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Current Microbiology

, Volume 76, Issue 5, pp 527–535 | Cite as

Microbial Diversity Profiling of Polysaccharide (gum)-Producing Bacteria Isolated from a South African Sugarcane Processing Factory

  • Sanet Nel
  • Stephen B. Davis
  • Akihito Endo
  • Leon M. T. DicksEmail author
Article
  • 96 Downloads

Abstract

Polysaccharide (gum)-producing bacteria are responsible for severe economic losses in the sugarcane processing industry. Increased polysaccharide levels in raw sugar are normally an indication that biodeterioration occurred in the cane, soon after harvesting. Once in the sugar processing plant, the cell numbers of gum-producing bacteria escalate and may reach levels difficult to control. We have isolated 430 gum-producing bacteria from sugarcane and different sampling points in a South African sugarcane processing factory. As expected, high cell numbers of gum-producing bacteria were isolated from the factory during a time when sugar with a high dextran content was produced. What we did not expect was to find the same species in the factory at a time when sugar with a low dextran content was produced. Phylogenetic analyses of the 16S rRNA gene sequences differentiated the gum-producing bacteria into four genera and nine species. The majority of these isolates belonged to the genus Weissella (47%), followed by members of Bacillus (24%), Leuconostoc (19%) and Lactobacillus (10%). For the first time, we report on the isolation of Weissella confusa, Weissella cibaria and Bacillus amyloliquefaciens from a sugarcane processing factory.

Notes

Acknowledgements

The authors acknowledge and thank Dr Deborah Sweby (South African Sugarcane Research Institute, Mt Edgecombe, South Africa) for the DNA sequencing analysis.

Supplementary material

284_2018_1625_MOESM1_ESM.docx (196 kb)
Supplementary material 1 (DOCX 196 KB)

References

  1. 1.
    Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410CrossRefGoogle Scholar
  2. 2.
    Anon (2015) ICUMSA method GS1/2/9–15 the determination of dextran in raw sugar by a modified alcohol haze method—accepted. In: ICUMSA Method Book. Verlag Dr Albert Bartens KG, BerlinGoogle Scholar
  3. 3.
    Antier P (1996) Microbiological control in a cane sugar mill: implications on sugar quality and on losses. Proc S Afr Sug Technol Ass 70:185–188Google Scholar
  4. 4.
    Bacci JC, Guichard V (1994) Some aspects of cane deterioration in Reunion Island. Proc S Afr Sug Technol Ass 68:97–100Google Scholar
  5. 5.
    Ben Amor K, Vaughan EE, de Vos WM (2007) Advanced molecular tools for the identification of lactic acid bacteria. J Nutr 137(3):741S–747SCrossRefGoogle Scholar
  6. 6.
    Berendsen EM, Koning RA, Boekhorst J, de Jong A, Kuipers OP, Wells-Bennik MHJ (2016) High-level heat resistance of spores of Bacillus amyloliquefaciens and Bacillus licheniformis results from the presence of a spoVA operon in a Tn1546 transposon. Front Microbiol 7:10.  https://doi.org/10.3389/fmicb.2016.01912 CrossRefGoogle Scholar
  7. 7.
    Bevan D, Bond J (1971) Microorganisms in field and mill—a preliminary study. Proc Qld Soc Sugar Cane Technol 38:137–143Google Scholar
  8. 8.
    Chirife J, Herszage L, Joseph A, Kohn ES (1983) In vitro study of bacterial growth inhibition in concentrated sugar solutions: microbiological basis for the use of sugar in treating infected wounds. Antimicrob Agents Chemother 23(5):766–773CrossRefGoogle Scholar
  9. 9.
    Clarridge JE (2004) Impact of 16S rRNA gene sequence analysis for identification of bacteria on clinical microbiology and infectious diseases. Clin Microbiol Rev 17(4):840–862CrossRefGoogle Scholar
  10. 10.
    Collins MD, Samelis J, Metaxopoulos J, Wallbanks S (1993) Taxonomic studies on some leuconostoc-like organisms from fermented sausages: description of a new genus Weissella for the Leuconostoc paramesenteroides group of species. J Appl Bacteriol 75:595–603CrossRefGoogle Scholar
  11. 11.
    Cuddihy JA Jr, Porro ME, Raiih JS (2001) The presence of total polysaccharides in sugar production and methods for reducing their negative effects. J Am Soc Sug Cane Technol 21:73–91Google Scholar
  12. 12.
    Dogsa I, Brloznik M, Stopar D, Mandic-Mulec I (2013) Exopolymer diversity and the role of levan in Bacillus subtilis biofilms. PLoS ONE 8(4):e62044.  https://doi.org/10.1371/jpurnal.pone.0062044 CrossRefGoogle Scholar
  13. 13.
    Egan B (1968) Post-harvest deterioration losses in sugarcane in Queensland. Proc Int Soc Sug Cane Technol 13:1729–1735Google Scholar
  14. 14.
    Egan BT, Rehbein CA (1963) Bacterial deterioration of mechanically harvested cut-up sugar cane during storage over weekends. Proc Qld Soc Sug Cane Technol 30:11–25Google Scholar
  15. 15.
    Eggleston G, Grisham M (2003) Oligosaccharides in cane and their formation on cane deterioration. In: Eggleston G, Côté G (eds) Oligosaccharides in food and agriculture. American Chemical Society, Washington, DC, pp 211–232CrossRefGoogle Scholar
  16. 16.
    Eggleston G, Harper W (2006) Determination of sugarcane deterioration at the factory: development of a rapid, easy and inexpensive enzymatic method to measure mannitol. Food Chem 98:366–372CrossRefGoogle Scholar
  17. 17.
    Eggleston G, Legendre BL, Tew T (2005) New insights on factory indicators of freeze deteriorated cane. Proc Int Soc Sug Cane Technol 25:9–24Google Scholar
  18. 18.
    Eggleston G, Monge A, Montes B, Stewart D (2009) Application of dextranases in sugarcane factory: overcoming practical problems. Sugar Technol 11(2):135–141CrossRefGoogle Scholar
  19. 19.
    Eggleston G, Morel du Boil PG, Walford SN (2008) A review of sugarcane deterioration in the United States and South Africa. Proc S Afr Sug Technol Ass 81:72–85Google Scholar
  20. 20.
    Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791CrossRefGoogle Scholar
  21. 21.
    Foster DH, Inkerman PA, McNeil K (1980) Studies on cane deterioration in Australia. Proc Int Soc Sug Cane Technol 17:2204–2220Google Scholar
  22. 22.
    Godshall MA, Legendre BL, Clarke MA, Miranda XM, Blanco RS (1996) Starch, polysaccharides and proanthocyanidin in Louisiana sugarcane varieties. Int Sugar J 98(1168E):144–148Google Scholar
  23. 23.
    Green MR, Sambrook J (2012) Molecular cloning. A laboratory manual, vol 3, 4th edn. Cold Spring Harbor Laboratory Press, Cold Spring HarborGoogle Scholar
  24. 24.
    Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucl Acids Symp Ser 41:95–98Google Scholar
  25. 25.
    Hector S, Willard K, Bauer R, Mulako I, Slabbert E, Kossmann J, George GM (2015) Diverse exopolysaccharide producing bacteria isolated from milled sugarcane: implications for cane spoilage and sucrose yield. PLoS ONE 10(12):1–10.  https://doi.org/10.1371/journal.pone.0145487 CrossRefGoogle Scholar
  26. 26.
    Hong S, Farrance CE (2015) Is it essential to sequence the entire 16S rRNA gene for bacterial identification? Am Pharm Rev 18(7):13 ppGoogle Scholar
  27. 27.
    Imrie FKE, Tilbury RH (1972) Polysaccharides in sugar cane and its products. Sugar Technol Rev 1:291–361Google Scholar
  28. 28.
    Janda JM, Abbott SL (2007) 16S rRNA gene sequencing for bacterial identificaiton in the diagnostic laboratory: pluses, perils and pitfalls. J Clin Microbiol 45(9):2761–2764CrossRefGoogle Scholar
  29. 29.
    Jimenez ER (2005) The dextranase along sugar-making industry. Biotecnologia Aplicada 22:20–27Google Scholar
  30. 30.
    Kalidass N, Singh I, Steyn AB (1996) An investigation into the low pol factor and the purity difference between mixed juice and cane (DAC) at the Transvaal Suiker Beperk Malelane factory. Proc S Afr Sug Technol Ass 70:179–184Google Scholar
  31. 31.
    Khalikova E, Susi P, Korpela T (2005) Microbial dextran-hydrolysing enzymes: fundamentals and applications. Microbiol Mol Biol Rev 69(2):306–325CrossRefGoogle Scholar
  32. 32.
    Kimura M (1980) A simple method for estimating evolutionary rate of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16:111–120CrossRefGoogle Scholar
  33. 33.
    Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874CrossRefGoogle Scholar
  34. 34.
    Lane DJ (1991) 16S/23S rRNA sequencing. In: Stackebrandt E, Goodfellow M (eds) Nucleic acid techniques in bacterial systematics. Wiley, New YorkGoogle Scholar
  35. 35.
    Leemhuis H, Pijning T, Dobruchowska JM, van Leeuwen SS, Kralj S, Dijkstra BW, Dijkhuizen L (2013) Glucansucrases: three-dimensional structures, reactions, mechanism, α-glucan analysis and their implications in biotechnology and food applications. J Biotechnol 163:250–272CrossRefGoogle Scholar
  36. 36.
    Lillehoj E, Clarke M, Tsang W (1984) Leuconostoc spp. in sugarcane processing samples. Proc Sug Proc Res Conf 1984:141–151Google Scholar
  37. 37.
    Lionnet GRE (1986) Post-harvest deterioration of whole stalk sugarcane. Proc S Afr Sug Technol Ass 60:52–557Google Scholar
  38. 38.
    Lionnet GRE (1996) Mud filtration. Proc S Afr Sug Technol Ass 70:280–282Google Scholar
  39. 39.
    Logan NA, De Vos P (2009) The Firmicutes. In: De Vos P, Garrity GM, Jones D et al (eds) Bergey’s Manual of Systematic Bacteriology, vol 3, 2nd edn. Springer, New York, p 1450Google Scholar
  40. 40.
    Mackrory LM, Cazalet JS, Smith IA (1984) A comparison of the microbiological activity associated with milling and cane diffusion. Proc S Afr Sug Technol Ass 58:86–89Google Scholar
  41. 41.
    Malang SK, Maina NH, Schwab C, Tenkanen M, Lacroix C (2015) Characterisation of exopolysaccharide and ropy capsular polysaccharide formation by Weissella. Food Microbiol 46:418–427CrossRefGoogle Scholar
  42. 42.
    Margosch D, Ehrmann MA, Buckow R, Heinz V, Vogel RF, Gänzle MG (2006) High-pressure-mediated survival of Clostridium botulinum and Bacillus amyloliquefaciens endospores at high temperature. Appl Environ Microbiol 72(5):3476–3481CrossRefGoogle Scholar
  43. 43.
    McNeil K, Bond J (1980) The identification, enumeration and properties of microflora of sugarcane, cane juice and processing liquors. Sug Res Inst Tech Rep (Mackay) (154):78 ppGoogle Scholar
  44. 44.
    Moodley M, Khomo N (2018) Dextran: a refiner’s perspective. Proc S Afr Sug Technol Ass 91:318–329Google Scholar
  45. 45.
    Morel du Boil PG (1995) Cane deterioration - oligosaccharide formation and some processing implications. Proc S Afr Sug Technol Ass 69:146–154Google Scholar
  46. 46.
    Morel du Boil PG, Wienese S (2002) Enzymatic reduction of dextran in process—laboratory evaluation of dextranases. Proc S Afr Sug Technol Ass 76:435–443Google Scholar
  47. 47.
    Morel du Boil PG, Wienese S, Schoonees BM (2005) The cause of sarkaran in sugarcane. Proc S Afr Sug Technol Ass 79:48–62Google Scholar
  48. 48.
    Odeniyi OA, Amoo OT (2015) Effect on environmental variables on biofilm formation by selected Gram-positive bacteria. NY Sci J 8(2):62–69Google Scholar
  49. 49.
    Patel JB (2001) 16S rRNA gene sequencing for bacterial pathogen identification in the clinical laboratory. Mol Diagn 6:313–321CrossRefGoogle Scholar
  50. 50.
    Perry LA, Hunter C, Watt DA (2007) Impact of post-harvest delays and temperature on cane deterioration. Proc Int Soc Sug Cane Technol 26:1026–1030Google Scholar
  51. 51.
    Rainey TJ, Thaval OP, Rackemann DW (2014) Developments in mud filtration technology in the sugarcane industry. In: Webb E (ed) Sugarcane: production, consumption and agricultural management systems. Nova Science Publishers Inc., New York, pp 263–292Google Scholar
  52. 52.
    Rein P (2007) Cane sugar engineering. Verlag Dr. Albert Bartens KG, BerlinGoogle Scholar
  53. 53.
    Rein PW (1995) A comparison of cane diffusion and milling. Proc S Afr Sug Technol Ass 69:196–200Google Scholar
  54. 54.
    Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425Google Scholar
  55. 55.
    Solomon S (2009) Post-harvest deterioration of sugarcane. Sugar Tech 11(2):109–123CrossRefGoogle Scholar
  56. 56.
    Solomon S (2000) Post-harvest deterioration of sugarcane and its milling consequences. Sugar Tech 2(1&2):1–18CrossRefGoogle Scholar
  57. 57.
    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):4673–4680CrossRefGoogle Scholar
  58. 58.
    Tian F, Inthanavong L, Karboune S (2011) Purification and characterisation of levansucrases from Bacillus amyloliquefaciens in intra- and extracellular forms uselful for the synthesis of levan and fructooligosaccharides. Biosci Biotechnol Biochem 75(10):1929–1938CrossRefGoogle Scholar
  59. 59.
    Tilbury R (1970) Biodeterioration of harvested sugarcane in Jamaica. University of Aston, BirminghamGoogle Scholar
  60. 60.
    Torino MI, Font de Valdez G, Mozzi F (2015) Biopolymers from lactic acid bacteria. Novel applications in foods and beverages. Front Microbiol 6:834.  https://doi.org/10.3389/fmicb.2015.00834 CrossRefGoogle Scholar
  61. 61.
    Tsuchiya HM, Koepsell HJ, Corman J, Bryant G, Bogard MO, Feger VH, Jackson RW (1952) The effect of certain cultural factors on production of dextransucrase by Leuconostoc mesenteroides. J Bacteriol 64:521–526Google Scholar
  62. 62.
    Turner S, Pryer KM, Miao VPW, Palmer JD (1999) Investigating deep phylogenetic relationships among cyanobacteria and plastids by small subunit rRNA sequence analysis. J Euk Microbiol 46:327–338CrossRefGoogle Scholar
  63. 63.
    van Hijum SAFT, Kralj S, Ozimek LK, Dijkhuizen L, Ineke GH, van Geel-Schutten IGH (2006) Structure-function relationships of glucansucrase and fructansucrase enzymes from lactic acid bacteria. Microbiol Mol Biol Rev 70(1):157–176CrossRefGoogle Scholar
  64. 64.
    Warth AD (1978) Relationships between the heat resistance of spores and the optimum and maximum growth temperatures of Bacillus species. J Bacteriol 134(3):699–705Google Scholar
  65. 65.
    Wolf BF, Fogler HS (2004) Growth of Leuconostoc mesenteroides NRRL-B523 in an alkaline medium: suboptimal pH growth inhibition of a lactic acid bacterium. Biotechnol Bioeng 89(1):96–101CrossRefGoogle Scholar
  66. 66.
    Wood RA (1976) Cane deterioration as affected by billet size, delay in milling and other factors. Proc S Afr Sug Technol Ass 50:12–17Google Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2019

Authors and Affiliations

  • Sanet Nel
    • 1
    • 2
  • Stephen B. Davis
    • 1
  • Akihito Endo
    • 3
  • Leon M. T. Dicks
    • 2
    Email author
  1. 1.Sugar Milling Research Institute NPCc/o University of KwaZulu-NatalDurbanSouth Africa
  2. 2.Department of MicrobiologyStellenbosch UniversityStellenboschSouth Africa
  3. 3.Department of Food, Aroma and Cosmetic ChemistryTokyo University of AgricultureHokkaidoJapan

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