Research advances of deciphering Shalgam microbiota profile and dynamics

Abstract

The relationship between the microbiota and their functions in the quality and characteristic flavors of the fermented foods that provide them autochthonous attributes has been remained elusive, so far. With the demand in elucidating the microbiota of the autochthonous fermented foods, the characterization of the shalgam microbiota via culture-dependent and culture-independent methods has been carried out. To shed light on shalgam microbiota harboring Lactic acid bacteria (LAB) and yeasts, microorganisms isolated from shalgam have been identified by culture-dependent methods including 16S rRNA and ITS (Internal Transcribed Spacer) gene regions sequencing, RAPD-PCR, Rep-PCR, and API CHL50. Culture-independent characterization methods such as 16S rRNA and ITS meta-barcoding sequencing were performed to pinpoint the microbial diversity within shalgam. More recently, bioinformatics and in vitro analysis of bacteria and yeast isolated from shalgam to find prospective probiotics and elucidate shalgam microbiota dynamics due to the types of salts used in shalgam production have been reported. In this review, we intend to collate the data on microorganisms identified via culture-dependent and culture-independent methods. Taken together, we presented a broad perspective on the shalgam microbiota and how future endeavors in shalgam microbiota research can move forward.

Keywords

• Shalgam microbiota
• Culture-independent
• Culture-dependent methods
• Lactic acid bacteria

References

1. Ağırman, B., & Erten, H. (2018). The Influence of Various Chloride Salts to Reduce Sodium Content on the Quality Parameters of Şalgam (Shalgam): A Traditional Turkish Beverage Based on Black Carrot. Journal of Food Quality, 11. https://doi.org/10.1155/2018/3292185.
2. Ağırman, B., Settanni, L., & Erten, H. (2021). Effect of different mineral salt mixtures and dough extraction procedure on the physical, chemical and microbiological composition of Shalgam: A black carrot fermented beverage Dough (dough fermentation) Sorting-Grading. Food Chemistry, 344. https://doi: 10.1016/j.foodchem.2020.128618.
3. Akbulut, M., & Çoklar, H. (2020). Utilization of Black Grape Pomace in the Production of Shalgam Juice: Effect on the Ethyl Alcohol Levels. Journal of Halal Life Style, 2(2), 109–115.
4. Akman, K. P., Özülkü, G., Tornuk, F., & Yetim, H. (2021). Potential probiotic lactic acid bacteria isolated from fermented gilaburu and shalgam beverages. LWT, 149(May), 111705.https://doi.org/10.1016/j.lwt.2021.111705.
5. Altay, F., Karbancioğlu-Güler, F., Daşkaya-Dikmen, C., & Heperkan, D. (2013). A review on traditional Turkish fermented non-alcoholic beverages: Microbiota, fermentation process and quality characteristics. International Journal of Food Microbiology, 167(1), 44–56. https://doi.org/10.1016/j.ijfoodmicro.2013.06.016.
6. Arıcı, M. (2004). Microbiological and chemical properties of a drink called shalgam. (Mikrobiologische und chemische eigenschaften von Shalgam), Ernahrungs-Umschau., 51 (1), 10.
7. Aydın, F., Özer, G., Alkan, M., & Çakır, İ. (2020). The utility of iPBS retrotransposons markers to analyze genetic variation in yeast. International Journal of Food Microbiology, 325. https://doi: 10.1016/j.ijfoodmicro.2020.108647.
8. Baser, M., Sofu, A., Özcan, E., Korachi, M., & Ekinci, F. Y. (2012). Characterization of dominant microbial populations in shalgam juice using 16S rRNA. New Biotechnology, 29 (September),118.https://doi.org/10.1016/j.nbt.2012.08.331.

9. Bayram, M., Erdoğan, S., Esin, Y., Saraçoğlu, O., & Kaya, C. (2014). Farklı siyah havuç miktarlarının şalgam suyunun bileşimine ve duyusal özellikleri üzerine etkisi. Akademik Gıda, 12(1), 29–34 (In Turkish)
10. Boeke, J. D., & Devine, S. E. (1998). Yeast retrotransposons: finding a nice quiet neighborhood. Cell, 93(7), 1087-1089. https://doi.org/10.1016/S0092-8674(00)81450-6.
11. Brandsma, J. B., Rustandi, N., Brinkman, J., Wolkers‐Rooijackers, J. C., Zwietering, M. H., & Smid, E. J. (2022). Pivotal role of cheese salting method for the production of 3‐methylbutanal by Lactococcus lactis. International Journal of Dairy Technology, 75(2), 421-430. https://doi.org/10.1111/1471-0307.12839.
12. Canbaş, A.; Fenercioglu, H. (1984). Şalgam suyu uzerine bir arastirma. Gıda (Food)., 9(5), 279–286 (In Turkish) Carraro, L., Maifreni, M., Bartolomeoli, I., Martino, M. E., Novelli, E., Frigo, F., Marino M. & Cardazzo, B. (2011). Comparison of culture-dependent and-independent methods for bacterial community monitoring during Montasio cheese manufacturing. Research in Microbiology, 162(3), 231-239.https://doi.org/10.1016/j.resmic.2011.01.002.
13. Coşkun, F. (2017). A traditional Turkish fermented non-alcoholic beverage, shalgam. Beverages, 3(4). https://doi.org/10.3390/beverages3040049.
14. Demir, N., Acar, J., & Bahçeci, K. S. (2004). Effects of storage on quality of carrot juices produced with lactofermentation and acidification. European Food Research and Technology, 218(5), 465–468. https://doi.org/10.1007/s00217-004-0883-8.
15. Demir, N., Bahçeci, K. S., & Acar, J. (2006). The effects of different initial Lactobacillus plantarum concentrations on some properties of fermented carrot juice. Journal of Food Processing and Preservation, 30(3), 352–363. https://doi.org/10.1111/j.1745-4549.2006.00070.x.
16. Dereli, U., Türkyilmaz, M., Yemiş, O., & Özkan, M. (2015). Effects of Clarification and Pasteurization on the Phenolics, Antioxidant Capacity, Color Density and Polymeric Color of Black Carrot (Daucus Carota L.) Juice. Journal of Food Biochemistry, 39(5), 528–537. https://doi.org/10.1111/jfbc.12155.
17. Ekici H., Kadiroğlu P., & Ilgaz C. (2022). Next-generation sequencing of shalgam flavor influencing microflora. Journal of Food Processing and Preservation, 1–12. https://doi.org/10.1111/jfpp.15982.
18. Ekinci, F. Y., Baser, G. M., Özcan, E., Üstündağ, Ö. G., Korachi, M., Sofu, A., Blumberg, J. B., & Chen, C. Y. O. (2016). Characterization of chemical, biological, and antiproliferative properties of fermented black carrot juice, shalgam. European Food Research and Technology, 242(8), 1355–1368. https://doi.org/10.1007/s00217-016-2639-7.
19. Erginkaya, Z., & Hammes, W. P. (1992). Şalgam suyu fermentasyonu sırasında mikroorganizmaların gelişimi ve izole edilen laktik asit bakterilerinin tanımlanmaları üzerine bir araştırma. Gıda 17(5), 311–314 (In Turkish)
20. Erginkaya, Z., & Turhan, E. Ü. (2016). Enumeration and Identification of Dominant Microflora during the Fermentation of Shalgam. Akademik Gıda, 14(2), 92–97.
21. Erten, H., Tanguler, H., & Canbaş, A. (2008). A traditional Turkish lactic acid fermented beverage: Shalgam (Şalgam). Food Reviews International, 24(3), 352–359. https://doi.org/10.1080/87559120802089324.
22. Gobbetti, M., Minervini, F., Pontonio, E., Di Cagno, R. & De Angelis, M. (2016). Drivers for the establishment and composition of the sourdough lactic acid bacteria biota. Int. J. Food Microbiol. 239, 3–18. https://doi.org/10.1016/j.ijfoodmicro.2016.05.022.
23. Gümüştop, İ. & Ortakçı, F. (2022). Evaluating the microbial growth kinetics and artificial gastric digestion survival of a novel Pichia kudriavzevii FOL-04. Biotech Studies. 31(1), 28-35. http://doi.org/10.38042/biotechstudies.1103767.
24. Güven, N., Yetim, H., & Cankurt, H. (2019). Physicochemical and Sensory Properties of low salt turnip juıce produced by using black carrot juıce and whey. Avrupa Bilim ve Teknoloji Dergisi Sayı, 15, 599–610. https://doi.org/10.31590/ejosat.539492 (In Turkish)
25. İbrahim, H., Akbulut, M., & Coklar, H. (2022). Identification and technological characterization of endogenous yeast isolated from fermented black carrot juice, shalgam. LWT, 154, 112823. https://doi.org/10.1016/j.lwt.2021.112823.
26. Kahve, H. I., Akbulut, M., & Coklar, H. (2022). Identification and technological characterization of endogenous yeast isolated from fermented black carrot juice, shalgam. LWT, 154, 112823. https://doi.org/10.1016/j.lwt.2021.112823.
27. Kafkaskıray, E. S. (2020). Şalgam suyu fermantasyon sürecinin mikrobiyal profilinin moleküler yöntemlerle belirlenmesi. Yüksek Lisans Tezi. İstanbul Sabahattin Zaim Üniversitesi (In Turkish)
28. Karaoğlan A. (2013). Şalgam suyunda bozulma yapan mayaların atımlı UV ışık ile inaktivasyonu. Yüksek Lisans Tezi. Cumhuriyet Üniversitesi (In Turkish)
29. Kelebek, H., Kadiroğlu, P., Sönmezdağ, A. S., Güçlü, G., Kola, O., Selli, S. (2018). Characterization of bioactive compounds and antioxidant potential of fermented beverage: Shalgam, International Conference on Raw Materials to Processed Foods, 11–13 April, http://rpfoods2018.org/.
30. Kırca, A., Özkan, M., & Cemeroǧlu, B. (2007). Effects of temperature, solid content and pH on the stability of black carrot anthocyanins. Food Chemistry, 101(1), 212–218. https://doi.org/10.1016/j.foodchem.2006.01.019.
31. Lamba, J., Goomer, S., & Saxena, S. K. (2019). International Journal of Gastronomy and Food Science Study the lactic acid bacteria content in traditional fermented Indian drink: Kanji. International Journal of Gastronomy and Food Science, 16(May 2018), 100143. https://doi.org/10.1016/j.ijgfs.2019.100143.
32. Materia, V. C., Linnemann, A. R., Smid, E. J., & Schoustra, S. E. (2021). Contribution of traditional fermented foods to food systems transformation: value addition and inclusive entrepreneurship. Food Security, 13(5), 1163-1177. https://doi.org/10.1007/s12571-021-01185-5.
33. Mete, A., Coşansu, S., Demirkol, O., & Ayhan, K. (2017). Amino acid decarboxylase activities and biogenic amine formation abilities of lactic acid bacteria isolated from shalgam. International Journal of Food Properties, 20(1), 171–178. https://doi.org/10.1080/10942912.2016.1152479.
34. Minervini, F., Dinardo, F. R., Angelis, M. De, & Gobbetti, M. (2019). Tap water is one of the drivers that establish and assembly the lactic acid bacterium biota during sourdough preparation. Scientific Reports, July 2018, 1–12. https://doi.org/10.1038/s41598-018-36786-2.
35. Okçu, G., Ayhan, K., Güneş Altuntaş, E., Vural, N., & Poyrazoğlu, E. S. (2016). Determination of phenolic acid decarboxylase produced by lactic acid bacteria isolated from shalgam (şalgam) juice using green analytical chemistry method. Lwt, 66, 615–621. https://doi.org/10.1016/j.lwt.2015.10.072.
36. Özdemir-Alper N., Acar, J. (1996) Flüssiges Obst 63:521–523 (In Turkish)
37. Özdemir S.S.& Güldemir O. Şalgam Ve Kanji: Kültürlerarasi Bir Ürün Olarak Fermente Siyah Havuç İçecekleri. (2021). Motif Akademi Halkbilimi Dergisi, 14(35), 0–3 (In Turkish).https://doi.org/10.12981/mahder.935537.
38. Özer, N. & Çoksöyler, F. N. (2015). Şalgam Suyunun Bazi Ki̇myasal Mi̇krobi̇yoloji̇ Özelli̇kleri̇. Gıda, 40, 31–38. https://doi.org/10.15237/gida.GD14068.
39. Schillinger, U., & Lücke, F. K. (1987). Identification of lactobacilli from meat and meat products. Food Microbiology, 4(3), 199–208. https://doi.org/10.1016/0740-0020(87)90002-5.
40. Tangüler, H. (2021). The Effect of Using Different Size Purple Carrots and Lactobacillus Plantarum on the Properties of Fermented Shalgam (Şalgam). Turkish Journal of Agriculture-Food Science and Technology, 9(10), 1759–1766. https://doi.org/10.24925/turjaf.v9i10.1759-1766.4246.
41. Tangüler, H., Dinç, S. Ö., & Beylikci, S. C. (2020). Suggestions and Last Trends Related to Şalgam Beverage which is Traditional Product of Turkey. Turkish Journal of Agriculture-Food Science and Technology, 8(6), 1266–1271. https://doi.org/10.24925/turjaf.v8i6.1266-1271.3266.
42. Tangüler, H., Dinç, S. Ö., Ekenel, G., Aytekin, D. A., Şimşek, C., & Ataklı, H. (2022). Effect of Production Method and Temperature on Quality Characteristics of Shalgam Beverages during Storage. Akademik Gida, 20(1), 20–29. https://doi.org/10.24323/akademik-gida.1097814.
43. Tangüler, H. & Erten, H. (2012a). Şalgam Suyu Üretiminde Gerçekleştirilen Hamur Fermantasyonu Sırasında. Akademik Gıda, 10(2), 48–54. (In Turkish)
44. Tangüler, H., & Erten, H. (2012b). Occurrence and growth of lactic acid bacteria species during the fermentation of shalgam (şalgam), a traditional Turkish fermented beverage. Lwt, 46(1), 36–41. https://doi.org/10.1016/j.lwt.2011.10.026.
45. Tangüler, H., & Erten, H. (2012c). Chemical and Microbiological Characteristics of Shalgam (Şalgam): A Traditional Turkish Lactic Acid Fermented Beverage. Journal of Food Quality, 35(4), 298–306. https://doi.org/10.1111/j.1745-4557.2012.00447.x.
46. Tangüler, H., & Erten, H. (2013). Selection of potential autochthonous starter cultures from shalgam, a traditional Turkish lactic acid-fermented beverage. Turkish Journal of Agriculture and Forestry, 37(2), 212–220. https://doi.org/10.3906/tar-1205-37.
47. Tangüler, H., Erten, H., Bozdogan, A., Aksay, S., & Kelebek, H. (2021). Comparison of anthocyanin profiles in şalgams (shalgams) produced with different production procedures. Journal of Food Processing and Preservation, 1–11. https://doi.org/10.1111/jfpp.14770.
48. Tangüler, H., Saris, P. E. J., & Erten, H. (2015). Microbial, chemical and sensory properties of shalgams made using different production methods. Journal of the Science of Food and Agriculture, 95(5), 1008–1015. https://doi.org/10.1002/jsfa.6781.
49. Tangüler, H., Selli, S., Sen, K., Cabaroglu, T., & Erten, H. (2017). Aroma composition of shalgam: a traditional Turkish lactic acid fermented beverage. Journal of Food Science and Technology, 54(7), 2011–2019. https://doi.org/10.1007/s13197-017-2637-1.
50. Tangüler, H., Utus, D., & Erten, H. (2014). Effect of black carrot size usage on the quality of shalgam (şalgam): A traditional Turkish lactic acid fermented beverage. Indian Journal of Traditional Knowledge, 13(4), 647–653.
51. Tanrıseven, D., Selli, S., & Kelebek, H. (2020). LC-DAD-ESI-MS / MS-assisted elucidation of the phenolic compounds in shalgams: Comparison of traditional and direct methods. Food Chemistry, 305(March 2019). https://doi.org/10.1016/j.foodchem.2019.125505.
52. Tazehkand, M. N., & Valipour, E. (2019). Cytotoxic , antimicrobial and DNA breaking activity of Şalgam. Indian Journal of Biochemistry & Biophysics, 56, 169–174.
53. Toktaş, B., Bildik, F., & Özçelik, B. (2018). Effect Of Fermentation On Anthocyanin Stability And In Vitro Bioaccessibility During Shalgam (Şalgam) Beverage Production. Journal of the Science of Food and Agriculture, 98(8), 3066–3075. https://doi.org/10.1002/jsfa.8806.
54. Türker, N., Aksay, S., & Ekiz, H. I. (2004). Effect of storage temperature on the stability of anthocyanins of a fermented black carrot (Daucus carota var. L.) beverage: Shalgam. Journal of Agricultural and Food Chemistry, 52(12), 3807–3813. https://doi.org/10.1021/jf049863s.
55. Türker, N., Aksay, S., Istanbullu, O., & Artuvan, E. (2007). A study on the relation between anthocyanin content and product quality: shalgam as a model beverage. Journal of food quality, 30(6), 953-969. https://doi.org/10.1021/jf049863s.
56. Türkyılmaz, M., Yemi, O., & Özkan, M. (2012). Clarification and pasteurisation effects on monomeric anthocyanins and percent polymeric colour of black carrot (Daucus carota L.) juice. Food Chemistry, 134(2), 1052–1058. https://doi.org/10.1016/j.foodchem.2012.03.013.
57. Ulucan, E. (2019). Fermentasyon Sonrasi Ultrason Uygulamasinin Şalgam Sularinin Bazi Fizikokimyasal ve Mikrobiyolojik Ozelligi Uzerine Etkisi. Yüksek Lisans Tezi. Selçuk Üniversitesi. (In Turkish)
58. Uzay, M., Öztürk, H. İ., Buzrul, S., & Maskan, M. (2021). A study on rheological properties, sensory evaluation and shelf life of ayran–shalgam mixtures. Journal of Food Science and Technology, 58(7), 2479-2486. https://doi: 10.1007/s13197-020-04754-2.
59. Wang, S., Wu, Q., Nie, Y., Wu, J., & Xu, Y. (2019). Construction of synthetic microbiota for reproducible flavor compound metabolism in Chinese light-aroma-type liquor produced by solid-state fermentation. Applied and Environmental Microbiology, 85(10), 1–14. https://doi.org/10.1128/AEM.03090-18.
60. Weinroth M. D., Belk A. D., Dean C., Noyes N., Dittoe D. K., Rothrock, M. J., Ricke S. C., Myer P. R., Henniger M. T., Ramírez G. A., Oakley B. B., Summers K. L., Miles A. M., Ault-Seay T. B., Yu Z., Metcalf J. L., Wells J. E. (2022) Considerations and best practices in animal science 16S ribosomal RNA gene sequencing microbiome studies, Journal of Animal Science, 100(2), https://doi.org/10.1093/jas/skab346. Wu, W., Wang, Z., Xu, B., Cai, J., Cheng, J., Mu, D., Wu, X., & Li, X. (2022). Exploring Core Microbiota Based on Characteristic Flavor Compounds in Different Fermentation Phases of Sufu. Molecules, 27(15). https://doi.org/10.3390/molecules27154933.
61. Yavuz, M., Kasavi, C., & Öner, E. T. (2021). Developments in effective use of volatile organic compound analysis to assess flavour formation during cheese ripening. Journal of Dairy Research, 88(4), 461-467. https://doi: 10.1017/S0022029921000790.
62. Yetiman, A. E., Keskin, A., Darendeli, B. N., Kotil, S. E., Ortakci, F., & Dogan, M. (2022). Characterization of genomic, physiological, and probiotic features Lactiplantibacillus plantarum DY46 strain isolated from traditional lactic acid fermented shalgam beverage. Food Bioscience, 46. https://doi.org/10.1016/j.fbio.2021.101499.
63. Yetiman, A. E., & Ortakci, F. (2022). Genomic, probiotic, and metabolic potentials of Liquorilactobacillus nagelii AGA58, a novel bacteriocinogenic motile strain isolated from lactic acid-fermented shalgam. Journal of Bioscience and Bioengineering.
64. Yetiman, A., Horzum, M., Bahar, D., & Akbulut, M. (2023). Assessment of Genomic and Metabolic Characteristics of Cholesterol-Reducing and GABA Producer imosilactobacillus fermentum AGA52 Isolated from Lactic Acid Fermented Shalgam Based on “In Silico” and “In Vitro” Approaches. Probiotics and Antimicrobial Proteins, 1-18. https://doi.org/10.1007/s12602-022-10038-2.
65. Yılmaz-Ersan, L., & Turan, M. A. (2012). Major and minor element concentrations in fermented shalgam beverage. International Journal of Food Properties, 15(4), 903–911. https://doi.org/10.1080/10942912.2010.506621.