Advertisement

Journal of Industrial Microbiology & Biotechnology

, Volume 46, Issue 12, pp 1657–1667 | Cite as

Characterization of the microbiota in long- and short-term natural indigo fermentation

  • Zhihao Tu
  • Helena de Fátima Silva Lopes
  • Kensuke Igarashi
  • Isao YumotoEmail author
Fermentation, Cell Culture and Bioengineering - Original Paper

Abstract

The duration for which the indigo-reducing state maintenance in indigo natural fermentation in batch dependent. The microbiota was analyzed in two batches of sukumo fermentation fluids that lasted for different durations (Batch 1: less than 2 months; Batch 2: nearly 1 year) to understand the mechanisms underlying the sustainability and deterioration of this natural fermentation process. The transformation of the microbiota suggested that the deterioration of the fermentation fluid is associated with the relative abundance of Alcaligenaceae. Principal coordinates analysis (PCoA) showed that the microbial community maintained a very stable state in only the long-term Batch 2. Therefore, entry of the microbiota into a stable state under alkaline anaerobic condition is an important factor for maintenance of indigo fermentation for long duration. This is the first report on the total transformation of the microbiota for investigation of long-term maintenance mechanisms and to address the problem of deterioration in indigo fermentation.

Keywords

Indigo reduction Natural fermentation Next-generation sequencing Alcaligenaceae Alkalibacterium Amphibacillus 

Notes

Funding

This work was funded by the Japan Society for the Promotion of Science (Grant No. 2357012 and 16K07684).

Supplementary material

10295_2019_2223_MOESM1_ESM.docx (30 kb)
Supplementary material 1 (DOCX 30 kb)

References

  1. 1.
    Aino K, Hirota K, Okamoto T, Tu Z, Matsuyama H, Yumoto I (2018) Microbial communities associated with indigo fermentation that thrive in anaerobic alkaline environments. Front Microbiol 9:1–16CrossRefGoogle Scholar
  2. 2.
    Aino K, Narihiro T, Minamida K, Kamagata Y, Yoshimune K, Yumoto I (2010) Bacterial community characterization and dynamics of indigo fermentation. FEMS Microbiol Ecol 74:174–183CrossRefGoogle Scholar
  3. 3.
    Blackburn RS, Bechtold T, John P (2009) The development of indigo reduction methods and pre-reduced indigo products. Coloration Technol 125:193–207CrossRefGoogle Scholar
  4. 4.
    Božič M, Kokol V (2008) Ecological alternatives to the reduction and oxidation processes in dyeing with vat and sulphur dyes. Dyes Pigm 76:299–309CrossRefGoogle Scholar
  5. 5.
    Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Pena AG, Goodrich JK, Gordon JI, Huttley GA (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7:335–336CrossRefGoogle Scholar
  6. 6.
    Cardon D (2007) Natural dyes-sources, tradition. Technology and Science. Archetype Publications Ltd., LondonGoogle Scholar
  7. 7.
    Fuller SJ, McMillan DGG, Renz MB, Shmit M, Burke IT, Stewart DI (2014) Extracellular electron transport-mediated Fe(III) reduction by a community of alkaliphilic bacteria that use flavins as electron shuttle. Appl Environ Microbiol 80:128–137CrossRefGoogle Scholar
  8. 8.
    Fuller SJ, Burke IT, McMillan DGG, Ding W, Stewart DI (2015) Population changes in a community of alkaliphilic iron-reducing bacteria due to changes in the electron acceptor: implications for bioremediation at alkaline Cr(VI)-contaminated sites. Water Air Soil Pollut 226:180CrossRefGoogle Scholar
  9. 9.
    Gorlenko V, Tsapin A, Namsaraev Z, Teal T, Tourova T, Engler D et al (2004) Anaerobranca californiensis sp. nov., an anaerobic alkalithermophilic ferementative bacterium isolated from a hot spring on Mono Lake. Int J Syst Evol Microbiol 54:739–743CrossRefGoogle Scholar
  10. 10.
    Hartl A, Gaibor ANP, van Bommel MR, Hofmann-de Keijzer R (2015) Searching for blue: experiments with woad fermentation vats and an explanation of the colours through dye analysis. J Archaeol Sci 2:9–39Google Scholar
  11. 11.
    Hirota K, Aino K, Nodasaka Y, Yumoto I (2013) Oceanobacillus indicireducens sp. nov., a facultative alkaliphile that reduces an indigo dye. Int J Syst Evol Microbiol 63:1437–1442CrossRefGoogle Scholar
  12. 12.
    Hirota K, Aino K, Nodasaka Y, Morita N, Yumoto I (2013) Amphibacillus indicireducens sp. nov., an alkaliphile that reduces an indigo dye. Int J Syst Evol Microbiol 63:464–469CrossRefGoogle Scholar
  13. 13.
    Hirota K, Aino K, Yumoto I (2013) Amphibacillus iburiensis sp. nov., an alkaliphile that reduces an indigo dye. Int J Syst Evol Microbiol 63:4303–4308CrossRefGoogle Scholar
  14. 14.
    Hirota K, Aino K, Yumoto I (2016) Fermentibacillus polygonigen nov., sp. nov., an alkaliphile that reduces indigo dye. Int J Syst Evol Microbiol 66:2247–2253CrossRefGoogle Scholar
  15. 15.
    Hirota K, Nishita M, Matsuyama H, Yumoto I (2017) Paralkalibacillus indicireducens gen., nov., sp. nov., an indigo-reducing obligate alkaliphile isolated from indigo fermentation liquor used for dyeing. Int J Syst Evol Microbiol 67:4050–4056CrossRefGoogle Scholar
  16. 16.
    Hirota K, Nishita M, Tu Z, Matsuyama H, Yumoto I (2018) Bacillus fermenti sp. nov., an indigo-reducing obligate alkaliphile isolated from indigo fermentation liquor for dyeing. Int J Syst Evol Microbiol 68:1123–1129CrossRefGoogle Scholar
  17. 17.
    Hirota K, Okamoto T, Matsuyama H, Yumoto I (2016) Polygonibacillus indicireducens gen nov., sp. nov., an indigo-reducing and obligate alkaliphile isolated from indigo fermentation liquor for dyeing. Int J Syst Evol Microbiol 66:4650–4656CrossRefGoogle Scholar
  18. 18.
    Hobbie SN, Li X, Basen M, Stingl U, Brune A (2012) Humic substance-mediated Fe(III) reduction by a fermenting Bacillus strain from the alkaline gut of humus-feeding scarab beetle larva. Syst Appl Microbiol 35:226–232CrossRefGoogle Scholar
  19. 19.
    Jung JY, Lee SH, Lee HJ, Jeon CO (2013) Microbial succession and metabolite changes during fermentation of saeu-jeot: traditional Korean salted seafood. Food Microbiol 34:360–368CrossRefGoogle Scholar
  20. 20.
    Jung JY, Lee HJ, Chun BH, Jeon CO (2016) Effect of temperature on bacterial communities and metabolites during fermentation of myeolchi-aekjeot, a traditional Korean fermented anchovy sauce. PLoS One 11:e0151351CrossRefGoogle Scholar
  21. 21.
    Kano R, Kobayashi Y, Nishikawa A, Murata R, Itou T, Ito T, Suzuki K, Kamata H (2018) Next-generation sequencing analysis of bacterial flora in bovine prototheca mastitic milk. Med Mycol J 59:41–46CrossRefGoogle Scholar
  22. 22.
    Klindworth A, Pruesse E, Schweer T, Peplies J, Quast C, Horn M, Glöckner FO (2013) Evaluation of general 16S ribosomal RNA gene PCR primers for classical and next-generation sequencing-based diversity studies. Nucleic Acids Res 41:1–11CrossRefGoogle Scholar
  23. 23.
    Liu CG, Xue C, Lin YH, Bai FW (2013) Redox potential control and applications in microaerobic and anaerobic fermentations. Biotechnol Adv 31:257–265CrossRefGoogle Scholar
  24. 24.
    Li S, Cunningham AB, Fan R, Wang Y (2019) Identity blues: the ethnobotany of the indigo dyeing by Landian Yao (Iu Mien) in Yunnan, Southwest China. J Ethnobiol Ethnomed 15:13CrossRefGoogle Scholar
  25. 25.
    Lucena-Padrós H, Ruiz-Barba JL (2016) Diversity and enumeration of halophilic and alkaliphilic bacteria in Spanish-style green table-olive fermentations. Food Microbiol 53:53–62CrossRefGoogle Scholar
  26. 26.
    Lee MH, Li FZ, Lee J, Kang J, Lim S, Nam YD (2017) Next-generation sequencing analyses of bacterial community structures in soybean pastes produced in Northeast China. J Food Sci 82:960–968CrossRefGoogle Scholar
  27. 27.
    Milanović V, Osimani A, Taccari M, Garofalo C, Butta A, Clementi F, Aquilanti L (2017) Insight into the bacterial diversity of fermentation woad dye vats as revealed by PCR-DGGE and pyrosequencing. J Ind Microbiol Biotechnol 44:997–1004CrossRefGoogle Scholar
  28. 28.
    Nakajima K, Hirota K, Nodasaka Y, Yumoto I (2005) Alkalibacterium iburiense sp. nov., an obligate alkaliphile that reduces an indigo dye. Int J Syst Evol Microbiol 55:1525–1530CrossRefGoogle Scholar
  29. 29.
    Nicholson SK, John P (2005) The mechanism of bacterial. Appl Microbial Biotechnol 68:117–123CrossRefGoogle Scholar
  30. 30.
    Okamoto T, Aino K, Narihiro T, Matsuyama H, Yumoto I (2017) Analysis of microbiota involved in the aged natural fermentation of indigo. World J Microbiol Biotechnol 33:70CrossRefGoogle Scholar
  31. 31.
    Osimani A, Aquilanti L, Baldini G, Silvestri G, Butta A, Clementi F (2012) Implementation of a biotechnological process for vat dyeing with woad. J Ind Microbiol Biotechnol 39:1309–1319CrossRefGoogle Scholar
  32. 32.
    Perkin, A.G.; Bloxam, W.P. CLXII. Indican. Part I Transactions. J. Chem. Soc. 1907, 91, 1715-1728Google Scholar
  33. 33.
    Rawat N, Joshi GK (2018) Bacterial community structure analysis of a hot spring soil by next generation sequencing of ribosomal RNA. Genomics.  https://doi.org/10.1016/j.ygeno.2018.06.008 CrossRefPubMedGoogle Scholar
  34. 34.
    Russell GA, Kaupp G (1969) Oxidation of carbanions. IV. Oxidation of indoxyl to indigo in basic solution. J Am Chem Soc 91:3851–3859CrossRefGoogle Scholar
  35. 35.
    Sakamoto N, Tanaka S, Sonomoto K, Nakayama J (2011) 16S rRNA pyrosequencing-based investigation of the bacterial community in nukadoko, a pickling bed of fermented rice bran. Int J Food Microbiol 144:352–359CrossRefGoogle Scholar
  36. 36.
    Singh G, Capalash N, Goel R, Sharma P (2007) A pH-stable laccase from alkali-tolerant γ-proteobacterium JB: purification, characterization and indigo carmine degradation. Enzyme Microbiol Technol 41:794–799CrossRefGoogle Scholar
  37. 37.
    Spitaels F, Wieme AD, Janssens M, Aerts M, Van Landschoot A, De Vuyst L, Vandamme P (2015) The microbial diversity of an industrially produced lambic beer shares members of a traditional produced one and reveals a core microbiota for lambic beer fermentation. Food Microbiol 49:23–32CrossRefGoogle Scholar
  38. 38.
    Visi DK, Souza ND, Ayre BG, Webber CL, Allen MS (2013) Investigation of the bacterial retting community of kenaf (Hibiscus cannabinus) under different conditions using next-generation semiconductor sequencing. J Ind Microbiol Biotechnol 40:465–475CrossRefGoogle Scholar
  39. 39.
    Vuorema A (2008) Reduction and analysis methods of indigo. Dissertation thesis, Department of Chemistry, University of Turku, FinlandGoogle Scholar
  40. 40.
    Wang X, Du H, Xu Y (2017) Source tracking of prokaryotic communities in fermented grain of Chinese strong-flavor liquor. Int J Food Microbiol 244:27–35CrossRefGoogle Scholar
  41. 41.
    Yumoto I, Hirota K, Nodasaka Y, Yokota Y, Hoshino T, Nakajima K (2004) Alkalibacterium psychrotolerans sp. nov., a psychrotolerant obligate alkaliphile that reduces an indigo dye. Int J Syst Evol Microbiol 54:2379–2383CrossRefGoogle Scholar
  42. 42.
    Yumoto I, Hirota K, Nodasaka Y, Tokiwa Y, Nakajima K (2008) Alkalibacterium indicireducens sp. nov., an obligate alkaliphile that reduces indigo dye. Int J Syst Evol Microbiol 58:901–905CrossRefGoogle Scholar
  43. 43.
    Yavuz M, Kaya G, Aytekin Ҫ (2014) Using Ceriporiopsis subvermispora CZ-3 laccase for indigo carmine decolorization and denim bleaching. Int Bioderion Biodegr 88:199–205CrossRefGoogle Scholar

Copyright information

© Society for Industrial Microbiology and Biotechnology 2019

Authors and Affiliations

  1. 1.Graduate School of AgricultureHokkaido UniversitySapporoJapan
  2. 2.Bioproduction Research InstituteNational Institute of Advanced Industrial Science and TechnologySapporoJapan

Personalised recommendations