Journal of Microbiology and Biotechnology

The Korean Society for Microbiology and Biotechnology (한국미생물·생명공학회)
권호 표지
DOI QR코드

DOI QR Code

Metagenome-Assembled Genomes of Komagataeibacter from Kombucha Exposed to Mars-Like Conditions Reveal the Secrets in Tolerating Extraterrestrial Stresses

  • Lee, Imchang (Department of Life Science, Multidisciplinary Genome Institute, Hallym University) ;
  • Podolich, Olga (Institute of Molecular Biology and Genetics of NASU) ;
  • Brenig, Bertram (Institute of Veterinary Medicine, Burckhardtweg, University of Gottingen) ;
  • Tiwari, Sandeep (Departamento de Genetica, Ecologia e Evolucao, Instituto de Ciencias Biologicas, Universidade Federal de Minas Gerais) ;
  • Azevedo, Vasco (Departamento de Genetica, Ecologia e Evolucao, Instituto de Ciencias Biologicas, Universidade Federal de Minas Gerais) ;
  • de Carvalho, Daniel Santana (Molecular and Computational Biology of Fungi Laboratory, Department of Microbiology, Institute of Biological Sciences, Federal University of Minas Gerais) ;
  • Uetanabaro, Ana Paula Trovatti (Molecular and Computational Biology of Fungi Laboratory, Department of Microbiology, Institute of Biological Sciences, Federal University of Minas Gerais) ;
  • Goes-Neto, Aristoteles (Molecular and Computational Biology of Fungi Laboratory, Department of Microbiology, Institute of Biological Sciences, Federal University of Minas Gerais) ;
  • Alzahrani, Khalid J. (Department of Clinical Laboratories Sciences, College of Applied Medical Sciences, Taif University) ;
  • Reva, Oleg (Centre for Bioinformatics and Computational Biology, Department of Biochemistry, Genetics and Microbiology, University of Pretoria) ;
  • Kozyrovska, Natalia (Institute of Molecular Biology and Genetics of NASU) ;
  • de Vera, Jean-Pierre (Microgravity User Support Center (MUSC), German Aerospace Center (DLR)) ;
  • Barh, Debmalya (Departamento de Genetica, Ecologia e Evolucao, Instituto de Ciencias Biologicas, Universidade Federal de Minas Gerais) ;
  • Kim, Bong-Soo (Department of Life Science, Multidisciplinary Genome Institute, Hallym University)
  • Received : 2022.04.07
  • Accepted : 2022.07.05
  • Published : 2022.08.28
Download PDF
⟨ Previous Next ⟩

Abstract

Kombucha mutualistic community (KMC) is composed by acetic acid bacteria and yeasts, producing fermented tea with health benefits. As part of the BIOlogy and Mars EXperiment (BIOMEX) project, the effect of Mars-like conditions on the KMC was analyzed. Here, we analyzed metagenome-assembled genomes (MAGs) of the Komagataeibacter, which is a predominant genus in KMC, to understand their roles in the KMC after exposure to Mars-like conditions (outside the International Space Station) based on functional genetic elements. We constructed three MAGs: K. hansenii, K. rhaeticus, and K. oboediens. Our results showed that (i) K. oboediens MAG functionally more complex than K. hansenii, (ii) K. hansenii is a keystone in KMCs with specific functional features to tolerate extreme stress, and (iii) genes related to the PPDK, betaine biosynthesis, polyamines biosynthesis, sulfate-sulfur assimilation pathway as well as type II toxin-antitoxin (TA) system, quorum sensing (QS) system, and cellulose production could play important roles in the resilience of KMC after exposure to Mars-like stress. Our findings show the potential mechanisms through which Komagataeibacter tolerates the extraterrestrial stress and will help to understand minimal microbial composition of KMC for space travelers.

Keywords

Acknowledgement

This research was supported by the Bio & Medical Technology Development Program of the National Research Foundation of Korea (NRF) funded by the Ministry of Science and ICT (2021M3A9I4023974), Basic Science Research Program through the NRF of Korea funded by the Ministry of Education (2021R1A6A1A03044501), and the Korea Health Technology R&D Project through the Korea Health Industry Development Institute (KHIDI) funded by the Ministry of Health & Welfare (HP20C0082). K.J.A. acknowledges the Taif University Researchers Supporting Program (project number: TURSP-2020/128), Taif University, Saudi Arabia.

References

  1. Dufresne C, Farnworth E. 2000. Tea, Kombucha, and health: a review. Food Res. Int. 33: 409-421. https://doi.org/10.1016/S0963-9969(00)00067-3
  2. Greenwalt C, Steinkraus K, Ledford R. 2000. Kombucha, the fermented tea: microbiology, composition, and claimed health effects. J. Food Prot. 63: 976-981. https://doi.org/10.4315/0362-028X-63.7.976
  3. Jayabalan R, Malbasa RV, Loncar ES, Vitas JS, Sathishkumar M. 2014. A review on kombucha tea - microbiology, composition, fermentation, beneficial effects, toxicity, and tea fungus. Compr. Rev. Food Sci. Food Saf. 13: 538-550. https://doi.org/10.1111/1541-4337.12073
  4. Arikan M, Mitchell AL, Finn RD, Gurel F. 2020. Microbial composition of Kombucha determined using amplicon sequencing and shotgun metagenomics. J. Food Sci. 85: 455-464. https://doi.org/10.1111/1750-3841.14992
  5. Villarreal-Soto SA, Bouajila J, Pace M, Leech J, Cotter PD, Souchard J-P, et al. 2020. Metabolome-microbiome signatures in the fermented beverage, Kombucha. Int. J. Food Microbiol. 333: 108778. https://doi.org/10.1016/j.ijfoodmicro.2020.108778
  6. Gomes RJ, Borges MdF, Rosa MdF, Castro-Gomez RJH, Spinosa WA. 2018. Acetic acid bacteria in the food industry: systematics, characteristics and applications. Food Technol. Biotechnol. 56: 139-151.
  7. Ramachandran S, Fontanille P, Pandey A, Larroche C. 2006. Gluconic acid: properties, applications and microbial production. Food Technol. Biotechnol. 44: 185-195.
  8. Banerjee S, Schlaeppi K, van der Heijden MG. 2018. Keystone taxa as drivers of microbiome structure and functioning. Nat. Rev. Microbiol. 16: 567-576. https://doi.org/10.1038/s41579-018-0024-1
  9. Goes-Neto A, Kukharenko O, Orlovska I, Podolich O, Imchen M, Kumavath R, et al. 2021. Shotgun metagenomic analysis of kombucha mutualistic community exposed to mars-like environment outside the international space station. Environ. Microbiol. 23: 3727-3742. https://doi.org/10.1111/1462-2920.15405
  10. Podolich O, Kukharenko O, Haidak A, Zaets I, Zaika L, Storozhuk O, et al. 2019. Multimicrobial kombucha culture tolerates marslike conditions simulated on low earth orbit. Astrobiology 19: 183-196. https://doi.org/10.1089/ast.2017.1746
  11. Beghini F, McIver LJ, Blanco-Miguez A, Dubois L, Asnicar F, Maharjan S, et al. 2021. Integrating taxonomic, functional, and strainlevel profiling of diverse microbial communities with bioBakery 3. Elife 10: e65088. https://doi.org/10.7554/eLife.65088
  12. Kruskal JB. 1964. Nonmetric multidimensional scaling: a numerical method. Psychometrika 29: 115-129. https://doi.org/10.1007/BF02289694
  13. Bray JR, Curtis JT. 1957. An ordination of the upland forest communities of southern Wisconsin. Ecol. Monogr. 27: 326-349.
  14. Dixon P. 2003. VEGAN, a package of R functions for community ecology. J. Veg. Sci. 14: 927-930. https://doi.org/10.1111/j.1654-1103.2003.tb02228.x
  15. Li D, Liu C-M, Luo R, Sadakane K, Lam T-W. 2015. MEGAHIT: an ultra-fast single-node solution for large and complex metagenomics assembly via succinct de Bruijn graph. Bioinformatics 31: 1674-1676. https://doi.org/10.1093/bioinformatics/btv033
  16. Langmead B, Salzberg SL. 2012. Fast gapped-read alignment with Bowtie 2. Nat. Methods 9: 357-359. https://doi.org/10.1038/nmeth.1923
  17. Menzel P, Ng KL, Krogh A. 2016. Fast and sensitive taxonomic classification for metagenomics with Kaiju. Nat. Commun. 7: 11257. https://doi.org/10.1038/ncomms11257
  18. Eren AM, Esen OC, Quince C, Vineis JH, Morrison HG, Sogin ML, et al. 2015. Anvi'o: an advanced analysis and visualization platform for 'omics data. PeerJ 3: e1319. https://doi.org/10.7717/peerj.1319
  19. Parks DH, Imelfort M, Skennerton CT, Hugenholtz P, Tyson GW. 2015. CheckM: assessing the quality of microbial genomes recovered from isolates, single cells, and metagenomes. Genome Res. 25: 1043-1055. https://doi.org/10.1101/gr.186072.114
  20. Camacho C, Coulouris G, Avagyan V, Ma N, Papadopoulos J, Bealer K, et al. 2009. BLAST+: architecture and applications. BMC Bioinformatics 10: 421. https://doi.org/10.1186/1471-2105-10-421
  21. Sayers EW, Agarwala R, Bolton EE, Brister JR, Canese K, Clark K, et al. 2019. Database resources of the national center for biotechnology information. Nucleic Acids Res. 47: D23-D28. https://doi.org/10.1093/nar/gky1069
  22. Lee I, Kim YO, Park S-C, Chun J. 2016. OrthoANI: an improved algorithm and software for calculating average nucleotide identity. Int. J. Syst. Evol. Microbiol. 66: 1100-1103. https://doi.org/10.1099/ijsem.0.000760
  23. Shakya M, Ahmed SA, Davenport KW, Flynn MC, Lo C-C, Chain PS. 2020. Standardized phylogenetic and molecular evolutionary analysis applied to species across the microbial tree of life. Sci. Rep. 10: 1723. https://doi.org/10.1038/s41598-020-58356-1
  24. Kanehisa M, Sato Y, Morishima K. 2016. BlastKOALA and GhostKOALA: KEGG tools for functional characterization of genome and metagenome sequences. J. Mol. Biol. 428: 726-731. https://doi.org/10.1016/j.jmb.2015.11.006
  25. Seemann T. 2014. Prokka: rapid prokaryotic genome annotation. Bioinformatics 30: 2068-2069. https://doi.org/10.1093/bioinformatics/btu153
  26. Papudeshi B, Haggerty JM, Doane M, Morris MM, Walsh K, Beattie DT, et al. 2017. Optimizing and evaluating the reconstruction of Metagenome-assembled microbial genomes. BMC Genomics 18: 915. https://doi.org/10.1186/s12864-017-4294-1
  27. Lee I, Barh D, Podolich O, Brenig B, Tiwari S, Azevedo V, et al. 2021. Metagenome-assembled genome sequences obtained from a reactivated Kombucha microbial community exposed to a Mars-like environment outside the International Space Station. Microbiol. Resour. Announc. 10: e00549-00521.
  28. Ng W-L, Bassler BL. 2009. Bacterial quorum-sensing network architectures. Annu. Rev. Genet. 43: 197-222. https://doi.org/10.1146/annurev-genet-102108-134304
  29. Rutherford ST, Bassler BL. 2012. Bacterial quorum sensing: its role in virulence and possibilities for its control. Cold Spring Harb. Perspect. Med. 2: a012427.
  30. Solano C, Echeverz M, Lasa I. 2014. Biofilm dispersion and quorum sensing. Curr. Opin. Microbiol. 18: 96-104. https://doi.org/10.1016/j.mib.2014.02.008
  31. Erental A, Sharon I, Engelberg-Kulka H. 2012. Two programmed cell death systems in Escherichia coli: an apoptotic-like death is inhibited by the mazEF-mediated death pathway. PLoS Biol. 10: e1001281. https://doi.org/10.1371/journal.pbio.1001281
  32. Yamaguchi Y, Park J-H, Inouye M. 2011. Toxin-antitoxin systems in bacteria and archaea. Annu. Rev. Genet. 45: 61-79. https://doi.org/10.1146/annurev-genet-110410-132412
  33. Zhang S, Bryant DA. 2011. The tricarboxylic acid cycle in cyanobacteria. Science 334: 1551-1553. https://doi.org/10.1126/science.1210858
  34. Cushman JC, Bohnert HJ. 1999. Crassulacean acid metabolism: molecular genetics. Annu. Rev. Plant Biol. 50: 305-332. https://doi.org/10.1146/annurev.arplant.50.1.305
  35. Osmond C. 1978. Crassulacean acid metabolism: a curiosity in context. Annu. Rev. Plant Physiol. 29: 379-414. https://doi.org/10.1146/annurev.pp.29.060178.002115
  36. Kerovuo J, Reinikainen T, Nyysso?la? A, Kaukinen P, von Weymarn N. 2000. Extreme halophiles synthesize betaine from glycine by methylation. J. Biol. Chem. 275: 22196-22201. https://doi.org/10.1074/jbc.M910111199
  37. Monobe M, Uzawa A, Hino M, Ando K, Kojima S. 2005. Glycine betaine, a beer component, protects radiation-induced injury. J. Radiat. Res. 46: 117-121. https://doi.org/10.1269/jrr.46.117
  38. Smith LT, Pocard J-A, Bernard T, Le Rudulier D. 1988. Osmotic control of glycine betaine biosynthesis and degradation in Rhizobium meliloti. J. Bacteriol. 170: 3142-3149. https://doi.org/10.1128/jb.170.7.3142-3149.1988
  39. Shah P, Swiatlo E. 2008. A multifaceted role for polyamines in bacterial pathogens. Mol. Microbiol. 68: 4-16. https://doi.org/10.1111/j.1365-2958.2008.06126.x
  40. Schneider J, Wendisch VF. 2011. Biotechnological production of polyamines by bacteria: recent achievements and future perspectives. Appl. Microbiol. Biotechnol. 91: 17-30. https://doi.org/10.1007/s00253-011-3252-0
  41. Kawano Y, Suzuki K, Ohtsu I. 2018. Current understanding of sulfur assimilation metabolism to biosynthesize L-cysteine and recent progress of its fermentative overproduction in microorganisms. Appl. Microbiol. Biotechnol. 102: 8203-8211. https://doi.org/10.1007/s00253-018-9246-4
  42. Mendoza-Cozatl D, Loza-Tavera H, Hernandez-Navarro A, Moreno-Sanchez R. 2005. Sulfur assimilation and glutathione metabolism under cadmium stress in yeast, protists and plants. FEMS Microbiol. Rev. 29: 653-671. https://doi.org/10.1016/j.femsre.2004.09.004