SpringerLink
Log in

Analysis of microbiota involved in the aged natural fermentation of indigo

  • Original Paper
  • Published:
World Journal of Microbiology and Biotechnology Aims and scope Submit manuscript

Abstract

Although the indigo reduction process is performed via natural fermentation and maintained under open-air condition, the indigo-reducing reactions continue for 6 months (on average) or longer. Identifying the mechanism underlying the maintenance of this process could lead to the development of a novel, long-lasting, unsterilized bioprocesses. To determine the mechanisms underlying the maintenance of the indigo fermentation system microbiota for more than 6 months in a reduced state in an anaerobic alkaline environment, we examined changes in the microbiota in one early-phase batch and two aged batches of indigo fermentation fluid. The microbiota in the aged fermentation fluid consisted mainly of the genera Alkalibacterium, Amphibacillus, Anaerobacillus and Polygonibacillus and the family Proteinivoraceae. The genera Alkalibacterium, Amphibacillus and Polygonibacillus are known to include indigo-reducing bacteria. Although the transition speed was slower in the aged fermentation fluid than in the early-stage fluid, the microbiota in the aged fermentation fluid maintained for more than 6 months was drastically changed within a period of 3 months. The results of this study indicate that the bacterial consortia consisted of various indigo-reducing species that replace the previous group of indigo-reducing bacteria. The notable transitional changes may be concomitant with changes in the environmental conditions, such as the nutritional conditions, observed over 3 months. This flexibility may lead to important changes in the microbiota that allow for the maintenance of a fermentation-reducing state over a long period.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Subscribe and save

Springer+ Basic
EUR 32.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or Ebook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Aino K, Narihiro T, Minamida K, Kamagata Y, Yoshimune K, Yumoto I (2010) Bacterial community characterization and dynamics of indigo fermentation. FEMS Microbiol Ecol 74:174–183

    Article  CAS  Google Scholar 

  • Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410

    Article  CAS  Google Scholar 

  • Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK et al (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7:335–336

    Article  CAS  Google Scholar 

  • Clark RJH, Cooksey CJ, Daniels MAM, Withnall R (1993) Indigo, woad, and Tyrian purple: important vat dyes from antiquity to the present. Endeavour 17:191–199

    Article  CAS  Google Scholar 

  • Edger RC (2010) Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26:2460–2461

    Article  Google Scholar 

  • Farrow JAE, Lawson PA, Hippe H, Gauglitz U, Collins MD (1995) Phylogenetic evidence that the gram-negative nonsporulating bacterium Tissierella (Bacteroides) praeacuta is a member of the Clostridium subphylum of the gram-positive bacteria and description of Tissierella creatinini sp. nov. Int J Syst Bacteriol 45:436–440

    Article  CAS  Google Scholar 

  • Felsentein J (1985) Confidence limits on phylogenies: an approach using phylogenies: an approach using the bootstrap. Evol Int J org Evol 39:783–791

    Article  Google Scholar 

  • Fuller SJ, McMillan DGG, Renz MB, Schmidt 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 80:128–137

    Article  CAS  Google Scholar 

  • Guindon S, Gascuel O. (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52:696–704

    Article  Google Scholar 

  • Hirota K, Aino K, Nodasaka Y, Morita N, Yumoto I (2013a) Amphibacillus indicireducens sp. nov., an alkaliphile that reduces an indigo dye. Int J Syst Evol Microbiol 63:464–469

    Article  CAS  Google Scholar 

  • Hirota K, Aino K, Nodasaka Y, Yumoto I (2013b) Oceanobacillus indicireducens sp. nov., a facultatively alkaliphile that reduces an indigo dye. Int J Syst Evol Microbiol 63:1437–1442

    Article  Google Scholar 

  • Hirota K, Aino K, Yumoto I (2013c) Amphibacillus iburiensis sp. nov., an alkaliphile that reduces an indigo dye. Int J Syst Evol Microbiol 63:4303–4308

    Article  CAS  Google Scholar 

  • Hirota K, Aino K, Yumoto I (2016a) Fermentibacillus polygoni gen. nov., sp. nov., an alkaliphile that reduces indigo dye. Int J Syst Evol Microbiol 66:2247–2253

    Article  Google Scholar 

  • Hirota K, Okamoto T, Matsuyama H, Yumoto I (2016b) Polygonibacillus indicireducensgen, nov., sp. nov., an indigo-reducing and obligate alkaliphile isolated from indigo fermentation liquor for dyeing. Int J Syst Evol Microbiol. doi:10.1099/ijsem.0.001015

    Google Scholar 

  • 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 a humus-feeding scarab beetle larva. Syst Appl Microbiol 35:226–232

    Article  CAS  Google Scholar 

  • Kamagata Y (2015) Keys to cultivating uncultured microbes: elaborate enrichment strategies and resuscitation of dormant cells. Microb Environ 30:289–290

    Article  Google Scholar 

  • Kevbrin V, Boltyanskaya Y, Zhilina T, Kolganova T, Lavrentjeva E, Kuznetsov B (2013) Proteinivorax tanatarense gen. nov., sp. nov., an anaerobic, haloalkaliphilic, proteolytic bacterium isolated from a decaying algal bloom, and proposal of Proteinivoraceae fam. nov. Extremophiles 17:747–756

    Article  CAS  Google Scholar 

  • Kimura M (1980) A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16:111–120

    Article  CAS  Google Scholar 

  • Lucena-Padrós H, Ruiz-Barba JL (2016) Diversity and enumeration of halophilic and alkaliphilic bacteria in Spanish-style green table-olive fermentations. Food Microbiol 53:53–62

    Article  Google Scholar 

  • Mori K, Kamagata Y (2014) The challenges of studying the anaerobic microbial world. Microb Environ 29:335–337

    Article  Google Scholar 

  • 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 55:1525–1530

    Article  CAS  Google Scholar 

  • Narihiro T, Kamagata Y (2013) Cultivating yet-to-be cultivated microbes: the challenge continues. Microb Environ 28:163–165

    Article  Google Scholar 

  • Ono H, Nishio S, Tsurii J, Kawamoto T, Sonomoto K, Nakayama J (2014) Monitoring of the microbiota profile in nukadoko, a naturally fermented rice bran bed for pickling vegetables. J Bioci Bioeng 118:520–525

    Article  CAS  Google Scholar 

  • Padden AN, Dillon VM, John P, Edmonds J, Collins MD, Alvarez N (1998) Clostridium used in medieval dyeing. Nature 396:225

    Article  CAS  Google Scholar 

  • Padden AN, Dillon VM, Edmonds J, Collins MD, Alvarez N, John P (1999) An indigo-reducing moderate thermophile from a woad vat, Clostridium isatidis sp. nov. Int J Syst Bacteriol 49:1025–1031

    Article  CAS  Google Scholar 

  • Roth E, Schwenninger SM, Eugster-Meier E, Lacroix C (2011) Facultative anaerobic halophilic and alkaliphilic bacteria isolated from a natural smear ecosystem inhibit Listeria growth in early ripening stages. Int J Food Microbiol 147:26–32

    Article  Google Scholar 

  • Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425

    CAS  Google Scholar 

  • Schmidt H (1997) Indigo—100 Jahre industrielle synthese. Chem Uns Zeit 31:121–128

    Article  CAS  Google Scholar 

  • Takahara Y, Tanabe O (1960) Studies on the reduction of indigo in industrial fermentation vat (VII). J Ferment Technol 38:329–331

    CAS  Google Scholar 

  • Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: Molecular evolutionary genetic analysis version 6.0. Mol Biol Evol 30:2725–2729

    Article  CAS  Google Scholar 

  • 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. Nucl Acid Res 22:4673–4680

    Article  CAS  Google Scholar 

  • Tiago I, Pires C, Mendes V, Morais PV, da Costa MS, Veríssimo A (2006) Bacillus foraminis sp. nov., isolated from a non-saline alkaline groundwater. Int J Syst Evol Microbiol 56:2571–2574

    Article  CAS  Google Scholar 

  • Vázquez-Baeza Y, Pirrung M, Gonzalez A, Knight R (2013) EMPeror: a tool for visualizing high-throughput microbial community data. GigaScience 2:16

    Article  Google Scholar 

  • Wei Q, Wang H, Chen Z, Lv Z, **e Y, Lu F (2013) Profiling of dynamic changes in the microbial community during the soy sauce fermentation process. Appl Microbiol Biotechnol 97:9111–9119

    Article  CAS  Google Scholar 

  • 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 54:2379–2383

    Article  CAS  Google Scholar 

  • Yumoto I, Hirota K, Nodasaka Y, Tokiwa Y, Nakajima K (2008) Alkalibacterium indicireducens sp. nov., an obligate alkaliphile that reduces an indigo dye. Int J Syst Evol Microbiol 58:901–905

    Article  CAS  Google Scholar 

Download references

Acknowledgements

This study was supported by the Japan Society for the Promotion of Science with Grant-in-Aids for Scientific Research Nos. 23570128 and 16K07684 to I.Y. and 26630250 and 15H05331 to T.N.

Author information

Authors and Affiliations

  1. Bioproduction Research Institute, National Institute of Advanced Industrial Science and Technology (AIST), Tsukisamu-Higashi, Toyohira-ku, Sapporo, 062-8517, Japan

    Takahiro Okamoto, Kenichi Aino & Isao Yumoto

  2. School of Biological Science and Engineering, Tokai University, Minamisawa, Minami-ku, Sapporo, 005-8601, Japan

    Takahiro Okamoto & Hidetoshi Matsuyama

  3. Laboratory of Environmental Microbiology, Graduate School of Agriculture, Hokkaido University, Kita-ku, Sapporo, Hokkaido, 060-8589, Japan

    Kenichi Aino & Isao Yumoto

  4. Bioproduction Research Institute, National Institute of Advanced Industrial Science and Technology, Central 6, 1-1-1, Higashi, Tukuba, 305-8566, Ikaraki, Japan

    Takashi Narihiro & Isao Yumoto

Authors
  1. Takahiro Okamoto
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Kenichi Aino
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Takashi Narihiro
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Hidetoshi Matsuyama
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Isao Yumoto
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Isao Yumoto.

Ethics declarations

Conflict of interest

The authors have declared that they have no competing interests.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 57 KB)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Okamoto, T., Aino, K., Narihiro, T. et al. Analysis of microbiota involved in the aged natural fermentation of indigo. World J Microbiol Biotechnol 33, 70 (2017). https://doi.org/10.1007/s11274-017-2238-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s11274-017-2238-1

Keywords

Search

Navigation