Journal of Microbiology and Biotechnology

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

DOI QR Code

Changes in Cell Membrane Fatty Acid Composition of Streptococcus thermophilus in Response to Gradually Increasing Heat Temperature

  • Min, Bonggyu (Department of Agricultural Biotechnology and Research Institute of Agriculture and Life Sciences, Seoul National University) ;
  • Kim, Kkotnim (Department of Agricultural Biotechnology and Research Institute of Agriculture and Life Sciences, Seoul National University) ;
  • Li, Vladimir (Interdisciplinary Program in Bioinformatics, Seoul National University) ;
  • Cho, Seoae (C&K genomics Inc.) ;
  • Kim, Heebal (Department of Agricultural Biotechnology and Research Institute of Agriculture and Life Sciences, Seoul National University)
  • Received : 2020.01.02
  • Accepted : 2020.02.28
  • Published : 2020.05.28
Download PDF
⟨ Previous Next ⟩

Abstract

In this study, a method of heat adaptation was implemented in an attempt to increase the upper thermal threshold of two Streptococcus thermophilus found in South Korea and identified the alterations in membrane fatty acid composition to adaptive response to heat. In order to develop heat tolerant lactic acid bacteria, heat treatment was continuously applied to bacteria by increasing temperature from 60℃ until the point that no surviving cell was detected. Our results indicated significant increase in heat tolerance of heat-adapted strains compared to the wild type (WT) strains. In particular, the survival ratio of basically low heat-tolerant strain increased even more. In addition, the strains with improved heat tolerance acquired cross protection, which improved their survival ratio in acid, bile salts and osmotic conditions. A relation between heat tolerance and membrane fatty acid composition was identified. As a result of heat adaptation, the ratio of unsaturated to saturated fatty acids (UFA/SFA) and C18:1 relative concentration were decreased. C6:0 in only heat-adapted strains and C22:0 in only the naturally high heat tolerant strain were detected. These results support the hypothesis, that the consequent increase of SFA ratio is a cellular response to environmental stresses such as high temperatures, and it is able to protect the cells from acid, bile salts and osmotic conditions via cross protection. This study demonstrated that the increase in heat tolerance can be utilized as a mean to improve bacterial tolerance against various environmental stresses.

Keywords

References

  1. FAO/WHO. 2001. Health and nutritional properties of probiotics in food including powder milk with live lactic acid bacteria. Report of a Joint FAO/WHO Expert Consultation on Evaluation of Health and Nutritional Properties of Probiotics in Food Including Powder Milk with Live Lactic Acid Bacteria. Cordoba, Argentina: Food and Agricultural Organization of the United Nations, World Health Organization.
  2. Lorenzo JM, Munekata P, Dominguez R, Pateiro M, Saraiva JA, Franco D. 2017. Main groups of microorganisms of relevance for food safety and stability: general aspects and overall description. Innov. Technol. Food Preserv. 2018: 53-107.
  3. Cui Y, Xu T, Qu X, Hu T, Jiang X, Zhao C. 2016. New insights into various production characteristics of streptococcus thermophilus strains. Int. J. Mol. Sci. 17(10): 1701. https://doi.org/10.3390/ijms17101701
  4. Chen J, Shen J, Ingvar Hellgren L, Jensen PR, Solem C. 2015. Adaptation of Lactococcus lactis to high growth temperature leads to a dramatic increase in acidification rate. Sci. Rep. 5: 14199. https://doi.org/10.1038/srep14199
  5. Angela L, Giuseppe S. 2019. Stress Responses of LAB. In Paramithiotis S, Patra JK, pp. 164-174 (Eds.), Food Mol. Microbiol. Boca Raton, U.S: CRC Press.
  6. Torres-Maravilla E, Lenoir M, Mayorga-Reyes L, Allain T, Sokol H, Langella P, et al. 2016. Identification of novel anti-inflammatory probiotic strains isolated from pulque. Appl. Microbiol. Biotechnol.100: 385-396 https://doi.org/10.1007/s00253-015-7049-4
  7. Kishimoto T, Iijima L, Tatsumi M, Ono N, Oyake A, Hashimoto T, et al. 2010. Transition from positive to neutral in mutation fixation along with continuing rising fitness in thermal adaptive evolution. PLoS Genet. 6(10): e1001164. https://doi.org/10.1371/journal.pgen.1001164
  8. Van de Guchte M, Serror P, Chervaux C, Smokvina T, Ehrlich SD, Maguin E. 2002. Stress responses in lactic acid bacteria. Antonie Van Leeuwenhoek 82: 187-216. https://doi.org/10.1023/A:1020631532202
  9. Guerzoni ME, Lanciotti R, Cocconcelli PS. 2001. Alteration in cellular fatty acid composition as a response to salt, acid, oxidative and thermal stresses in Lactobacillus helveticus. Microbiology 147: 2255-2264. https://doi.org/10.1099/00221287-147-8-2255
  10. Ruiz L, Sanchez B, Ruas-Madiedo P, De Los Reyes-Gavilan CG, Margolles A. 2007. Cell envelope changes in Bifidobacterium animalis ssp. lactis as a response to bile. FEMS Microbiol. Lett. 274: 316-22. https://doi.org/10.1111/j.1574-6968.2007.00854.x
  11. Alvarez-Ordonez A, Fernandez A, Lopez M, Arenas R, Bernardo A. 2008. Modifications in membrane fatty acid composition of Salmonella typhimurium in response to growth conditions and their effect on heat resistance. Int. J. Food Microbiol. 123: 212-219. https://doi.org/10.1016/j.ijfoodmicro.2008.01.015
  12. Zhang YM, Rock CO. 2008. Membrane lipid homeostasis in bacteria. Nat. Rev. Microbiol 6: 222-233. https://doi.org/10.1038/nrmicro1839
  13. Beal C, Fonseca F, Corrieu G. 2010. Resistance to freezing and frozen storage of Streptococcus thermophilus is related to membrane fatty acid composition. J. Dairy Sci. 84: 2347-2356. https://doi.org/10.3168/jds.S0022-0302(01)74683-8
  14. Auffray Y, Lecesne E, Hartke A, Boutibonnes P. 1995. Basic features of the Streptococcus thermophilus heat shock response. Curr. Microbiol. 30: 87-91. https://doi.org/10.1007/BF00294188
  15. Wei Y, Gao J, Liu D, Li Y, Liu W. 2019. Adaptational changes in physiological and transcriptional responses of Bifidobacterium longum involved in acid stress resistance after successive batch cultures. Microb. Cell Fact. 18(1): 156. https://doi.org/10.1186/s12934-019-1206-x
  16. Guo L, Li T, Tang Y, Yang L, Huo G. 2016. Probiotic properties of enterococcus strains isolated from traditional naturally fermented cream in China. Microb. Biotechnol. 9: 737-745. https://doi.org/10.1111/1751-7915.12306
  17. Kim WS, Perl L, Park JH, Tandianus JE, Dunn NW. 2001. Assessment of stress response of the probiotic Lactobacillus acidophilus. Curr. Microbiol. 43: 346-350. https://doi.org/10.1007/s002840010314
  18. Devereux R, Willis SG. 2011. Amplification of ribosomal RNA sequences. In Mol. Microb. Ecol. Man. pp. 277-287.
  19. Kim O-S, Cho Y-J, Lee K, Yoon S-H, Kim M, Na H, et al. 2012. Introducing EzTaxon-e: a prokaryotic 16S rRNA gene sequence database with phylotypes that represent uncultured species. Int. J. Syst. Evol. Microbiol. 62: 716-721. https://doi.org/10.1099/ijs.0.038075-0
  20. Kumar S, Stecher G, Li M, Knyaz C, Tamura K. 2018. MEGA X: Molecular evolutionary genetics analysis across computing platforms. Mol. Biol. Evol. 35: 1547-1549. https://doi.org/10.1093/molbev/msy096
  21. Barrick JE, Yu DS, Yoon SH, Jeong H, Oh K, Schneider, et al. 2009. Genome evolution and adaptation in a long-term experiment with Escherichia coli. Nature 461: 1243-1247. https://doi.org/10.1038/nature08480
  22. Shibai A, Takahashi Y, Ishizawa Y, Motooka D, Nakamura S, Ying BW, et al. 2017. Mutation accumulation under UV radiation in Escherichia coli. Sci. Rep. 7(1): 14531. https://doi.org/10.1038/s41598-017-15008-1
  23. Shin YJ, Kang CH, Kim W, So JS. 2018. Heat Adaptation improved cell viability of probiotic Enterococcus faecium HL7 upon various environmental stresses. Probiotics Antimicrob. Proteins 11: 618-626. https://doi.org/10.1007/s12602-018-9400-4
  24. Mazzola PG, Penna TCV, da S Martins AM. 2003. Determination of decimal reduction time (D value) of chemical agents used in hospitals for disinfection purposes. BMC Infect. Dis. 3: 24. https://doi.org/10.1186/1471-2334-3-24
  25. Alvarez-Ordonez A, Fernandez A, Lopez M, Bernardo A. 2009. Relationship between membrane fatty acid composition and heat resistance of acid and cold stressed Salmonella senftenberg CECT 4384. Food Microbiol.
  26. Lee KW, Shim JM, Park SK, Heo HJ, Kim HJ, Ham KS, et al. 2016. Isolation of lactic acid bacteria with probiotic potentials from kimchi, traditional Korean fermented vegetable. LWT - Food Sci. Technol. 26: 347-353.
  27. GarcEs R, Mancha M. 1993. One-step lipid extraction and fatty acid methyl esters preparation from fresh plant tissues. Anal. Biochem. 211: 139-143. https://doi.org/10.1006/abio.1993.1244
  28. R Development Core Team R. 2011. R: A Language and Environment for Statistical Computing. R Found. Stat. Comput.
  29. Ghattargi VC, Nimonkar YS, Burse SA, Davray D, Kumbhare SV, Shetty SA, et al. 2018. Genomic and physiological analyses of an indigenous strain, Enterococcus faecium 17OM39. Funct. Integr. Genomics.
  30. Caspeta L, Chen Y, Nielsen J. 2016. Thermotolerant yeasts selected by adaptive evolution express heat stress response at $30^{\circ}C$. Sci. Rep. 6: 27003. https://doi.org/10.1038/srep27003
  31. Wang C, Cui Y, Qu X. 2018. Mechanisms and improvement of acid resistance in lactic acid bacteria. Arch. Microbiol. 200: 195-201. https://doi.org/10.1007/s00203-017-1446-2
  32. Alvarez-Ordonez A, Begley M, Prieto M, Messens W, Lopez M, Bernardo A, et al. 2011. Salmonella spp. survival strategies within the host gastrointestinal tract. Microbiology 157: 3268-3281. https://doi.org/10.1099/mic.0.050351-0
  33. Maragkoudakis PA, Zoumpopoulou G, Miaris C, Kalantzopoulos G, Pot B, Tsakalidou E. 2006. Probiotic potential of Lactobacillus strains isolated from dairy products. Int. Dairy J. 16: 188-199.
  34. Abee T, Wouters JA. 1999. Microbial stress response in minimal processing. Int. J. Food Microbiol. 50: 65-91. https://doi.org/10.1016/S0168-1605(99)00078-1
  35. Casadei MA, Manas P, Niven G, Needs E, Mackey BM. 2002. Role of membrane fluidity in pressure resistance of Escherichia coli NCTC 8164. Appl. Environ. Microbiol. 68: 5965-5972. https://doi.org/10.1128/AEM.68.12.5965-5972.2002
  36. Rudolph B, Gebendorfer KM, Buchner J, Winter J. 2010. Evolution of Escherichia coli for growth at high temperatures. J. Biol. Chem. 285: 19029-19034. https://doi.org/10.1074/jbc.M110.103374
  37. Oide S, Gunji W, Moteki Y, Yamamoto S, Suda M, Jojima T, et al. 2015. Thermal and solvent stress cross-tolerance conferred to Corynebacterium glutamicum by adaptive laboratory evolution. Appl. Environ. Microbiol. 81: 2284-2298. https://doi.org/10.1128/AEM.03973-14
  38. Henriksson A, Khaled AKD, Conway PL. 1999. Lactobacillus colonization of the gastrointestinal tract of mice after removal of the non-secreting stomach region. Microb. Ecol. Health Dis. 11: 96-99. https://doi.org/10.1080/089106099435835
  39. Suutari M, Laakso S. 1994. Microbial fatty acids and thermal adaptation. Crit. Rev. Microbiol. 20: 285-328. https://doi.org/10.3109/10408419409113560
  40. Bajerski F, Wagner D, Mangelsdorf K. 2017. Cell membrane fatty acid composition of Chryseobacterium frigidisoli PB4T, isolated from antarctic glacier forefield soils, in response to changing temperature and pH conditions. Front. Microbiol. 8: 677.
  41. Wang Y, Corrieu G, Beal C. 2005. Fermentation pH and temperature influence the cryotolerance of Lactobacillus acidophilus RD758. J. Dairy Sci. 88: 21-29. https://doi.org/10.3168/jds.S0022-0302(05)72658-8
  42. Fulco AJ. 1983. Fatty acid metabolism in bacteria. Prog. Lipid Res. 22: 133-160. https://doi.org/10.1016/0163-7827(83)90005-X
  43. Annous BA, Kozempel MF, Kurantz M J. 1999. Changes in membrane fatty acid composition of Pediococcus sp. strain NRRL B-2354 in response to growth conditions and its effect on thermal resistance. Appl. Environ. Microbiol. 65: 2857-2862. https://doi.org/10.1128/aem.65.7.2857-2862.1999
  44. Russell NJ, Evans RI, ter Steeg PF, Hellemons J, Verheul A, Abee T. 1995. Membranes as a target for stress adaptation. Int. J. Food Microbiol. 28: 255-261. https://doi.org/10.1016/0168-1605(95)00061-5

Cited by

  1. Cross protection of lactic acid bacteria during environmental stresses: Stress responses and underlying mechanisms vol.144, 2020, https://doi.org/10.1016/j.lwt.2021.111203