Metagenomic analysis of microbial diversity in sucuk, a traditional Turkish dry-fermented sausage, and its relationship with organic acid compounds

Main Article Content

Ali Soyuçok https://orcid.org/0000-0003-2626-5827

Keywords

Metagenomic; Microbiota; Organic acid; Sucuk; Turkish fermented sausage

Abstract

Sucuk is a traditional Turkish fermented meat product that is widely consumed in Türkiye. The aim of this study was to determine the microbial diversity and organic acid profile and to elucidate their mutual relationship. The most abundant phylum in sucuk was Firmicutes, followed by Proteobacteria and Cyanobacteria phyla. The most abundant genera in sucuk were Lactobacillus, Pediococcus, and Staphylococcus. Acetic, lactic, and tartaric acids were found in all sucuk samples. Tartaric and lactic acids were positively correlated with microbial diversity parameters. Furthermore, tartaric acid was found to be an indicator of the presence of a rare genus, while lactic acid was found to be an indicator of a balanced distribution among genus and the dominance of some genus. This study for the first time showed that the microbiota of fermented Turkish sausage will be an important contribution to future studies.

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References

Aquilanti L., Garofalo C., Osimani A. and Clementi F. 2016. Ecology of lactic acid bacteria and coagulase negative cocci in fermented dry sausages manufactured in Italy and other Mediterranean countries: an overview. Int. Food Res. J. 23(2):429–445.
Akköse A., Oğraş Ş.Ş., Kaya, M and Kaban G. 2023. Microbiological, physicochemical and sensorial changes during the ripening of sucuk, a traditional Turkish dry-fermented sausage: effects of autochthonous strains, sheep tail fat and ripening rate. Fermentation, 9(6):558. https://doi.org/10.3390/fermentation9060558
Anonymous. 2019. Turkish food codex Communiqu´e on meat, prepared meat mixtures and meat products, No.: 2018/52 (https://www.resmigazete.gov.tr/eskiler/2019/01/20190129-4.htm), Last access date: 10/12/2024.
Baka A.M., Papavergou E.J., Pragalaki T., Bloukas J.G. and Kotzekidou P. 2011. Effect of selected autochthonous starter cultures on processing and quality characteristics of Greek fermented sausages. LWT. 44 (1):54–61. https://doi.org/10.1016/j.lwt.2010.05.019
Bangar S.P., Suri S., Trif M. and Ozogul F. 2022. Organic acids production from lactic acid bacteria: a preservation approach. Food biosci. 46:101615. https://doi.org/10.1016/j.fbio.2022.101615
Barbieri F., Tabanelli G., Montanari C., Dall’Osso N., Šimat V., Smole Možina S., et al. 2021. Mediterranean spontaneously fermented sausages: spotlight on microbiological and quality features to exploit their bacterial biodiversity. Foods. 10(11):2691. https://doi.org/10.3390/foods10112691
Bassi D., Milani G., Belloso Daza M.V., Barbieri F., Montanari C., Lorenzini S., et al. 2022. Taxonomical identification and safety characterization of Lactobacillaceae from Mediterranean natural fermented sausages. Foods. 11(18):2776. https://doi.org/10.3390/foods11182776
Casaburi A., Di Martino V., Ferranti P., Picariello L. and Villani, F. 2016. Technological properties and bacteriocins production by Lactobacillus curvatus 54M16 and its use as starter culture for fermented sausage manufacture. Food Contr. 59, 31–45. https://doi.org/10.1016/j.foodcont.2015.05.016
Charmpi C., Van der Veken D., Van Reckem E., De Vuyst L. and Leroy F. 2020. Raw meat quality and salt levels affect the bacterial species diversity and community dynamics during the fermentation of pork mince. Food microbiol. 89:103434. https://doi.org/10.1016/j.fm.2020.103434
Cinar K., Kaban G., Borekci B.S., Gulluce M., Karadayi M. and Kaya M. 2018. Identification and characterization of lactic acid bacteria isolated from sucuk, a traditional Turkish dry-fermented sausage. J. Biotech. 280S,S61–S62. https://doi.org/10.1016/j.jbiotec.2018.06.198
De Filippis F., Parente E. and Ercolini D. 2017. Metagenomics insights into food fermentations. Microb. Biotechnol. 10(1):91–102. https://doi.org/10.1111/1751-7915.12421
Degenhardt R., Sobral Marques Souza D., Acordi Menezes L.A., de Melo Pereira G.V., Rodríguez-Lázaro D., Fongaro G., et al. 2021. Detection of enteric viruses and core microbiome analysis in artisanal colonial salami-type dry-fermented sausages from Santa Catarina, Brazil. Foods. 10(8):1957. https://doi.org/10.3390/foods10081957
Demirel Y.N. and Gürler, Z. 2018. The effect of natural microbiota on colour, texture and sensory properties of sucuk during the production. Ank. Univ. Vet. Fak. Derg. 65(2):137–143.
De Mey E., De Maere H., Paelinck H. and Fraeye I. 2017. Volatile N-nitrosamines in meat products: potential precursors, influence of processing, and mitigation strategies. Crit. Rev. Food Sci. Nutr. 57(13):2909–2923. https://doi.org/10.1080/10408398.2015.1078769
Doğan Y.N., Lenger Ö.F., Düz M., Doğan I. and Gürler Z. 2020. Effects of wild type lactic acid bacteria on histamine and tyramine formation in sucuk. J. Hellenic Vet. Med. Soc. 71:2553–2558. https://doi.org/10.12681/jhvms.25936
Erginkaya Z. 1993. Fermente sucuklarda organik asit miktarlarının belirlenmesi. Gıda, 18:6
Ferrocino I., Bellio A., Giordano M., Macori G., Romano A., Rantsiou K., et al. 2018. Shotgun metagenomics and volatilome profile of the microbiota of fermented sausages. Appl. Environ. Microbiol. 84(3):02120. https://doi.org/10.1128/AEM.02120-17
Fontana C., Bassi D., López C., Pisacane V., Otero M.C., Puglisi E., et al. 2016. Microbial ecology involved in the ripening of naturally fermented llama meat sausages. A focus on lactobacilli diversity. Int. J. Food Microbiol. 236:17–25. https://doi.org/10.1016/j.ijfoodmicro.2016.07.002
Franciosa I., Ferrocino I., Giordano M., Mounier J., Rantsiou K. and Cocolin L. 2021. Specific metagenomic asset drives the spontaneous fermentation of Italian sausages. Food Res. Int. 144:110379. https://doi.org/10.1016/j.foodres.2021.110379
Halagarda M. and Wójciak K.M. 2022. Health and safety aspects of traditional European meat products. A review. Meat Sci. 184:108623. https://doi.org/10.1016/j.meatsci.2021.108623
Hwang J., Kim Y., Seo Y., Sung M., Oh J. and Yoon Y. 2023. Effect of starter cultures on quality of fermented sausages. Food Sci. Anim. Resour. 43(1):1–9. https://doi.org/10.5851/kosfa.2022.e75
Janßen D., Eisenbach L., Ehrmann M.A. and Vogel R.F. 2018. Assertiveness of Lactobacillussakei and Lactobacillus curvatus in a fermented sausage model. Int. J. Food Microbiol. 285:188–197. https://doi.org/10.1016/j.ijfoodmicro.2018.04.030
Kaban G. and Kaya M. 2008. Identification of lactic acid bacteria and gram‐positive catalase‐positive cocci isolated from naturally fermented sausage (sucuk). J. Food. Sci. 73(8): 385–388. https://doi.org/10.1111/j.1750-3841.2008.00906.x
Kaban G., Kaya M. and Lücke F.K. 2012. Meat starter cultures. Taylor & Francis. New York.
Kamiloğlu A., Kaban G. and Kaya M. 2019. Effects of autochthonous Lactobacillus plantarum strains on Listeria monocytogenes in sucuk during ripening. J. Food Saf. 39(3):e12618. https://doi.org/10.1111/jfs.12618
Kamiloğlu A., Kaban G. and Kaya M. 2020. Technological properties of autochthonous Lactobacillus plantarum strains isolated from sucuk (Turkish dry-fermented sausage). Braz. J. Microbiol. 51(3):1279–1287. https://doi.org/10.1007/s42770-020-00262-9
Kesmen Z., Yetiman A.E., Gulluce A., Kacmaz N., Sagdic O., Çetin B, et al. 2012. Combination of culture-dependent and culture-independent molecular methods for the determination of lactic microbiota in sucuk. Int. J. Food Microbiol. 153(3):428-435. https://doi.org/10.1016/j.ijfoodmicro.2011.12.008
Kilic B. 2009. Current trends in traditional Turkish meat products and cuisine. LWT. 42(10):1581–1589. https://doi.org/10.1016/j.lwt.2009.05.016
Kim J.H., Lee E.S., Kim B.M. and Oh M.H. 2022. Potential correlation between microbial diversity and volatile flavor compounds in different types of Korean dry-fermented sausages. Foods. 11(20):3182. https://doi.org/10.3390/foods11203182
Laranjo M., Potes M.E. and Elias M. 2019. Role of starter cultures on the safety of fermented meat products. Front. Microbiol. 10:853. https://doi.org/10.3389/fmicb.2019.00853
Liao R., Xia Q., Zhou C., Geng F., Wang Y., Sun Y., et al. 2022. LC-MS/MS-based metabolomics and sensory evaluation characterize metabolites and texture of normal and spoiled dry-cured hams. Food Chem. 371:131156. https://doi.org/ 10.1016/j.foodchem.2021.131156
Liu D., Ainsworth A.J., Austin F.W. and Lawrence M.L. 2004. Use of PCR primers derived from a putative transcriptional regulator gene for species-specific determination of Listeria monocytogenes. Int. J. Food Microbiol. 91(3):297–304. https://doi.org/10.1016/j.ijfoodmicro.2003.07.004
Liu Y., Cao Y., Yohannes Woldemariam K., Zhong S., Yu Q. and Wang J. 2023. Antioxidant effect of yeast on lipid oxidation in salami sausage. Front. Microbiol. 13:1113848. https://doi.org/10.3389/fmicb.2022.1113848
Metin B. and Toy A. 2023. Dynamics of lactic acid bacteria during pastırma production. JMBFS. 12(4):9071. https://doi.org/10.55251/jmbfs.9071
Nazlı B., Pehlivanoglu H. and Caglar M.Y. 2017. Characteristics of traditional Turkish fermented soudjouk and current situation. Int. J. Vet. Sci. Techno. 1(1):013–019.
Nediani M.T., García L., Saavedra L., Martínez S., Lopez Alzogaray S. and Fadda S. 2017. Adding value to goat meat: biochemical and technological characterization of autochthonous lactic acid bacteria to achieve high-quality fermented sausages. Microorganisms. 5(2):26. https://doi.org/10.3390/microorganisms5020026
Özdal T. 2020. Changes in physicochemical, microbiological and sensory characteristics of traditionally produced Turkish sucuk during ripening and storage: natural or synthetic additives? Gıda. 45(2):329–339. https://doi.org/10.15237/gida.GD20013
Parmar S., Li Q., Wu Y., Li X., Yan J., Sharma V.K., et al. 2018. Endophytic fungal community of Dysphania ambrosioides from two heavy metal‐contaminated sites: evaluated by culture‐dependent and culture‐independent approaches. Microb. Biotechnol. 11(6):1170–1183. https://doi.org/10.1111/1751-7915.13308
Ravyts F., Vuyst L. and Leroy F. 2012. Bacterial diversity and functionalities in food fermentations. Eng. Life. Sci. 12(4):356–367. https://doi.org/10.1002/elsc.201100119
Soyuçok A. 2022. Fermantasyon ve Kurutma Boyunca Tarhana Hamurunda Meydana Gelen Organik Asit Kinetiğinin Belirlenmesi. Van Vet. J. 33(3):130–134. https://doi.org/10.36483/vanvetj.1182691
Stavropoulou D.A, Reckem E.V., Smet S.D., Vuyst L.D. and Leroy F. 2018a. The narrowing down of inoculated communities of coagulase-negative staphylococci in fermented meat models is modulated by temperature and pH. Int. J. Food Microbiol. 274:52–59. https://doi.org/10.1016/j.ijfoodmicro. 2018.03.00
Stavropoulou D.A., Filippou P., De Smet S., De Vuyst L. and Leroy F. (2018b). Effect of temperature and pH on the community dynamics of coagulase-negative staphylococci during spontaneous meat fermentation in a model system. Food microbiol. 76:180–188. https://doi.org/10.1016/j.fm.2018.05.006
Ucak S., Yurt M.N.Z., Tasbasi B.B., Acar E.E., Altunbas O., Soyucok A., et al. 2022. Identification of bacterial communities of fermented cereal beverage Boza by metagenomic analysis. LWT. 153:112465. https://doi.org/10.1016/j.lwt.2021.112465
Van Reckem E., Geeraerts W., Charmpi C., Van der Veken D., De Vuyst L. and Leroy F. 2019. Exploring the link between the geographical origin of European fermented foods and the diversity of their bacterial communities: the case of fermented meats. Front. Microbiol. 10:2302. https://doi.org/10.3389/fmicb.2019.02302
Yang P., Zhong G., Yang J., Zhao L., Sun D., Tian Y., et al. 2022. Metagenomic and metabolomic profiling reveals the correlation between the microbiota and flavor compounds and nutrients in fermented sausages. Food Chem. 375:131645. https://doi.org/10.1016/j.foodchem.2021.131645
Zheng J., Wittouck S., Salvetti E., Franz C.M., Harris H., Mattarelli P., et al. 2020. A taxonomic note on the genus Lactobacillus: description of 23 novel genera, emended description of the genus Lactobacillus Beijerinck 1901, and union of Lactobacillaceae and Leuconostocaceae. Int. J. Syst. Evol. Microbiol. 70(4):2782–2858. https://doi.org/10.1099/ijsem.0.004107