Skip to main content
SpringerLink
Log in

Genome Sequencing Unveils Nomadic Traits of Lactiplantibacillus plantarum in Japanese Post-Fermented Tea

  • Published:
Current Microbiology Aims and scope Submit manuscript

Abstract

Post-fermented tea production involving microbial fermentation is limited to a few regions, such as Southeast Asia and Japan, with Japan's Shikoku island being particularly prominent. Lactiplantibacillus plantarum was the dominant species found in tea leaves after anaerobic fermentation of Awa-bancha in Miyoshi City, Tokushima, and Ishizuchi-kurocha in Ehime. Although the draft genome of L. plantarum from Japanese post-fermented tea has been previously reported, its genetic diversity requires further exploration. In this study, whole-genome sequencing was conducted on four L. plantarum strains isolated from Japanese post-fermented tea using nanopore sequencing. These isolates were then compared with other sources to examine their genetic diversity revealing that L. plantarum isolated from Japanese post-fermented tea contained several highly variable gene regions associated with sugar metabolism and transportation. However, no source-specific genes or clusters were identified within accessory or core gene regions. This study indicates that L. plantarum possesses high genetic diversity and that the unique environment of Japanese post-fermented tea does not appear to exert selective pressure on L. plantarum growth.

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

Access this article

Log in via an institution

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

Data Availability

The SRA and BioProject accession numbers for the raw reads of IYO2065, AWA2013, and AWA2045 are as follows: DRR463489-DRR463492, and PRJDB1576. The BioProject and SRA accession numbers for IYO1511 are available via DRR463489 and PRJDB9324.

References

  1. Horie M, Nara K, Sugino S et al (2017) Comparison of antioxidant activities among four kinds of Japanese traditional fermented tea. Food Sci Nutr 5:639–645. https://doi.org/10.1002/fsn3.442

    Article  CAS  PubMed  Google Scholar 

  2. Horie M, Sato H, Tada A et al (2019) Regional characteristics of Lactobacillus plantarum group strains isolated from two kinds of Japanese post-fermented teas, Ishizuchi-kurocha and Awa-bancha. Biosci Microbiota Food Health 38:11–22. https://doi.org/10.12938/bmfh.18-005

    Article  CAS  PubMed  Google Scholar 

  3. Nishioka H, Ohno T, Iwahashi H, Horie M (2021) Diversity of lactic acid bacteria involved in the fermentation of Awa-Bancha. Microbes Environ 36:ME21029. https://doi.org/10.1264/jsme2.ME21029

    Article  PubMed  PubMed Central  Google Scholar 

  4. Mizuno T, Iwahashi H, Horie M (2020) Identification of microbial flora associated with fermentation of Ishizuchi-Kurocha. J Jpn Soc Taste Technol 19:46–52

    Google Scholar 

  5. Yamamoto M, Horie M, Fukushima M, Toyotome T (2019) Culture-based analysis of fungi in leaves after the primary and secondary fermentation processes during Ishizuchi-kurocha production and lactate assimilation of P. kudriavzevii. Int J Food Microbiol 306:108263. https://doi.org/10.1016/j.ijfoodmicro.2019.108263

    Article  CAS  PubMed  Google Scholar 

  6. Liu Y-W, Liong M-T, Tsai Y-C (2018) New perspectives of Lactobacillus plantarum as a probiotic: the gut-heart-brain axis. J Microbiol 56:601–613. https://doi.org/10.1007/s12275-018-8079-2

    Article  PubMed  Google Scholar 

  7. Yang X, Zhou J, Fan L et al (2018) Antioxidant properties of a vegetable–fruit beverage fermented with two Lactobacillus plantarum strains. Food Sci Biotechnol 27:1719–1726. https://doi.org/10.1007/s10068-018-0411-4

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Devi SM, Aishwarya S, Halami PM (2016) Discrimination and divergence among Lactobacillus plantarum-group (LPG) isolates with reference to their probiotic functionalities from vegetable origin. Syst Appl Microbiol 39:562–570. https://doi.org/10.1016/j.syapm.2016.09.005

    Article  CAS  PubMed  Google Scholar 

  9. Todorov SD, Franco BDGDM (2010) Lactobacillus Plantarum: characterization of the species and application in food production. Food Rev Int 26:205–229. https://doi.org/10.1080/87559129.2010.484113

    Article  CAS  Google Scholar 

  10. Martino ME, Bayjanov JR, Caffrey BE et al (2016) Nomadic lifestyle of Lactobacillus plantarum revealed by comparative genomics of 54 strains isolated from different habitats. Environ Microbiol 18:4974–4989. https://doi.org/10.1111/1462-2920.13455

    Article  CAS  PubMed  Google Scholar 

  11. Bringel F, CURK M-C, HUBERT J-C, (1996) Characterization of lactobacilli by southern-type hybridization with a Lactobacillus plantarum pyrDFE probe. Int J Syst Evol Microbiol 46:588–594. https://doi.org/10.1099/00207713-46-2-588

    Article  CAS  Google Scholar 

  12. Sun Z, Harris HMB, McCann A et al (2015) Expanding the biotechnology potential of lactobacilli through comparative genomics of 213 strains and associated genera. Nat Commun 6:8322. https://doi.org/10.1038/ncomms9322

    Article  CAS  PubMed  Google Scholar 

  13. Choi S, Jin G-D, Park J, Kim IY, Kim EB (2018) Pan-genomics of lactobacillus plantarum revealed group-specific genomic profiles without habitat association. J. Microbiol. Biotechnol 28:1352–1359. https://doi.org/10.4014/jmb.1803.03029

    Article  CAS  PubMed  Google Scholar 

  14. Mao B, Yin R, Li X et al (2021) Comparative genomic analysis of Lactiplantibacillus plantarum isolated from different niches. Genes 12:241. https://doi.org/10.3390/genes12020241

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Phillippy AM, Schatz MC, Pop M (2008) Genome assembly forensics: finding the elusive mis-assembly. Genome Biol 9:R55. https://doi.org/10.1186/gb-2008-9-3-r55

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Khrenova MG, Panova TV, Rodin VA et al (2022) Nanopore sequencing for de novo bacterial genome assembly and search for single-nucleotide polymorphism. Int J Mol Sci 23:8569. https://doi.org/10.3390/ijms23158569

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Niwa R, Syaputri Y, Horie M, Iwahashi H (2020) Draft genome sequence of Lactobacillus plantarum IYO1511 isolated from Ishizuchi-Kurocha. Microbiol Resour Announc. https://doi.org/10.1128/mra.00143-20

    Article  PubMed  PubMed Central  Google Scholar 

  18. Manni M, Berkeley MR, Seppey M (2021) BUSCO update: novel and streamlined workflows along with broader and deeper phylogenetic coverage for scoring of eukaryotic, prokaryotic, and viral genomes. Mol Biol Evol 38:4647–4654

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Improvements to PATRIC, the all-bacterial Bioinformatics Database and Analysis Resource Center | Nucleic Acids Research | Oxford Academic. https://academic.oup.com/nar/article/45/D1/D535/2605866?login=true. Accessed 9 Feb 2023

  20. Eren AM, Kiefl E, Shaiber A et al (2021) Community-led, integrated, reproducible multi-omics with anvi’o. Nat Microbiol 6:3–6. https://doi.org/10.1038/s41564-020-00834-3

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Kim J, Na S-I, Kim D, Chun J (2021) UBCG2: Up-to-date bacterial core genes and pipeline for phylogenomic analysis. J Microbiol 59:609–615. https://doi.org/10.1007/s12275-021-1231-4

    Article  CAS  PubMed  Google Scholar 

  22. Surve S, Shinde DB, Kulkarni R (2022) Isolation, characterization and comparative genomics of potentially probiotic Lactiplantibacillus plantarum strains from Indian foods. Sci Rep 12:1940. https://doi.org/10.1038/s41598-022-05850-3

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Zhang B, Zuo F, Yu R et al (2015) Comparative genome-based identification of a cell wall-anchored protein from Lactobacillus plantarum increases adhesion of Lactococcus lactis to human epithelial cells. Sci Rep 5:14109. https://doi.org/10.1038/srep14109

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Chokesajjawatee N, Santiyanont P, Chantarasakha K et al (2020) Safety assessment of a Nham Starter culture Lactobacillus plantarum BCC9546 via whole-genome analysis. Sci Rep 10:10241. https://doi.org/10.1038/s41598-020-66857-2

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Garcia-Gonzalez N, Bottacini F, van Sinderen D et al (2022) Comparative genomics of Lactiplantibacillus plantarum: insights into probiotic markers in strains isolated from the human gastrointestinal tract and fermented Foods. Front Microbiol. https://doi.org/10.3389/fmicb.2022.854266

    Article  PubMed  PubMed Central  Google Scholar 

  26. Fuhren J, Nijland R, Wels M et al (2021) Complete closed genome sequence of the inulin-utilizing Lactiplantibacillus plantarum strain Lp900, obtained using a hybrid nanopore and illumina assembly. Microbiol Resour Announc 10:e00185-e221. https://doi.org/10.1128/MRA.00185-21

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. McLeod A, Fagerlund A, Rud I, Axelsson L (2019) Large plasmid complement resolved: complete genome sequencing of Lactobacillus plantarum MF1298, a candidate probiotic strain associated with unfavorable effect. Microorganisms 7:262. https://doi.org/10.3390/microorganisms7080262

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Carpi FM, Coman MM, Silvi S et al (2022) Comprehensive pan-genome analysis of Lactiplantibacillus plantarum complete genomes. J Appl Microbiol 132:592–604. https://doi.org/10.1111/jam.15199

    Article  CAS  PubMed  Google Scholar 

  29. Mendes-Soares H, Suzuki H, Hickey RJ, Forney LJ (2014) Comparative functional genomics of lactobacillus spp. reveals possible mechanisms for specialization of vaginal lactobacilli to their environment. J Bacteriol 196:1458–1470. https://doi.org/10.1128/JB.01439-13

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Cai H, Thompson R, Budinich MF et al (2009) Genome sequence and comparative genome analysis of Lactobacillus casei: insights into their niche-associated evolution. Genome Biol Evol 1:239–257. https://doi.org/10.1093/gbe/evp019

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Douillard FP, Ribbera A, Kant R et al (2013) Comparative genomic and functional analysis of 100 Lactobacillus rhamnosus strains and their comparison with strain GG. PLoS Genet 9:e1003683. https://doi.org/10.1371/journal.pgen.1003683

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Torriani S, Felis GE, Dellaglio F (2001) Differentiation of Lactobacillus plantarum, L. pentosus, and L. paraplantarum by recA gene sequence analysis and multiplex PCR assay with recA Gene-derived primers. Appl Environ Microbiol 67:3450–3454. https://doi.org/10.1128/AEM.67.8.3450-3454.2001

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Draft Genome Sequence of Lactiplantibacillus pentosus AWA1501, Isolated from Awa-bancha | Microbiology Resource Announcements. /https://doi.org/10.1128/MRA.00518-21. Accessed 20 Apr 2023

Download references

Acknowledgements

Computations were partially performed on the NIG supercomputer at ROIS National Institute of Genetics. We thank Kazuma Suematsu (Graduate School of Natural Science and Technology, Gifu University) for his support in DNA extraction. We would like to thank Editage (www.editage.com) for English language editing.

Author information

Authors and Affiliations

  1. Department of Life Science and Chemistry, Graduate School of Natural Science and Technology, Gifu University, Gifu, 501-1193, Japan

    Kyoka Sato, Yuichiro Ikagawa & Hitoshi Iwahashi

  2. Graduate School of Medicine, Kyoto University, Kyoto, 606-8501, Japan

    Ryo Niwa

  3. Food and Biotechnology Division, Tokushima Prefectural Industrial Technology Center, Tokushima, 770-8021, Japan

    Hiroki Nishioka

  4. Health and Medical Research Institute (HMRI), National Institute of Advanced Industrial Science and Technology (AIST), Kagawa, 761-0395, Japan

    Masanori Horie

Authors
  1. Kyoka Sato
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Yuichiro Ikagawa
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Ryo Niwa
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Hiroki Nishioka
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Masanori Horie
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Hitoshi Iwahashi
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

KS and HI conceived the study. KS and RN developed the research idea, designed the experimental methodology, and drafted the original manuscript. HN and MH isolated the Japanese post-fermented tea strains. KS and YI performed sequencing. HI critically reviewed the manuscript and provided feedback. All authors contributed to the final version of the manuscript and approved its submission for publication.

Corresponding authors

Correspondence to Kyoka Sato or Hitoshi Iwahashi.

Ethics declarations

Conflict of interest

All authors declare that they have no conflicts of interest.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Below is the link to the electronic supplementary material.

284_2023_3566_MOESM1_ESM.xls

Supplementary file1 (XLS 637 KB)—Table 1 Overview of strains isolated from post-fermented teas. Table 2 Strains used in the analysis and their isolation sources. Table 3 Overview of strains isolated from different isolation sources. Table 4 Gene sequence identity compared with WCFS1 strain exported by BV-BRC.

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Sato, K., Ikagawa, Y., Niwa, R. et al. Genome Sequencing Unveils Nomadic Traits of Lactiplantibacillus plantarum in Japanese Post-Fermented Tea. Curr Microbiol 81, 52 (2024). https://doi.org/10.1007/s00284-023-03566-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s00284-023-03566-9

Search

Navigation