • Cheung KH, Gu JD (2003) Reduction of chromate (CrO42−) by an enrichment consortium and an isolate of marine sulfate reducing bacteria. Chemosphere 52:1523–1529

    Article  CAS  Google Scholar 

  • Colliec S, Boisson-vidal C, Jozefonvicz J (1994) A low molecular weight fucoidan fraction from the brown seaweed Pelvetia canaliculata. Phytochemistry 35(3):697–700

    Article  CAS  Google Scholar 

  • Comte S, Guibaud G, Baudu M (2006) Biosorption properties of extracellular polymeric substances (EPS) resulting from activated sludge according to their type: soluble or bound. Process Biochem 41(4):815–823

    Article  CAS  Google Scholar 

  • Comte S, Guibaud G, Baudu M (2008) Biosorption properties of extracellular polymeric substances (EPS) towards Cd, Cu and Pb for different pH values. J Hazard Mater 151(1):185–193

    Article  CAS  Google Scholar 

  • Corsaro MM, Lanzetta R, Parrilli E, Parrilli M, Tutino ML, Ummarino S (2004) Influence of growth temperature on lipid and phosphate contents of surface polysaccharides from the Antarctic bacterium Pseudoalteromonas haloplanktis TAC 125. J Bacteriol 186(1):29–34

    Article  CAS  Google Scholar 

  • d’Ayala GG, Malinconico M, Laurienzo P (2008) Marine derived polysaccharides for biomedical applications: chemical modification approaches. Molecules 13(9):2069–2106

    Article  CAS  Google Scholar 

  • Das S, Shanmugapriya R, Lyla PS, Khan SA (2007) Heavy metal tolerance of marine bacteria—an index of marine pollution. Nat Acad Sci Lett (India) 30:279–284

    CAS  Google Scholar 

  • Das P, Mukherjee S, Sen R (2008) Improved bioavailability and biodegradation of a model polyaromatic hydrocarbon by a biosurfactant producing bacterium of marine origin. Chemosphere 72:1229–1234

    Article  CAS  Google Scholar 

  • Das P, Mukherjee S, Sen R (2009) Biosurfactant of marine origin exhibiting heavy metal remediation properties. Bioresour Technol 100(20):4887–4890

    Article  CAS  Google Scholar 

  • Dash HR, Mangwani N, Das S (2014) Characterization and potential application in mercury bioremediation of highly mercury-resistant marine bacterium Bacillus thuringiensis PW-05. Environ Sci Pollut Res 21(4):2642–2653

    Article  CAS  Google Scholar 

  • De Rore H, Top E, Houwen F, Mergcay M, Verstraete W (1994) Evolution of heavy metal-resistant transconjugants in a soil environment with a concomitant selective pressure. FEMS Microbiol Ecol 14:263–273

    Article  Google Scholar 

  • De J, Ramaiah N, Bhosle NB, Garg A, Vardanyan L, Nagle VL, Fukami K (2007) Potential of mercury resistant marine bacteria for detoxification of chemicals of environmental concern. Microbes Environ 22:336–345

    Article  Google Scholar 

  • De J, Ramaiah N, Vardanyan L (2008) Detoxification of toxic heavy metals by marine bacteria highly resistant to mercury. Mar Biotechnol 10(4):471–477

    Article  CAS  Google Scholar 

  • DeAngelis PL (2002) Evolution of glycosaminoglycans and their glycosyltransferases: implications for the extracellular matrices of animals and the capsules of pathogenic bacteria. Anat Rec 268(3):317–326

    Article  CAS  Google Scholar 

  • DeAngelis PL, Gunay NS, Toida T, Mao W-J, Linhardt RJ (2002) Identification of the capsular polysaccharides of Type D and F Pasteurella multocida as unmodified heparin and chondroitin, respectively. Carbohydr Res 337:1547–1552

    Article  CAS  Google Scholar 

  • Decho AW (1990) Microbial exopolymer secretions in ocean environments: their role(s) in food webs and marine processes. In: Barnes M (ed) Oceanogr Mar Biol Annu Rev. Aberdeen University Press, Aberdeen, pp 73–153

    Google Scholar 

  • Decho AW, Visscher RS, Norman PT (2010) Quorum sensing in natural environments: emerging views from microbial mats. Trends Microbiol 18:73–80

    Article  CAS  Google Scholar 

  • Dubreucq G, Domon B, Fournet B (1996) Structure determination of a novel uronic acid residue isolated from the exopolysaccharide produced by a bacterium originating from deep sea hydrothermal vents. Carbohydr Res 290(2):175–181

    Article  CAS  Google Scholar 

  • El-Deeb B (2009) Natural combination of genetic systems for degradation of phenol and resistance to heavy metals in phenol and cyanide assimilating bacteria. Malay J Microbiol 5:94–103

    Google Scholar 

  • Esko JD, Lindahl U (2001) Molecular diversity of heparan sulfate. J Clin Invest 108(2):169–173

    Article  CAS  Google Scholar 

  • Finore I, Di Donato P, Mastascusa V, Nicolaus B, Poli A (2014) Fermentation technologies for the optimization of marine microbial exopolysaccharide production. Mar Drugs 12:3005–3024

    Article  CAS  Google Scholar 

  • Flemming HC, Wingender J (2010) The biofilm matrix. Nat Rev Microbiol 8:623–633

    CAS  Google Scholar 

  • Freitas F, Alves VD, Reis MAM (2011) Advances in bacterial exopolysaccharides: from production to biotechnological applications. Trends Biotechnol 29:388–398

    Article  CAS  Google Scholar 

  • Fu F, Wang Q (2011) Removal of heavy metal ions from wastewaters: a review. J Environ Manag 92:407–418

    Article  CAS  Google Scholar 

  • Gadd GM (2009) Biosorption: critical review of scientific rationale, environmental importance and significance for pollution treatment. J Chem Technol Biotechnol 84(1):13–28

    Article  CAS  Google Scholar 

  • Gadd GM, White C (1989) Removal of thorium from simulated acid process streams by fungal biomass. Biotechnol Bioeng 33(5):592–597

    Google Scholar 

  • Geesey GG, Jang L, Jolley JG, Hankins MR, Iwaoka T, Griffiths PR (1988) Binding of metal ions by extracellular polymers of biofilm bacteria. Water Sci Technol 20(11–12):161–165

    CAS  Google Scholar 

  • Georgiou G, Lin SC, Sharma MM (1992) Surface-active compounds from microorganisms. Biotechnology 10:60–65

    Article  CAS  Google Scholar 

  • Gericke M, Liebert T, Seoud OAE, Heinze T (2011) Tailored media for homogeneous cellulose chemistry: ionic liquid/co‐solvent mixtures. Macromol Mater Eng 296(6):483–493

    Article  CAS  Google Scholar 

  • Gnanamani A, Kavitha V, Radhakrishnan N, Rajakumar GS, Sekaran G, Mandal AB (2010) Microbial products (biosurfactant and extracellular chromate reductase) of marine microorganism are the potential agents reduce the oxidative stress induced by toxic heavy metals. Colloids Surf B: Biointerfaces 79(2):334–339

    Article  CAS  Google Scholar 

  • Guezennec J (2002) Deep-sea hydrothermal vents: a new source of innovative bacterial exopolysaccharides of biotechnological interest? J Ind Microbiol Biotechnol 29:204–208

    Article  CAS  Google Scholar 

  • Guezennec J, Ortega‐Morales O, Raguenes G, Geesey G (1998) Bacterial colonization of artificial substrate in the vicinity of deep‐sea hydrothermal vents. FEMS Microbiol Ecol 26(2):89–99

    Article  CAS  Google Scholar 

  • Guézennec J, Moppert X, Raguénès G, Richert L, Costa B, Simon-Colin C (2011) Microbial mats in French Polynesia and their biotechnological applications. Process Biochem 46:16–22

    Article  CAS  Google Scholar 

  • Guibaud G, Comte S, Bordas F, Dupuy S, Baudu M (2005) Comparison of the complexation potential of extracellular polymeric substances (EPS), extracted from activated sludge and produced by pure bacterial strains, for cadmium, lead and nickel. Chemosphere 59:629–638

    Article  CAS  Google Scholar 

  • Gutiérrez T, Mulloy B, Black K, Green DH (2007) Glycoprotein emulsifiers from two marine Halomonas species: chemical and physical characterization. J Appl Microbiol 103:1716–1727

    Article  CAS  Google Scholar 

  • Gutierrez T, Shimmield T, Haidon C, Black K, Green DH (2008) Emulsifying and metal ion binding activity of a glycoprotein exopolymer produced by Pseudoalteromonas sp. strain TG12. Appl Environ Microbiol 74:4867–4876

    Article  CAS  Google Scholar 

  • Gutierrez T, Morris G, Green DH (2009) Yield and physicochemical properties of EPS from Halomonas sp. strain TG39 identifies a role for protein and anionic residues (sulfate and phosphate) in emulsification of n-hexadecane. Biotechnol Bioeng 103:207–216

    Article  CAS  Google Scholar 

  • Gyurcsik B, Nagy L (2000) Carbohydrates as ligands: coordination equilibria and structure of the metal complexes. Coord Chem Rev 203:81–149

    Article  CAS  Google Scholar 

  • Ha J, Gélabert A, Spormann AM, Brown GE (2010) Role of extracellular polymeric substances in metal ion complexation on Shewanella oneidensis: batch uptake, thermodynamic modeling, ATR-FTIR, and EXAFS study. Geochim Cosmochim Acta 74(1):1–15

    Article  CAS  Google Scholar 

  • Hamer DH (1986) Metallothionein1, 2. Annu Rev Biochem 55(1):913–951

    Article  CAS  Google Scholar 

  • Hardikar VV, Matijević E (2001) Influence of ionic and nonionic dextrans on the formation of calcium hydroxide and calcium carbonate particles. Colloids Surf A Physicochem Eng Asp 186(1):23–31

    Article  CAS  Google Scholar 

  • Hassler CS, Alasonati E, Nichols CM, Slaveykova VI (2011) Exopolysaccharides produced by bacteria isolated from the pelagic Southern Ocean—role in Fe binding, chemical reactivity, and bioavailability. Mar Chem 123(1):88–98

    Article  CAS  Google Scholar 

  • Hoagland KD, Rosowski JR, Gretz MR, Roemer SC (1993) Diatom extracellular polymeric substances: function, fine structure, chemistry, and physiology. J Phycol 29:537–566

    Article  CAS  Google Scholar 

  • Hosono T, Su C, Delinom R, Umezawa Y, Toyota T, Kaneko S, Taniguchi M (2011) Decline in heavy metal contamination in marine sediments in Jakarta Bay, Indonesia due to increasing environmental regulations. Estuar Coast Shelf Sci 92:297–306

    Article  CAS  Google Scholar 

  • Huston AL, Methe B, Deming JW (2004) Purification, characterization, and sequencing of an extracellular cold-active aminopeptidase produced by marine psychrophile Colwellia psychrerythraea strain 34H. Appl Environ Microbiol 70(6):3321–3328

    Article  CAS  Google Scholar 

  • Ishaque AB, Johnson L, Gerald T, Boucaud D, Okoh J, Tchounwou PB (2006) Assessment of individual and combined toxicities of four non-essential metals (As, Cd, Hg and Pb) in the microtox assay. Int J Environ Res Public Health 3:118–120

    Article  CAS  Google Scholar 

  • Iyer A, Mody K, Jha B (2004) Accumulation of hexavalent chromium by an exopolysaccharide producing marine Enterobacter cloacae. Mar Pollut Bull 49(11):974–977

    Article  CAS  Google Scholar 

  • Iyer A, Mody K, Jha B (2005) Biosorption of heavy metals by a marine bacterium. Mar Pollut Bull 50(3):340–343

    Article  CAS  Google Scholar 

  • Iyer A, Mody K, Jha B (2006) Emulsifying properties of a marine bacterial exopolysaccharide. Enzym Microb Technol 38(1):220–222

    Article  CAS  Google Scholar 

  • Jouault SC, Chevolot L, Helley D, Ratiskol J, Bros A, Sinquin C, Fischer AM (2001) Characterization, chemical modifications and in vitro anticoagulant properties of an exopolysaccharide produced by Alteromonas infernus. Biochim Biophys Acta Gen Subj 1528(2):141–151

    Article  Google Scholar 

  • Jouault SC, Delbarre-Ladrat C (2014) Marine-derived bioactive polysaccharides from microorganisms. In: Brahmachari G (ed) Natural bioactive molecules. Impacts and prospects. Narosa Publishing House, New Delhi, pp 5.1–5.21

    Google Scholar 

  • Jouault SC, Zanchetta P, Helley D, Ratiskol J, Sinquin C, Fischer AM et al (2004) Microbial polysaccharides of marine origin and their potential in human therapeutics. Pathol Biol 52:127–130

    Article  CAS  Google Scholar 

  • Karigar CS, Rao SS (2011) Role of microbial enzymes in the bioremediation of pollutants: a review. Enzym Res 2011:1–11

    Article  CAS  Google Scholar 

  • Khanolkar D, Dubey SK, Naik MM (2015) Tributyltin Chloride (TBTCl)-enhanced exopolysaccharide and siderophore production in an estuarine Alcaligenes faecalis strain. Arch Environ Contam Toxicol 68(4):612–621

    Article  CAS  Google Scholar 

  • Kim SJ, Yim JH (2007) Cryoprotective properties of exopolysaccharide (P-21653) produced by the Antarctic bacterium, Pseudoalteromonas arctica KOPRI 21653. J Microbiol (Seoul Korea) 45(6):510–514

    CAS  Google Scholar 

  • Kivela HM, Madonna S, Krupovic M, Tutino ML, Bamford JKH (2008) Genetics for Pseudoalteromonas provides tools to manipulate marine bacterial virus PM2. J Bacteriol 190:1298–1307

    Article  CAS  Google Scholar 

  • Kong JY, Lee HW, Hong JW, Kang YS, Kim JD, Chang MW, Bae SK (1998) Utilization of a cell-bound polysaccharide produced by the marine bacterium Zooglea sp.: new biomaterial for metal adsorption and enzyme immobilization. J Mar Biotechnol 6:99–103

    CAS  Google Scholar 

  • Kuo M-S, Mort AJ, Dell A (1986) Identification and location of l-glycerate, an unusual acyl substituent in gellan gum. Carbohydr Res 156:173–187

    Article  CAS  Google Scholar 

  • Laurent TC, Fraser JR (1992) Hyaluronan. FASEB J 6:2397–2404

    CAS  Google Scholar 

  • Laurienzo P (2010) Marine polysaccharides in pharmaceutical applications: an overview. Mar Drugs 8:2435–2465

    Article  CAS  Google Scholar 

  • Lemoine J, Chirat F, Wieruszeski JM, Strecker G, Neeser N, Favre JR (1997) Structural characterization of the exocellular polysaccharides produced by Streptococcus thermophilus SFi39 and SFi12. Appl Environ Microbiol 63:3512–3518

    CAS  Google Scholar 

  • Lewinson O, Lee AT, Rees DC (2009) A P-type ATPase importer that discriminates between essential and toxic transition metals. Proc Natl Acad Sci U S A 106:4677–4682

    Article  CAS  Google Scholar 

  • Liu H, Fang HH (2002) Characterization of electrostatic binding sites of extracellular polymers by linear programming analysis of titration data. Biotechnol Bioeng 80(7):806–811

    Article  CAS  Google Scholar 

  • Liu S-B, Chen X-L, He H-L, Zhang X-Y, Xie B-B, Yu Y et al (2013) Structure and ecological roles of a novel exopolysaccharide from the Arctic Sea Ice bacterium Pseudoalteromonas sp. strain SM20310. Appl Environ Microbiol 79:224–230

    Article  CAS  Google Scholar 

  • Llamas I, Mata JA, Tallon R, Bressollier P, Urdaci MC, Quesada E, Béjar V (2010) Characterization of the exopolysaccharide produced by Salipiger mucosus A3T, a halophilic species belonging to the Alphaproteobacteria, isolated on the Spanish mediterranean seaboard. Mar Drugs 8(8):2240–2251

    Article  CAS  Google Scholar 

  • Loaec M, Olier R, Guezennec J (1997) Uptake of lead, cadmium and zinc by a novel bacterial exopolysaccharide. Water Res 31:1171–1179

    Article  CAS  Google Scholar 

  • Loaec M, Olier R, Guezennec J (1998) Chelating properties of bacterial exopolysaccharides from deep-sea hydrothermal vents. Carbohydr Polym 35(1):65–70

    Article  CAS  Google Scholar 

  • Maalej H, Boisset C, Hmidet N, Buon L, Heyraud A, Nasri M (2014) Purification and structural data of a highly substituted exopolysaccharide from Pseudomonas stutzeri AS22. Carbohydr Polym 112:404–411

    Article  CAS  Google Scholar 

  • Mancuso Nichols CA, Garon S, Bowman JP, Raguenes G, Guezennec J (2004) Production of exopolysaccharides by Antarctic marine bacterial isolates. J Appl Microbiol 96:1057–1066

    Article  CAS  Google Scholar 

  • Mancuso Nichols CA, Guezennec J, Bowman JP (2005a) Bacterial exopolysaccharides from extreme marine environments with special consideration of the southern ocean, sea ice, and deep-sea hydrothermal vents. Mar Biotechnol 7(4):253–271

    Article  CAS  Google Scholar 

  • Mancuso Nichols C, Bowman JP, Guezennec J (2005b) Effects of incubation temperature on growth and production of exopolysaccharides by an Antarctic sea ice bacterium grown in batch culture. Appl Environ Microbiol 71:3519–3523

    Article  CAS  Google Scholar 

  • Mancuso Nichols C, Garon Lardière S, Bowman JP, Nichols PD, Gibson JAE, Guézennec J (2005c) Chemical characterization of exopolysaccharides from Antarctic marine bacteria. Microb Ecol 49:578–589

    Article  CAS  Google Scholar 

  • Martinez-Canovas MJ, Quesada E, Llamas I, Béjar V (2004) Halomonas ventosae sp. nov., a moderately halophilic, denitrifying, exopolysaccharide-producing bacterium. Int J Syst Evol Microbiol 54:733–737

    Article  CAS  Google Scholar 

  • Marx JG, Carpenter SD, Deming JW (2009) Production of cryoprotectant extracellular polysaccharide substances (EPS) by the marine psychrophilic bacterium Colwellia psychrerythraea strain 34H under extreme conditions. Can J Microbiol 55:63–72

    Article  CAS  Google Scholar 

  • Marzocca MP, Harding NE, Petroni EA, Cleary JM, Ielpi L (1991) Location and cloning of the ketal pyruvate transferase gene of Xanthomonas campestris. J Bacteriol 173:7519–7524

    CAS  Google Scholar 

  • Mata JA, Béjar V, Llamas I, Arias S, Bressollier P et al (2006) Exopolysaccharides produced by the recently described halophilic bacteria Halomonas ventosae and Halomonas anticariensis. Res Microbiol 157:827–835

    Article  CAS  Google Scholar 

  • Morcillo F, Gonza’lez-Mun˜oz MT, Reitz T, Romero-Gonzalez ME, Arias JM et al (2014) Biosorption and Biomineralization of U (VI) by the marine bacterium Idiomarina loihiensis MAH1: effect of background electrolyte and pH. PLoS ONE 9(3):e91305

    Article  CAS  Google Scholar 

  • Moriello VS, Lama L, Poli A, Gugliandolo C, Maugeri TL, Gambacorta A, Nicolaus B (2003) Production of exopolysaccharides from a thermophilic microorganism isolated from a marine hot spring in flegrean areas. J Ind Microbiol Biotechnol 30(2):95–101

    Article  CAS  Google Scholar 

  • Mulligan CN, Yong CN, Gibbs BF (2001) Heavy metal removal from sediments by biosurfactants. J Hazard Mater 85:111–125

    Article  CAS  Google Scholar 

  • Muraleedharan TR, Iyengar L, Venkobachar C (1991) Biosorption: alternative for metal removal and recovery. Curr Sci 61:379–385

    CAS  Google Scholar 

  • Nagy L, Yamaguchi T, Yoshida K (2003) Application of EXAFS and XANES methods in coordination chemistry of carbohydrates and their derivatives. Struct Chem 14:77–84

    Article  CAS  Google Scholar 

  • Naik MM, Pandey A, Dubey SK (2012) Pseudomonas aeruginosa strain WI-1 from Mandovi estuary possesses metallothionein to alleviate lead toxicity and promotes plant growth. Ecotoxicol Environ Saf 79:129–133

    Article  CAS  Google Scholar 

  • Nardella A, Chaubet F, Boisson-Vidal C, Blondin C, Durand P, Jozefonvicz J (1996) Anticoagulant low molecular weight fucans produced by radical process and ion exchange chromatography of high molecular weight fucans extracted from the brown seaweed Ascophyllum nodosum. Carbohydr Res 289:201–208

    Article  CAS  Google Scholar 

  • Nazarenko EL, Komandrova NA, Gorshkova RP, Tomshich SV, Zubkov VA, Kilcoyne M et al (2003) Structures of polysaccharides and oligosaccharides of some gram-negative marine proteobacteria. Carbohydr Res 338:2449–2457

    Article  CAS  Google Scholar 

  • Nicolaus B, Manca MC, Ramano I, Lama L (1993) Production of an exopolysaccharide from two thermophilic archaea belonging to the genus Sulfolobus. FEMS Microbiol Lett 109:203–206

    Article  CAS  Google Scholar 

  • Nicolaus B, Kambourova M, Oner ET (2010) Exopolysaccharides from extremophiles: from fundamentals to biotechnology. Environ Technol 31:1145–1158

    Article  CAS  Google Scholar 

  • Nies DH (2003) Efflux‐mediated heavy metal resistance in prokaryotes. FEMS Microbiol Rev 27(2–3):313–339

    Article  CAS  Google Scholar 

  • Nunkaew T, Kantachote D, Nitoda T, Kanzaki H, Ritchie RJ (2015) Characterization of exopolymeric substances from selected Rhodopseudomonas palustris strains and their ability to adsorb sodium ions. Carbohydr Polym 115:334–341

    Article  CAS  Google Scholar 

  • Ozturk S, Aslim B, Suludere Z (2009) Evaluation of chromium (VI) removal behaviour by two isolates of Synechocystis sp. in terms of exopolysaccharide (EPS) production and monomer composition. Bioresour Technol 100:5588–5593

    Article  CAS  Google Scholar 

  • Pal A, Paul AK (2008) Microbial extracellular polymeric substances: central elements in heavy metal bioremediation. Indian J Microbiol 48:49–64

    Article  CAS  Google Scholar 

  • Panwichian S, Kantachote D, Wittayaweerasa B, Mallavarapu M (2011) Removal of heavy metals by exopolymeric substances produced by resistant purple non sulphur bacteria isolated from contaminated shrimp ponds. Electron J Biotechnol 14. ISSN: 0717-3458

    Google Scholar 

  • Park D, Yun YS, Park JM (2010) The past, present, and future trends of biosorption. Biotechnol Bioprocess Eng 15(1):86–102

    Article  CAS  Google Scholar 

  • Parolis H, Parolis LAS, Boan IF, Rodriguez-Valera F, Widmalm G, Manca MC et al (1996) The structure of the exopolysaccharide produced by the halophilic archaeon Haloferax mediterranei strain R4 (ATCC 33500). Carbohydr Res 295:147–156

    Article  CAS  Google Scholar 

  • Pepi M, Cesàro A, Liut G, Baldi F (2005) An Antarctic psychrotrophic bacterium Halomonas sp. ANT-3b, growing on n-hexadecane, produces a new emulsifying glycolipid. FEMS Microbiol Ecol 53:157–166

    Article  CAS  Google Scholar 

  • Pieper DH, Reineke W (2000) Engineering bacteria for bioremediation. Curr Opin Biotechnol 11(3):262–270

    Article  CAS  Google Scholar 

  • Poirier I, Jean N, Guary JC, Bertrand M (2008) Responses of the marine bacterium Pseudomonas fluorescens to an excess of heavy metals: physiological and biochemical aspects. Sci Total Environ 406:76–87

    Article  CAS  Google Scholar 

  • Poirier I, Hammann P, Kuhn L, Bertrand M (2013) Strategies developed by the marine bacterium Pseudomonas fluorescens BA3SM1 to resist metals: a proteome analysis. Aquat Toxicol 128:215–232

    Article  CAS  Google Scholar 

  • Poli A, Esposito E, Orlando P, Lama L, Giordano A, De Appolonia F et al (2007) Halomonas alkaliantarctica sp. nov., isolated from saline lake Cape Russell in Antarctica, an alkalophilic moderately halophilic, exopolysaccharide-producing bacterium. Syst Appl Microbiol 30:31–38

    Article  CAS  Google Scholar 

  • Poli A, Anzelmo G, Nicolaus B (2010) Bacterial exopolysaccharides from extreme marine habitats: production, characterization and biological activities. Mar Drugs 8:1779–1802

    Article  CAS  Google Scholar 

  • Poli A, Di Donato P, Abbamondi GR, Nicolaus B (2011) Synthesis, production, and biotechnological applications of exopolysaccharides and polyhydroxyalkanoates by Archaea. Archaea 2011:693253

    Article  CAS  Google Scholar 

  • Pomin VH (2014) Marine medicinal glycomics. Front Cell Infect Microbiol 4:5

    Google Scholar 

  • Poremba K, Gunkel W, Lang S, Wagner F (1991) Marine biosurfactants, III. Toxicity testing with marine microorganisms and comparison with synthetic surfactants. Z Naturforsch 46c:210–216

    Google Scholar 

  • Qin G, Zhu L, Chen X, Wang PG, Zhang Y (2007) Structural characterization and ecological roles of a novel exopolysaccharide from the deep-sea psychrotolerant bacterium Pseudoalteromonas sp. SM9913. Microbiology 153:1566–1572

    Article  CAS  Google Scholar 

  • Quigley MS, Santschi PH, Hung CC, Guo L, Honeyman BD (2002) Importance of acid polysaccharides for 234Th complexation to marine organic matter. Mar Chem 76:27–45

    Article  Google Scholar 

  • Raedts J, Kengen SWM, van der Oost J (2011) Occurrence of L-iduronic acid and putative D-glucuronyl C5-epimerases in prokaryotes. Glycoconj J 28:57–66

    Article  CAS  Google Scholar 

  • Raedts J, Lundgren M, Kengen SWM, Li J-P, van der Oost J (2013) A novel bacterial enzyme with D-glucuronyl C5-epimerase activity. J Biol Chem 288:24332–24339

    Article  CAS  Google Scholar 

  • Raguenes G, Pignet P, Gauthier G, Peres A, Christen R, Rougeaux H et al (1996) Description of a new polymer-secreting bacterium from a deep-sea hydrothermal vent, Alteromonas macleodii subsp. fijiensis, and preliminary characterization of the polymer. Appl Environ Microbiol 62:67–73

    CAS  Google Scholar 

  • Raguenes GH, Peres A, Ruimy R, Pignet P, Christen R, Loaec M et al (1997) Alteromonas infernus sp. nov., a new polysaccharide-producing bacterium isolated from a deep-sea hydrothermal vent. J Appl Microbiol 82:422–430

    Article  CAS  Google Scholar 

  • Raguenes G, Cambon-Bonavita MA, Lohier JF, Boisset C, Guezennec J (2003) A novel, highly viscous polysaccharide excreted by an Alteromonas isolated from a deep-sea hydrothermal vent shrimp. Curr Microbiol 46:448–452

    Article  CAS  Google Scholar 

  • Rajaram R, Banu JS, Mathivanan K (2013) Biosorption of Cu (II) ions by indigenous copper-resistant bacteria isolated from polluted coastal environment. Toxicol Environ Chem 95(4):590–604

    Article  CAS  Google Scholar 

  • Rendleman JA (1978) Metal-polysaccharide complexes-part 1. Food Chem 3:47–79

    Article  CAS  Google Scholar 

  • Reuber TL, Walker GC (1993) Biosynthesis of succinoglycan, a symbiotically important exopolysaccharide of Rhizobium meliloti. Cell 74:269–280

    Article  CAS  Google Scholar 

  • Ridout MJ, Brownsey GJ, York GM, Walker GC, Morris VJ (1997) Effect of o-acyl substituents on the functional behaviour of Rhizobium meliloti succinoglycan. Int J Biol Macromol 20(1):1–7

    Article  CAS  Google Scholar 

  • Rinker KD, Kelly RM (2000) Effect of carbon and nitrogen sources on growth dynamics and exopolysaccharide production for the hyperthermophilic archaeon Thermococcus litoralis and bacterium Thermotoga maritima. Biotechnol Bioeng 69:537–547

    Article  CAS  Google Scholar 

  • Roane TM (1999) Lead resistance in two bacterial isolates from heavy metal contaminated soils. Microb Ecol 37:218–224

    Article  CAS  Google Scholar 

  • Roger O, Kervarec N, Ratiskol J, Colliec-Jouault S, Chevolot L (2004) Structural studies of the main exopolysaccharide produced by the deep-sea bacterium Alteromonas infernus. Carbohydr Res 339:2371–2380

    Article  CAS  Google Scholar 

  • Ron EZ, Rosenberg E (1999) Natural roles of biosurfactants. Environ Microbiol 3:229–236

    Article  Google Scholar 

  • Rosenberg E, Ron EZ (1999) High-and low-molecular-mass microbial surfactants. Appl Microbiol Biotechnol 52(2):154–162

    Article  CAS  Google Scholar 

  • Rougeaux H, Talaga P, Carlson RW, Guezennec J (1998) Structural studies of an exopolysaccharide produced by Alteromonas macleodii subsp. fijiensis originating from a deep-sea hydrothermal vent. Carbohydr Res 312:53–59

    Article  CAS  Google Scholar 

  • Rougeaux H, Guezennec J, Carlson RW, Kervarec N, Pichon R, Talaga P (1999a) Structural determination of the exopolysaccharide of Pseudoalteromonas strain HYD 721 isolated from a deep-sea hydrothermal vent. Carbohydr Res 315:273–285

    Article  CAS  Google Scholar 

  • Rougeaux H, Kervarec N, Pichon R, Guezennec J (1999b) Structure of the exopolysaccharide of Vibrio diabolicus isolated from a deep-sea hydrothermal vent. Carbohydr Res 322:40–45

    Article  CAS  Google Scholar 

  • Ruas-Madiedo P, De Los Reyes-Gavilán CG (2005) Invited review: methods for the screening, isolation, and characterization of exopolysaccharides produced by lactic acid bacteria. J Dairy Sci 88(3):843–856

    Article  CAS  Google Scholar 

  • Sakamoto N, Kano N, Imaizumi H (2008) Biosorption of uranium and rare earth elements using biomass of algae. Bioinorg Chem Appl 1–8. doi:10.1155/2008/706240

  • Satpute SK, Banat IM, Dhakephalkar PK, Banpurkar AG, Chopade BA (2010) Biosurfactants, bioemulsifiers and exopolysaccharides from marine microorganisms. Biotechnol Adv 28:436–450

    Article  CAS  Google Scholar 

  • Schiano Moriello V, Lama L, Poli A, Gugliandolo C, Maugeri TL, Gambacorta A, Nicolaus B (2003) Production of exopolysaccharides from a thermophilic microorganism isolated from a marine hot spring in flegrean areas. J Ind Microbiol Biotechnol 30:95–101

    Article  CAS  Google Scholar 

  • Schreiber DR, Millero FJ, Gordon AS (1990) Production of an extracellular copper-binding compound by the heterotrophic marine bacterium Vibrio alginolyticus. Mar Chem 28(4):275–284

    Article  CAS  Google Scholar 

  • Shah V, Ray A, Garg N, Madamwar D (2000) Characterization of the extracellular polysaccharide produced by a marine cyanobacterium, Cyanothece sp. ATCC 51142, and its exploitation toward metal removal from solutions. Curr Microbiol 40(4):274–278

    Google Scholar 

  • Senni K, Pereira J, Gueniche F, Delbarre-Ladrat C, Sinquin C, Ratiskol J ... Colliec-Jouault S (2011) Marine polysaccharides: a source of bioactive molecules for cell therapy and tissue engineering. Marine Drug 9(9):1664–1681

    Google Scholar 

  • Singh P, Cameotra SS (2004) Enhancement of metal bioremediation by use of microbial surfactants. Biochem Biophys Res Commun 319:291–297

    Article  CAS  Google Scholar 

  • Singh S, Pradhan S, Rai LC (1998) Comparative assessment of Fe3+ and Co+ biosorption by field and laboratory-grown Microcystis. Process Biochem 33(495):504

    Google Scholar 

  • Stahl A, Pletzer D, Mehmood A, Ullrich MS (2015) Marinobacter adhaerens HP15 harbors two CzcCBA efflux pumps involved in zinc detoxification. Antonie Van Leeuwenhoek 108(3):649–658

    Article  CAS  Google Scholar 

  • Steigedal M, Sletta H, Moreno S, Maerk M, Christensen BE, Bjerkan T et al (2008) The Azotobacter vinelandii AlgE mannuronan C-5-epimerase family is essential for the in vivo control of alginate monomer composition and for functional cyst formation. Environ Microbiol 10:1760–1770

    Article  CAS  Google Scholar 

  • Trincone A (2010) Potential biocatalysts originating from sea environments. J Mol Catal B Enzym 66(3):241–256

    Article  CAS  Google Scholar 

  • Valls M, de Lorenzo V (2002) Exploiting the genetic and biochemical capacities of bacteria for the remediation of heavy metal pollution. FEMS Microbiol Rev 26:327–338

    Article  CAS  Google Scholar 

  • Van Hullebusch ED, Zandvoort MH, Lens PNL (2003) Metal immobilization by biofilms: mechanisms and analytical tools. Rev Environ Sci Biotechnol 2:9–33

    Article  Google Scholar 

  • Vanfossen AL, Lewis DL, Nichols JD, Kelly RM (2008) Polysaccharide degradation and synthesis by extremely thermophilic anaerobes. Ann NY Acad Sci 1125:322–337

    Article  CAS  Google Scholar 

  • Verdugo P, Alldredge AL, Azam F, Kirchman DL, Passow U, Santschi PH (2004) The role of marine gel-phase on carbon cycling in the ocean. Mar Chem 92:65–66

    Article  CAS  Google Scholar 

  • Vieira RH, Volesky B (2010) Biosorption: a solution to pollution? Int Microbiol 3(1):17–24

    Google Scholar 

  • Vincent P, Pignet P, Talmont F, Bozzi L, Fournet B, Guezennec J (1994) Production and characterization of an exopolysaccharide excreted by a deep-sea hydrothermal vent bacterium isolated from the polychaete annelid Alvinella pompejana. Appl Environ Microbiol 60:4134–4141

    CAS  Google Scholar 

  • Von Canstein H, Li Y, Leonhäuser J, Haase E, Felske A, Deckwer WD, Wagner-Döbler I (2002) Spatially oscillating activity and microbial succession of mercury-reducing biofilms in a technical-scale bioremediation system. Appl Environ Microbiol 68(4):1938–1946

    Article  CAS  Google Scholar 

  • Vyrides I, Stuckey DC (2009) Adaptation of anaerobic biomass to saline conditions: Role of compatible solutes and extracellular polysaccharides. Enzym Microb Technol 44(1):46–51

    Article  CAS  Google Scholar 

  • Watanabe M, Kawahara K, Sasaki K, Noparatnaraporn N (2003) Biosorption of cadmium ions using a photosynthetic bacterium, Rhodobacter sphaeroides S and a marine photosynthetic bacterium. Rhodobacter sphaeroides S and their biosorption kinetics. J Biosci Bioeng 95(4):374–378

    Article  CAS  Google Scholar 

  • Wolfaardt GM, Lawrence JR, Korber DR (1999) Function of EPS. In: Microbial extracellular polymeric substances. Springer, Berlin, pp 171–200

    Google Scholar 

  • Wu Y, Xia L, Yu Z, Shabbir S, Kerr PG (2013) In situ bioremediation of surface waters by periphytons. Bioresour Technol 151:367–372

    Article  CAS  Google Scholar 

  • Zanchetta P, Lagarde N, Guezennec J (2003) A new bone-healing material: a hyaluronic acid-like bacterial exopolysaccharide. Calcif Tissue Int 72(1):74–79

    Article  CAS  Google Scholar 

  • Zhang W, Chen L, Liu D (2012) Characterization of a marine-isolated mercury-resistant Pseudomonas putida strain SP1 and its potential application in marine mercury reduction. Appl Microbiol Biotechnol 93(3):1305–1314

    Article  CAS  Google Scholar 

  • Zou W, Laferriere CA, Jennings HJ (1998) Oligosaccharide fragments of the type III group B streptococcal polysaccharide derived from S. pneumoniae type 14 capsular polysaccharide by a chemoenzymatic method. Carbohydr Res 309(3):297–301

    Article  CAS  Google Scholar 

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Acknowledgments

Dr.P.V. Bramhachari gratefully acknowledges DST-SERB, Government of India for financial support under the Grant No: SR/FT/LS-109-2011

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  1. Department of Biotechnology and Botany, Krishna University, Machilipatnam, 521001, Andhra Pradesh, India

    P. V. Bramhachari

  2. Department of Hematology and Medical Oncology, Winship Cancer Institute, Emory University, Atlanta, GA, 30322, USA

    Ganji Purnachandra Nagaraju

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  1. Department of Microbiology, Goa University Department of Microbiology, Goa, Goa, India

    Milind Mohan Naik

  2. Department of Microbiology, Goa University Department of Microbiology, Goa, Goa, India

    Santosh Kumar Dubey

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Bramhachari, P.V., Nagaraju, G.P. (2017). Extracellular Polysaccharide Production by Bacteria as a Mechanism of Toxic Heavy Metal Biosorption and Biosequestration in the Marine Environment. In: Naik, M., Dubey, S. (eds) Marine Pollution and Microbial Remediation. Springer, Singapore. https://doi.org/10.1007/978-981-10-1044-6_5

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