Regional microbial content of fermented traditional and industrial East Mediterranean sausages from the islands of Cyprus and Mytilini

Eleni Kamilari , Catherine Stanton , Dimitrios Tsaltas , R. Paul Ross

Microbiome Research Reports ›› 2024, Vol. 4 ›› Issue (1) : 3

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Microbiome Research Reports ›› 2024, Vol. 4 ›› Issue (1) :3 DOI: 10.20517/mrr.2024.47
Original Article

Regional microbial content of fermented traditional and industrial East Mediterranean sausages from the islands of Cyprus and Mytilini

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Abstract

Objective: To characterize the microbial biodiversity of fermented sausages from the East Mediterranean islands of Cyprus and Mytilini, and to identify differences between the microbial diversity of traditionally and industrially produced Cypriot sausages.

Method: The microbial diversity of thirty sausages from Cyprus and Mytilini (traditionally and industrially produced) was analyzed using high throughput sequencing (HTS) (amplicon sequencing) of 16S rRNA gene and ITS loci fragments. By applying microbial signature detection and machine learning algorithms, we identified key microbes that distinguish traditionally produced sausages from those produced industrially. Focusing on selected microbial taxa and using interaction network analysis, we identified associations among the sausages’ microbiota that may affect the shaping of the sausages’ microbial consortia.

Results: Cypriot and Mytilini sausages indicated increased relative representation of Lactobacillus and Leuconostoc. Cypriot sausages were distinguished by the presence of the fungi Debaryomyces hansenii and Candida spp., whereas Mytilini sausages by the bacteria Lactococcus and Streptococcus. Traditionally produced sausages from the Pitsilia region of Cyprus were differentiated by the presence of the species Lactobacillus helveticus, whereas industrially produced sausages were differentiated by the species Leuconostoc mesenteroides. Focusing mainly on Lactobacillus and Leuconostoc, negative associations with pathogenic bacteria, such as Salmonella, and spoilage fungi, such as Fusarium poae, were revealed.

Conclusion: The present metataxonomic analysis provided insights into the microbial communities that characterize Cypriot and Mytilini sausages. The findings provide an indication that the microbial diversity might be applied as an additional marker of Cypriot sausages’ authenticity.

Keywords

Sausages / fermented / Mediterranean / 16S rRNA gene / ITS loci / high-throughput sequencing / interaction networks

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Eleni Kamilari, Catherine Stanton, Dimitrios Tsaltas, R. Paul Ross. Regional microbial content of fermented traditional and industrial East Mediterranean sausages from the islands of Cyprus and Mytilini. Microbiome Research Reports, 2024, 4(1): 3 DOI:10.20517/mrr.2024.47

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References

[1]

Kamilari E,Anagnostopoulos DA.Cyprus sausages’ bacterial community identification through metataxonomic sequencing: evaluation of the impact of different DNA extraction protocols on the sausages’ microbial diversity representation.Front Microbiol2021;12:662957 PMCID:PMC8165277

[2]

Carballo J.Sausages: nutrition, safety, processing and quality improvement.Foods2021;10:890 PMCID:PMC8073304

[3]

Škrlep M,Batorek-Lukač N,Flores M.Aromatic profile, physicochemical and sensory traits of dry-fermented sausages produced without nitrites using pork from Krškopolje pig reared in organic and conventional husbandry.Animals2019;9:55 PMCID:PMC6406518

[4]

Van Reckem E, Geeraerts W, Charmpi C, Van der Veken D, De Vuyst L, Leroy F. Exploring the link between the geographical origin of European fermented foods and the diversity of their bacterial communities: the case of fermented meats.Front Microbiol2019;10:2302 PMCID:PMC6794416

[5]

Leroy F,Janssens M,Scholliers P.Meat fermentation at the crossroads of innovation and tradition: a historical outlook.Trends Food Sci Tech2013;31:130-7

[6]

Gaydos NJ,Campbell JA.Fate of pathogenic bacteria associated with production of pickled sausage by using a cold fill process.J Food Prot2016;79:1693-9

[7]

Nychas GJ,Tassou CC.Meat spoilage during distribution.Meat Sci2008;78:77-89

[8]

Francesca N,Moschetti G.Microbial characterisation of fermented meat products from the Sicilian swine breed “Suino Nero Dei Nebrodi”.Ann Microbiol2013;63:53-62

[9]

Hultman J,Ali J,Björkroth KJ.Meat processing plant microbiome and contamination patterns of cold-tolerant bacteria causing food safety and spoilage risks in the manufacture of vacuum-packaged cooked sausages.Appl Environ Microbiol2015;81:7088-97 PMCID:PMC4579449

[10]

Benson AK,Gilbreth SE.Microbial successions are associated with changes in chemical profiles of a model refrigerated fresh pork sausage during an 80-day shelf life study.Appl Environ Microbiol2014;80:5178-94 PMCID:PMC4136103

[11]

Połka J,Pisacane V,Puglisi E.Bacterial diversity in typical Italian salami at different ripening stages as revealed by high-throughput sequencing of 16S rRNA amplicons.Food Microbiol2015;46:342-56

[12]

Fontana C,López C.Microbial ecology involved in the ripening of naturally fermented llama meat sausages. A focus on lactobacilli diversity.Int J Food Microbiol2016;236:17-25

[13]

Pateiro M,Sant’Ana AS,Rodríguez-Lázaro D.Application of essential oils as antimicrobial agents against spoilage and pathogenic microorganisms in meat products.Int J Food Microbiol2021;337:108966

[14]

Alirezalu K,Yaghoubi M,Peighambardoust SH.Phytochemical constituents, advanced extraction technologies and techno-functional properties of selected Mediterranean plants for use in meat products. A comprehensive review.Trend Food Sci Tech2020;100:292-306

[15]

Singh VP.Recent approaches in food bio-preservation - a review.Open Vet J2018;8:104-11 PMCID:PMC5918123

[16]

Gómez I,Ibañez FC.The effects of processing and preservation technologies on meat quality: sensory and nutritional aspects.Foods2020;9:1416 PMCID:PMC7601710

[17]

Feng C.Optimisation of immersion vacuum cooling operation and quality of Irish cooked sausages by using response surface methodology.Int J Food Sci Tech2014;49:1850-8

[18]

Ferrocino I,Giordano M.Shotgun metagenomics and volatilome profile of the microbiota of fermented sausages.Appl Environ Microbiol2018;84:e02120-17 PMCID:PMC5772244

[19]

Bokulich NA,Richardson PM.Microbial biogeography of wine grapes is conditioned by cultivar, vintage, and climate.Proc Natl Acad Sci U S A2014;111:E139-48 PMCID:PMC3890796

[20]

Anagnostopoulos DA,Tsaltas D.Contribution of the microbiome as a tool for estimating wine’s fermentation output and authentication. In: Morata A, Loira I, editors. Advances in grape and wine biotechnology. IntechOpen; 2019.

[21]

Kamilari E,Antoniades A.High throughput sequencing technologies as a new toolbox for deep analysis, characterization and potentially authentication of protection designation of origin cheeses?.Int J Food Sci2019;2019:5837301 PMCID:PMC6925717

[22]

Franciosa I,Giordano M,Rantsiou K.Specific metagenomic asset drives the spontaneous fermentation of Italian sausages.Food Res Int2021;144:110379

[23]

Matchado MS,Reitmeier S.Network analysis methods for studying microbial communities: a mini review.Comput Struct Biotechnol J2021;19:2687-98 PMCID:PMC8131268

[24]

Kamilari E,Papademas P,Tsaltas D.Characterizing Halloumi cheese’s bacterial communities through metagenomic analysis.LWT2020;126:109298

[25]

Kamilari E,Karallis C.Metataxonomic analysis of grape microbiota during wine fermentation reveals the distinction of Cyprus regional terroirs.Front Microbiol2021;12:726483 PMCID:PMC8494061

[26]

Papademas P,Aspri M.Investigation of donkey milk bacterial diversity by 16S rDNA high-throughput sequencing on a Cyprus donkey farm.J Dairy Sci2021;104:167-78

[27]

Kamilari E,Papademas P,Tretiak S.Snapshot of Cyprus raw goat milk bacterial diversity via 16S rDNA high-throughput sequencing; impact of cold storage conditions.Fermentation2020;6:100

[28]

Anderson MJ.A new method for non-parametric multivariate analysis of variance.Austral Ecol2001;26:32-46

[29]

Bokulich NA,Rideout JR.Optimizing taxonomic classification of marker-gene amplicon sequences with QIIME 2’s q2-feature-classifier plugin.Microbiome2018;6:90 PMCID:PMC5956843

[30]

McDonald D,Goodrich J.An improved Greengenes taxonomy with explicit ranks for ecological and evolutionary analyses of bacteria and archaea.ISME J2012;6:610-8 PMCID:PMC3280142

[31]

Abarenkov K,Larsson KH.The UNITE database for molecular identification of fungi - recent updates and future perspectives.New Phytol2010;186:281-5

[32]

Segata N,Goll J.Microbial community function and biomarker discovery in the human microbiome.Genome Biol2011;12:P47

[33]

Pedregosa F,Gramfort A. Scikit-learn: machine learning in Python. J Mach Learning Res 2011;12:2825-30. Available from: https://www.jmlr.org/papers/volume12/pedregosa11a/pedregosa11a.pdf. [Last accessed on 19 Oct 2024]

[34]

Bokulich NA,Bolyen E,Huttley GA.q2-sample-classifier: machine-learning tools for microbiome classification and regression.J Open Res Softw2018;3:934 PMCID:PMC6759219

[35]

Kamilari E,Stanton C.Metataxonomic mapping of the microbial diversity of Irish and Eastern Mediterranean cheeses.Foods2022;11:2483 PMCID:PMC9407514

[36]

Faust K.CoNet app: inference of biological association networks using Cytoscape.F1000Res2016;5:1519 PMCID:PMC5089131

[37]

Shannon P,Ozier O.Cytoscape: a software environment for integrated models of biomolecular interaction networks.Genome Res2003;13:2498-504 PMCID:PMC403769

[38]

Barbieri F,Montanari C.Mediterranean spontaneously fermented sausages: spotlight on microbiological and quality features to exploit their bacterial biodiversity.Foods2021;10:2691 PMCID:PMC8624356

[39]

Huang Z,Huang X,He RK.Microbial diversity of representative traditional fermented sausages in different regions of China.J Appl Microbiol2021;130:133-41

[40]

Prado N,González P,Díaz J.Physicochemical, sensory and microbiological characterization of Asturian Chorizo, a traditional fermented sausage manufactured in Northern Spain.Meat Sci2019;156:118-24

[41]

Liu Y,Yohannes KW.Functional characteristics of lactobacillus and yeast single starter cultures in the ripening process of dry fermented sausage.Front Microbiol2020;11:611260 PMCID:PMC7819883

[42]

Drosinos EH,Kolovos G,Metaxopoulos I.Phenotypic and technological diversity of lactic acid bacteria and staphylococci isolated from traditionally fermented sausages in southern Greece.Food Microbiol2007;24:260-70

[43]

Montel M,Talon R.Bacterial role in flavour development.Meat Sci1998;49:S111-23

[44]

Bhattacharya D,Pateiro M,Dhar P.Lactic acid bacteria and bacteriocins: novel biotechnological approach for biopreservation of meat and meat products.Microorganisms2022;10:2058 PMCID:PMC9611938

[45]

Arief II,Suryati T,Fuziawan A.Antimicrobial activity of bacteriocin from indigenous Lactobacillus plantarum 2C12 and its application on beef meatball as biopreservative.J Indonesian Trop Anim Agric2014;37:90-5

[46]

Gao Y,Liu X.Effects of Lactobacillus sakei C2 and sakacin C2 individually or in combination on the growth of Listeria monocytogenes, chemical and odor changes of vacuum-packed sliced cooked ham.Food Control2015;47:27-31

[47]

Aspri M,Tsaltas D,Papademas P.Raw donkey milk as a source of Enterococcus diversity: assessment of their technological properties and safety characteristics.Food Control2017;73:81-90

[48]

Tidona F,Povolo M.Applicability of Lactococcus hircilactis and Lactococcus laudensis as dairy cultures.Int J Food Microbiol2018;271:1-7

[49]

FAO and WHO. Guidelines for the evaluation of probiotics in food. 2002. Available from: https://isappscience.org/wp-content/uploads/2019/04/probiotic_guidelines.pdf. [Last accessed on 19 Oct 2024]

[50]

Seleshe S.Effect of different Pediococcus pentosaceus and Lactobacillus plantarum strains on quality characteristics of dry fermented sausage after completion of ripening period.Food Sci Anim Resour2021;41:636-49 PMCID:PMC8277175

[51]

Porto MC,Azevedo PO,Oliveira RP.Pediococcus spp.: an important genus of lactic acid bacteria and pediocin producers.Biotechnol Adv2017;35:361-74

[52]

Ilavenil S,Kim DH.Assessment of probiotic, antifungal and cholesterol lowering properties of Pediococcus pentosaceus KCC-23 isolated from Italian ryegrass.J Sci Food Agric2016;96:593-601

[53]

Fugaban JII,Park YJ.Antimicrobial properties of Pediococcus acidilactici and Pediococcus pentosaceus isolated from silage.J Appl Microbiol2022;132:311-30

[54]

Kabiraz MP,Mahmud MMC,Ali A.Conventional and advanced detection techniques of foodborne pathogens: a comprehensive review.Heliyon2023;9:e15482 PMCID:PMC10161726

[55]

Chang SH,Tsai GJ.Effects of chitosan on Clostridium perfringens and application in the preservation of pork sausage.Mar Drugs2020;18:70 PMCID:PMC7074077

[56]

Pernu N,Lindström M.High prevalence of Clostridium botulinum in vegetarian sausages.Food Microbiol2020;91:103512

[57]

Muratoglu K,Hampikyan H,Cetin O.Detection, characterization and antibiotic susceptibility of Clostridioides (Clostridium) difficile in meat products.Food Sci Anim Resour2020;40:578-87 PMCID:PMC7372980

[58]

Mladenović KG,Kiš M.Enterobacteriaceae in food safety with an emphasis on raw milk and meat.Appl Microbiol Biotechnol2021;105:8615-27

[59]

Gwida M,Geue L.Occurrence of Enterobacteriaceae in raw meat and in human samples from egyptian retail sellers.Int Sch Res Notices2014;2014:565671 PMCID:PMC4897388

[60]

Jansen W,Müller A.The safety and quality of pork and poultry meat imports for the common European market received at border inspection post Hamburg Harbour between 2014 and 2015.PLoS One2018;13:e0192550 PMCID:PMC5806876

[61]

Nováková D,Pantůček R,Švec P.Staphylococcus equorum and Staphylococcus succinus isolated from human clinical specimens.J Med Microbiol2006;55:523-8

[62]

Prpich NZ, Camprubí GE, Cayré ME, Castro MP. Indigenous microbiota to leverage traditional dry sausage production.Int J Food Sci2021;2021:6696856 PMCID:PMC7868150

[63]

Van Ba H,Kim J.The effects of starter culture types on the technological quality, lipid oxidation and biogenic amines in fermented sausages.LWT2016;74:191-8

[64]

EFSA Panel on Biological Hazards. Scientific opinion on the maintenance of the list of QPS biological agents intentionally added to food and feed (2013 update).EFSA J2013;11:3449

[65]

Erkmen O. Microbiological analysis of foods and food processing environments. 2022. Available from: https://www.researchgate.net/publication/354968527_Microbiological_Analysis_of_Foods_and_Food_Processing_Environments. [Last accessed on 19 Oct 2024]

[66]

Wen R,Li XA,Kong B.The potential correlations between the fungal communities and volatile compounds of traditional dry sausages from Northeast China.Food Microbiol2021;98:103787

[67]

Ramos-Moreno L,Rodríguez-Castro E.Debaryomyces hansenii is a real tool to improve a diversity of characteristics in sausages and dry-meat products.Microorganisms2021;9:1512 PMCID:PMC8303870

[68]

Cano-García L,Belloch C.Generation of aroma compounds in a fermented sausage meat model system by Debaryomyces hansenii strains.Food Chem2014;151:364-73

[69]

Flores M,Cano-García L,Belloch C.Yeast strains as potential aroma enhancers in dry fermented sausages.Int J Food Microbiol2015;212:16-24

[70]

Prista C,Miranda IM.The halotolerant Debaryomyces hansenii, the Cinderella of non-conventional yeasts.Yeast2016;33:523-33

[71]

Angulo M,Medina-Córdova N,Angulo C.Probiotic and nutritional effects of Debaryomyces hansenii on animals.Appl Microbiol Biotechnol2020;104:7689-99

[72]

Jain U,Xiong S.Debaryomyces is enriched in Crohn’s disease intestinal tissue and impairs healing in mice.Science2021;371:1154-9 PMCID:PMC10114606

[73]

Haarer BK,Lillie SH.Identification of MYO4, a second class V myosin gene in yeast.J Cell Sci1994;107:1055-64

[74]

Makky EA,Mahmood MH,Qi WZ.Evaluation of the antioxidant and antimicrobial activities of ethyl acetate extract of Saccharomyces cerevisiae.Food Technol Biotechnol2021;59:127-36 PMCID:PMC8284104

[75]

Alarcón M,Díaz-Maroto MC,García-Ruiz A.Inactive dry yeast to improve the oxidative stability of Spanish dry-fermented sausage “salchichón”.LWT2021;146:111385

[76]

Kokkinofta R,Zervou M.Isotopic and elemental authenticity markers: a case study on cypriot wines.Food Anal Methods2017;10:3902-13

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