Impact of high hydrostatic pressure on the single nucleotide polymorphism of stress-related dnaK, hrcA, and ctsR in the Lactobacillus strains

Main Article Content

Joanna Bucka-Kolendo https://orcid.org/0000-0002-8082-1153
Barbara Sokołowska https://orcid.org/0000-0002-6217-2401

Keywords

high hydrostatic pressure, lactic acid bacteria, nonsynonymous mutation, single nucleotide polymorphism, stress response, synonymous mutation

Abstract

Lactic acid bacteria (LAB) are widespread in environments and can either have a positive impact because their ability to survive in harsh conditions and influence the product (probiotic properties, change of structure-EPS [exopolysaccharides], etc.), or a negative impact, (so not needed) because of their spoilage ability (beer, juices). High hydrostatic pressure (HHP), one of the non-thermal preservation methods used in the food industry, can force the LAB to activate the adaptative mechanisms. Under pressurization, the changes in the bacteria cells can occur at the transcriptional or translational level. This study evaluated the HHP on the single nucleotide polymorphism (SNP) changes in three genes, dnaK, ctsR, and hrcA, related to the stress-response mechanism in LAB. The correlation between the DNA polymorphism and the gene expression under HHP stress was assessed. The applied pressure of 300 MPa resulted in a low ratio of nonsynonymous substitutions to the synonymous substitutions (0 to 1.12), and a lower number of mutations was observed for pressurized strains (from 6 in hrcA to 11 in dnaK) than in controlled (from 3 in ctsR to 92 in hrcA). In all pressurized strains, the expression of genes was observed, whereas, in control strains, the gene expression was detected in three out of five strains. Although there was a noticeable change in stress-related gene expression after HHP, there was no correlation with SNPs. At the same time, with a high frequency of synonymous changes in nucleotide and high diversity for hrcA and dnaK, a very low diversity was found in ctsR sequences. The LAB strains stress response mechanisms are much more complex. The study requires information on the general mechanism and changes in the membranes’ composition, proteome changes, and gene expression patterns. The mutations in genes related to stress can have important implications for the strains’ fitness effect and adaptive ability of LAB strains, especially considering their food industry implication where the HHP techniques are used.

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References

Bailey, S.F., Angela, L., Morales, A. and Kassen, R., 2021. Effects of synonymous mutations beyond codon bias: the evidence for adaptive synonymous substitutions from microbial evolution experiments. Genome Biology and Evolution 13(9): evab141. 10.1093/gbe/evab141

Bailey, S.F., Hinz, A. and Kassen, R., 2014. Adaptive synonymous mutations in an experimentally evolved Pseudomonas fluorescens population. Nature Communications 10(5): 4076. 10.1038/ncomms5076

Bangar, S.P., Sharma, N., Bhardwaj, A. and Phimolsiripol, Y., 2022. Lactic acid bacteria: a bio-green preservative against mycotoxins for food safety and shelf-life extension. Quality Assurance and Safety of Crops & Foods 14(2): 13–31. 10.15586/qas.v14i2.1014

Bron, P.A., Molenaar, D., de Vos, W.M. and Kleerebezem, M., 2006. DNA micro-array-based identification of bile-responsive genes in Lactobacillus plantarum. Journal of Applied Microbiology 100: 728–738. 10.4161/bbug.2.2.13910

Bucka-Kolendo, J., Juszczuk-Kubiak, E. and Sokołowska, B., 2021. Effect of high hydrostatic pressure on stress-related dnaK, hrcA, and ctsR expression patterns in selected Lactobacilli Strains. Genes 12: 1720. 10.3390/genes12111720

Bucka-Kolendo, J. and Sokołowska, B., 2017. Lactic acid bacteria stress response to preservation processes in the beverage and juice industry. Acta Biochimica Polonica 64: 459–464. 10.18388/abp.2017_1496

Bucka-Kolendo, J., Sokołowska, B. and Winiarczyk, S., 2020. Influence of high hydrostatic pressure on the identification of Lactobacillus by MALDI-TOF MS-preliminary study. Microorganisms 8: 813. 10.3390/microorganisms8060813

Chen, Y.-S., Wu, H.-C., Yu, C.-R., Chen, Z.-Y., Lu, Y.-C. and Yanagida, F., 2016. Isolation and characterization of lactic acid bacteria from Xi-Gua-Mian (fermented watermelon), a traditional fermented food in Taiwan. Italian Journal of Food Science 28(1): 9–14. 10.14674/1120-1770/ijfs.v451

De Angelis, M., Di Cagno, R., Huet, C., Crecchio, C., Fox, P.F. and Gobbetti, M., 2004. Heat shock response in Lactobacillus plan-tarum. Applied and Environmental Microbiology 70: 1336–1346. 10.1128/AEM.70.3.1336-1346.2004

Douillard, F.P., Ribbera, A., Xiao, K., Ritari, J., Rasinkangas, P., Paulin, L., Palva, A., Hao, Y., de Vos, W.M., 2016. Polymorphisms, chromosomal rearrangements, and mutator phenotype development during experimental evolution of Lactobacillus rhamnosus GG. American Society for Microbiology. Applied and Environmental Microbiology 82(13): 3783–3792. 10.1128/AEM.00255-16

Guidone, A., Parente, E., Zotta, T., Guinane, C.M., Rea, M.C., Stanton, C., Ross, R.P., Ricciadi, A., 2015. Polymorphisms in stress response genes in Lactobacillus plantarum: implications for classification and heat stress response. Annals of Microbiology 65: 297–305. 10.1007/s13213-014-0862-7

Han, J., Chen, D., Li, S., Li, X., Zhou, W.-W., Zhang, B. and Jia, Y., 2015. Antibiotic susceptibility of potentially probiotic Lactobacillus strains. Italian Journal of Food Science 27: 282–289. 10.14674/1120-1770/ijfs.v270

Huang, C.H. and Lee, F.L., 2011. The dnaK gene as a molecular marker for the classification and discrimination of the Lactobacillus casei group. Antonie Van Leeuwenhoek 99(2): 319–327. 10.1007/s10482-010-9493-6

Hunt, R., Sauna, Z.E., Ambudkar, S.V., Gottesman, M.M. and Kimchi-Sarfaty, C., 2009. Silent (synonymous) SNPs: should we care about them? Methods in Molecular Biology 578: 23–39. 10.1007/978-1-60327-411-1_2

Jeon, S., Kim, H., Choi, Y., Cho, S., Seo, M. and Kim, H., 2021. Complete genome sequence of the newly developed Lactobacillus acidophilus strain with improved thermal adaptability. Frontiers in Microbiology 12: 697351. 10.3389/fmicb.2021.697351

Kumar, S., Stecher, G. and Tamura, K., 2016. MEGA7: molecular evolutionary genetics analysis version 7.0. Molecular Biology and Evoluation 33: 1870–1874. 10.1093/molbev/msw054

Lebeuf-Taylor, E., McCloskey, N., Bailey, S.F., Hinz, A. and Kassen, R., 2019. The distribution of fitness effects among synonymous mutations in a gene under directional selection. eLife 8: e45952. 10.7554/eLife.45952

Liu, W., Su, X., Duo, N., Yu, J., Song, Y., Sun, T., Zha, M., Menghe, B., Zhang, H. and Sun, Z., 2019. A survey of the relationship between functional genes and acetaldehyde production characteristics in Streptococcus thermophilus by multilocus sequence typing. Journal of Dairy Science 102(11): 9651–9662. 10.3168/jds.2018-16203

López-González, M.J., Escobedo, S., Rodríguez, A., Neves Rute, A., Janzen, T. and Martínez, B., 2018. Adaptive evolution of industrial Lactococcus lactis under cell envelope stress provides phenotypic diversity. Frontiers in Microbiology 9: 2654. 10.3389/fmicb.2018.02654

Mahmmodi, P., Khoshkoo, Z., Basti, A.A., Shotorbani, P.M. and Khanjari, A., 2021. Effect of Bunium persicum essential oil, NaCl, bile salt, and their combinations on the viability of Lactobacillus acidophilus in probiotic yogurt. Quality Assurance and Safety of Crops & Foods 13(1): 37–48. 10.15586/qas.v13i1.858

Molina-Hoppner, A., Sato, T., Kato, C., Ganzle, M.G. and Vogel, R.F., 2003. Effects of pressure on cell morphology and cell division of lactic acid bacteria. Extremophiles 7: 511–516. 10.1007/s00792-003-0349-0

Papadimitriou, K., Alegría, Á., Bron, P.A., De Angelis, M., Gobbetti, M., Kleerebezem, M., Lemos, J.A., Linares, D.M., Ross, P., Stanton, C., Turroni, F., Van Sinderen, D., Varmanen, P., Ventura, M., Zuniga, M., Tsakalidou, E., Kok, J., 2016. Stress physiology of lactic acid bacteria. American Society for Microbiology. Microbiology and Molecular Biology Reviews 80(3): 837–890. 10.1128/MMBR.00076-15

Parente, E., Ciocia, F., Ricciardi, A., Zotta, T., Felis, G.E. and Torriani, S., 2010. Diversity of stress tolerance in Lactobacillus plantarum, Lactobacillus pentosus and Lactobacillus paraplantarum: a multivariate screening study. International Journal of Food Microbiology 144: 270–279. 10.1016/j.ijfoodmicro.2010.10.005

Price, M.N., Arkin, A.P. and Alm, E.J., 2006. The life-cycle of operons. PLoS Genetics 2(6): e96. 10.1371/journal.pgen.0020096

Riccardi, A., Parente, E., Guidone, A., Ianniello, R.G., Zotta, T., Abu Sayem, S.M. and Varcamonti, M., 2012. Genotypic diversity of stress response in Lactobacillus plantarum, Lactobacillus paraplantarum and Lactobacillus pentosus. International Journal of Food Microbiology 157: 278–285. 10.1016/j.ijfoodmicro.2012.05.018

Rocha, E.P.C., 2018. Neutral theory, microbial practice: challenges in bacterial population genetics. Molecular Biology and Evolution 35(6): 1338–1347. 10.1093/molbev/msy078

Rozas, J., Ferrer-Mata, A., Sánchez-Del Barrio, J.C., Guirao-Rico, S., Librado, P., Ramos-Onsins, S.E. and Sánchez-Gracia, A., 2017. DnaSP 6: DNA sequence polymorphism analysis of large data-sets. Molecular Biology and Evolution 34: 3299–3302 Editor Sudhir Kumar, Oxford University Press. 10.1093/molbev/msx248

Salvador-Castell, M., Oger, P. and Peters, J., 2020. Chapter 8 – high-pressure adaptation of extremophiles and biotechnological applications. In: Physiological and biotechnological aspects of extremophiles. Academic Press, pp. 105–122. 10.1016/B978-0-12-818322-9.00008-3

Serrano, L.M., Molenaar, D., Wels, M., Teusink, B., Bron, P.A., de Vos, W.M. and Smid, E.J., 2007. Thioredoxin reductase is a key factor in the oxidative stress response of Lactobacillus plantarum WCFS1. Microbial Cell Factories 6: 29. 10.1186/1475-2859-6-29

Sharma, A., Kaur, J., Lee, S. and Park, Y.S., 2019. Tracking of intentionally inoculated lactic acid bacteria strains in yogurt and pro-biotic powder. Microorganisms 8(1): 5. 10.3390/microorganisms8010005

Szklarczyk, D., Gable, A.L., Lyon, D., Junge, A., Wyder, S., Huerta-Cepas, J., Simonovic, M., Doncheva, N.T., Morris, J.H., Bork, P., Jensen, L.J., von Mering, C., 2019. STRING v11: protein-protein association networks with increased coverage, supporting functional discovery in genome-wide experimental datasets. Nucleic Acids Research 47: D607–D613. 10.1093/nar/gky1131

Tsuda, H., Okuda, S., Haraguchi, T. and Kodama, K., 2019. Influence of exopolysaccharide on the growth of lactic acid bacteria. Italian Journal of Food Science 31: 233–242. 10.14674/IJFS-1317

Van de Guchte, M., Serror, P., Chervaux, C., Smokvina, T., Ehrlich, S.D. and Maguin, E., 2002. Stress responses in lactic acid bacteria. Antonie Van Leeuwenhoek 82: 187–216. 10.1007/978-94-017-2029-8_12

Yaman, H., Sarica, E. and Coskun, H., 2020. A comparative study on the effect of high hydrostatic pressure on the ripening of Turkish white cheese from different milk species. Italian Journal of Food Science 32: 589–595. 10.14674/IJFS-1712

Yang, D., Zhang, Y., Zhao, L., Wang, Y., Rao, L. and Liao, X., 2021a. Pressure-resistant acclimation of lactic acid bacteria from a natural fermentation product using high pressure. LWT–Food Science and Technology 69: 102660. 10.1016/j.ifset.2021.102660

Yang, H., He, M. and Wu, C., 2021b. Cross protection of lactic acid bacteria during environmental stresses: stress responses and underlying mechanisms. LWT–Food Science and Technology 144: 111203. 10.1016/j.lwt.2021.111203

Zapaśnik, A., Sokołowska, B. and Bryła, M., 2022. Role of lactic acid bacteria in food preservation and safety. Foods 11(9): 1283. 10.3390/foods11091283