Characterization of aerobic spore-forming bacteria associated with industrial dairy processing environments and product spoilage
Due to changes in the design of industrial food processing and increasing international trade, highly thermoresistant spore-forming bacteria are an emerging problem in food production. Minimally processed foods and products with extended shelf life, such as milk products, are at special risk for con...
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description | Due to changes in the design of industrial food processing and increasing international trade, highly thermoresistant spore-forming bacteria are an emerging problem in food production. Minimally processed foods and products with extended shelf life, such as milk products, are at special risk for contamination and subsequent product damages, but information about origin and food quality related properties of highly heat-resistant spore-formers is still limited. Therefore, the aim of this study was to determine the biodiversity, heat resistance, and food quality and safety affecting characteristics of aerobic spore-formers in the dairy sector. Thus, a comprehensive panel of strains (n=467), which originated from dairy processing environments, raw materials and processed foods, was compiled. The set included isolates associated with recent food spoilage cases and product damages as well as isolates not linked to product spoilage. Identification of the isolates by means of Fourier-transform infrared spectroscopy and molecular methods revealed a large biodiversity of spore-formers, especially among the spoilage associated isolates. These could be assigned to 43 species, representing 11 genera, with Bacillus cereus s.l. and Bacillus licheniformis being predominant. A screening for isolates forming thermoresistant spores (TRS, surviving 100°C, 20min) showed that about one third of the tested spore-formers was heat-resistant, with Bacillus subtilis and Geobacillus stearothermophilus being the prevalent species. Strains producing highly thermoresistant spores (HTRS, surviving 125°C, 30min) were found among mesophilic as well as among thermophilic species. B. subtilis and Bacillus amyloliquefaciens were dominating the group of mesophilic HTRS, while Bacillus smithii and Geobacillus pallidus were dominating the group of thermophilic HTRS. Analysis of spoilage-related enzymes of the TRS isolates showed that mesophilic strains, belonging to the B. subtilis and B. cereus groups, were strongly proteolytic, whereas thermophilic strains displayed generally a low enzymatic activity and thus spoilage potential. Cytotoxicity was only detected in B. cereus, suggesting that the risk of food poisoning by aerobic, thermoresistant spore-formers outside of the B. cereus group is rather low.
•Great biodiversity of aerobic spore-formers associated with dairy product spoilage•Characterization of thermoresistant spores (TRS) from dairy production•Non-dairy ingredients are important TRS |
doi_str_mv | 10.1016/j.ijfoodmicro.2013.07.004 |
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•Great biodiversity of aerobic spore-formers associated with dairy product spoilage•Characterization of thermoresistant spores (TRS) from dairy production•Non-dairy ingredients are important TRS contamination sources in dairy production.•Mesophilic TRS show generally a higher spoilage potential than thermophilic TRS.•Spoilage potential of TRS is high, while toxigenic potential is in general low.</description><identifier>ISSN: 0168-1605</identifier><identifier>EISSN: 1879-3460</identifier><identifier>DOI: 10.1016/j.ijfoodmicro.2013.07.004</identifier><identifier>PMID: 23973839</identifier><identifier>CODEN: IJFMDD</identifier><language>eng</language><publisher>Amsterdam: Elsevier B.V</publisher><subject>Animals ; Bacillus amyloliquefaciens ; Bacillus cereus ; Bacillus licheniformis ; Bacillus smithii ; Bacillus subtilis ; Bacteria, Aerobic - classification ; Bacteria, Aerobic - enzymology ; Bacteria, Aerobic - isolation & purification ; Bacteria, Aerobic - physiology ; Bacterial Toxins - metabolism ; Bacterial Toxins - toxicity ; Biodiversity ; Biological and medical sciences ; Cell Survival - drug effects ; Cercopithecus aethiops ; Cytotoxic potential ; Dairy processing environment ; Dairy products ; Dairy Products - microbiology ; Dairying ; Food Handling ; Food industries ; Food Microbiology ; Food spoilage ; Fundamental and applied biological sciences. Psychology ; Geobacillus ; Hot Temperature ; Milk - microbiology ; Milk and cheese industries. Ice creams ; Phylogeny ; RNA, Ribosomal, 16S - genetics ; Spore heat resistance ; Spore-forming bacteria ; Spores, Bacterial - chemistry ; Spores, Bacterial - classification ; Spores, Bacterial - isolation & purification ; Vero Cells</subject><ispartof>International journal of food microbiology, 2013-09, Vol.166 (2), p.270-279</ispartof><rights>2013 Elsevier B.V.</rights><rights>2014 INIST-CNRS</rights><rights>2013 Elsevier B.V. All rights reserved.</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c473t-3c9fd64430f7a3fa271be8ec15478f3e83976f15e070c6cfd11ea83fbeb9b35a3</citedby><cites>FETCH-LOGICAL-c473t-3c9fd64430f7a3fa271be8ec15478f3e83976f15e070c6cfd11ea83fbeb9b35a3</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktohtml>$$Uhttps://dx.doi.org/10.1016/j.ijfoodmicro.2013.07.004$$EHTML$$P50$$Gelsevier$$H</linktohtml><link.rule.ids>314,780,784,3550,27924,27925,45995</link.rule.ids><backlink>$$Uhttp://pascal-francis.inist.fr/vibad/index.php?action=getRecordDetail&idt=27761801$$DView record in Pascal Francis$$Hfree_for_read</backlink><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/23973839$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Lücking, Genia</creatorcontrib><creatorcontrib>Stoeckel, Marina</creatorcontrib><creatorcontrib>Atamer, Zeynep</creatorcontrib><creatorcontrib>Hinrichs, Jörg</creatorcontrib><creatorcontrib>Ehling-Schulz, Monika</creatorcontrib><title>Characterization of aerobic spore-forming bacteria associated with industrial dairy processing environments and product spoilage</title><title>International journal of food microbiology</title><addtitle>Int J Food Microbiol</addtitle><description>Due to changes in the design of industrial food processing and increasing international trade, highly thermoresistant spore-forming bacteria are an emerging problem in food production. Minimally processed foods and products with extended shelf life, such as milk products, are at special risk for contamination and subsequent product damages, but information about origin and food quality related properties of highly heat-resistant spore-formers is still limited. Therefore, the aim of this study was to determine the biodiversity, heat resistance, and food quality and safety affecting characteristics of aerobic spore-formers in the dairy sector. Thus, a comprehensive panel of strains (n=467), which originated from dairy processing environments, raw materials and processed foods, was compiled. The set included isolates associated with recent food spoilage cases and product damages as well as isolates not linked to product spoilage. Identification of the isolates by means of Fourier-transform infrared spectroscopy and molecular methods revealed a large biodiversity of spore-formers, especially among the spoilage associated isolates. These could be assigned to 43 species, representing 11 genera, with Bacillus cereus s.l. and Bacillus licheniformis being predominant. A screening for isolates forming thermoresistant spores (TRS, surviving 100°C, 20min) showed that about one third of the tested spore-formers was heat-resistant, with Bacillus subtilis and Geobacillus stearothermophilus being the prevalent species. Strains producing highly thermoresistant spores (HTRS, surviving 125°C, 30min) were found among mesophilic as well as among thermophilic species. B. subtilis and Bacillus amyloliquefaciens were dominating the group of mesophilic HTRS, while Bacillus smithii and Geobacillus pallidus were dominating the group of thermophilic HTRS. Analysis of spoilage-related enzymes of the TRS isolates showed that mesophilic strains, belonging to the B. subtilis and B. cereus groups, were strongly proteolytic, whereas thermophilic strains displayed generally a low enzymatic activity and thus spoilage potential. Cytotoxicity was only detected in B. cereus, suggesting that the risk of food poisoning by aerobic, thermoresistant spore-formers outside of the B. cereus group is rather low.
•Great biodiversity of aerobic spore-formers associated with dairy product spoilage•Characterization of thermoresistant spores (TRS) from dairy production•Non-dairy ingredients are important TRS contamination sources in dairy production.•Mesophilic TRS show generally a higher spoilage potential than thermophilic TRS.•Spoilage potential of TRS is high, while toxigenic potential is in general low.</description><subject>Animals</subject><subject>Bacillus amyloliquefaciens</subject><subject>Bacillus cereus</subject><subject>Bacillus licheniformis</subject><subject>Bacillus smithii</subject><subject>Bacillus subtilis</subject><subject>Bacteria, Aerobic - classification</subject><subject>Bacteria, Aerobic - enzymology</subject><subject>Bacteria, Aerobic - isolation & purification</subject><subject>Bacteria, Aerobic - physiology</subject><subject>Bacterial Toxins - metabolism</subject><subject>Bacterial Toxins - toxicity</subject><subject>Biodiversity</subject><subject>Biological and medical sciences</subject><subject>Cell Survival - drug effects</subject><subject>Cercopithecus aethiops</subject><subject>Cytotoxic potential</subject><subject>Dairy processing environment</subject><subject>Dairy products</subject><subject>Dairy Products - microbiology</subject><subject>Dairying</subject><subject>Food Handling</subject><subject>Food industries</subject><subject>Food Microbiology</subject><subject>Food spoilage</subject><subject>Fundamental and applied biological sciences. Psychology</subject><subject>Geobacillus</subject><subject>Hot Temperature</subject><subject>Milk - microbiology</subject><subject>Milk and cheese industries. Ice creams</subject><subject>Phylogeny</subject><subject>RNA, Ribosomal, 16S - genetics</subject><subject>Spore heat resistance</subject><subject>Spore-forming bacteria</subject><subject>Spores, Bacterial - chemistry</subject><subject>Spores, Bacterial - classification</subject><subject>Spores, Bacterial - isolation & purification</subject><subject>Vero Cells</subject><issn>0168-1605</issn><issn>1879-3460</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2013</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNqNkc1u1DAUhS0EotOBV0BmgcQmgx0nsbNEo_IjVWIDa-vGvm49SuzBToraFY-Ooxl-dnTlxf3O8bU_Ql5ztuOMd-8OO39wMdrJmxR3NeNix-SOseYJ2XAl-0o0HXtKNoVVFe9Ye0Eucz4wxloh2HNyUYteCiX6Dfm5v4UEZsbkH2D2MdDoKGCKgzc0H2PCysU0-XBDhxMGFHKOxsOMlv7w8y31wS55LpORWvDpnh5TNJjzGsJw51MME4Y5Uwh2ndnFzGu3H-EGX5BnDsaML8_nlnz7cPV1_6m6_vLx8_79dWUaKeZKmN7ZrmkEcxKEg1ryARUa3jZSOYHlMbJzvEUmmemMs5wjKOEGHPpBtCC25O2ptyzwfcE868lng-MIAeOSNW9rJqRqe_V_tKwhOqWYfAQqeN2rtl7R_oQWZzkndPqY_ATpXnOmV636oP_RqletmkldtJbsq_M1yzCh_ZP87bEAb84AZAOjSxCMz385KTuuSuGW7E8clq--85h0Nh6DQesTmlnb6B-xzi-Xi8oL</recordid><startdate>20130902</startdate><enddate>20130902</enddate><creator>Lücking, Genia</creator><creator>Stoeckel, Marina</creator><creator>Atamer, Zeynep</creator><creator>Hinrichs, Jörg</creator><creator>Ehling-Schulz, Monika</creator><general>Elsevier B.V</general><general>Elsevier</general><scope>IQODW</scope><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7X8</scope><scope>7QL</scope><scope>7T7</scope><scope>8FD</scope><scope>C1K</scope><scope>FR3</scope><scope>P64</scope></search><sort><creationdate>20130902</creationdate><title>Characterization of aerobic spore-forming bacteria associated with industrial dairy processing environments and product spoilage</title><author>Lücking, Genia ; Stoeckel, Marina ; Atamer, Zeynep ; Hinrichs, Jörg ; Ehling-Schulz, Monika</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c473t-3c9fd64430f7a3fa271be8ec15478f3e83976f15e070c6cfd11ea83fbeb9b35a3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2013</creationdate><topic>Animals</topic><topic>Bacillus amyloliquefaciens</topic><topic>Bacillus cereus</topic><topic>Bacillus licheniformis</topic><topic>Bacillus smithii</topic><topic>Bacillus subtilis</topic><topic>Bacteria, Aerobic - classification</topic><topic>Bacteria, Aerobic - enzymology</topic><topic>Bacteria, Aerobic - isolation & purification</topic><topic>Bacteria, Aerobic - physiology</topic><topic>Bacterial Toxins - metabolism</topic><topic>Bacterial Toxins - toxicity</topic><topic>Biodiversity</topic><topic>Biological and medical sciences</topic><topic>Cell Survival - drug effects</topic><topic>Cercopithecus aethiops</topic><topic>Cytotoxic potential</topic><topic>Dairy processing environment</topic><topic>Dairy products</topic><topic>Dairy Products - microbiology</topic><topic>Dairying</topic><topic>Food Handling</topic><topic>Food industries</topic><topic>Food Microbiology</topic><topic>Food spoilage</topic><topic>Fundamental and applied biological sciences. Psychology</topic><topic>Geobacillus</topic><topic>Hot Temperature</topic><topic>Milk - microbiology</topic><topic>Milk and cheese industries. Ice creams</topic><topic>Phylogeny</topic><topic>RNA, Ribosomal, 16S - genetics</topic><topic>Spore heat resistance</topic><topic>Spore-forming bacteria</topic><topic>Spores, Bacterial - chemistry</topic><topic>Spores, Bacterial - classification</topic><topic>Spores, Bacterial - isolation & purification</topic><topic>Vero Cells</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Lücking, Genia</creatorcontrib><creatorcontrib>Stoeckel, Marina</creatorcontrib><creatorcontrib>Atamer, Zeynep</creatorcontrib><creatorcontrib>Hinrichs, Jörg</creatorcontrib><creatorcontrib>Ehling-Schulz, Monika</creatorcontrib><collection>Pascal-Francis</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><collection>Bacteriology Abstracts (Microbiology B)</collection><collection>Industrial and Applied Microbiology Abstracts (Microbiology A)</collection><collection>Technology Research Database</collection><collection>Environmental Sciences and Pollution Management</collection><collection>Engineering Research Database</collection><collection>Biotechnology and BioEngineering Abstracts</collection><jtitle>International journal of food microbiology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Lücking, Genia</au><au>Stoeckel, Marina</au><au>Atamer, Zeynep</au><au>Hinrichs, Jörg</au><au>Ehling-Schulz, Monika</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Characterization of aerobic spore-forming bacteria associated with industrial dairy processing environments and product spoilage</atitle><jtitle>International journal of food microbiology</jtitle><addtitle>Int J Food Microbiol</addtitle><date>2013-09-02</date><risdate>2013</risdate><volume>166</volume><issue>2</issue><spage>270</spage><epage>279</epage><pages>270-279</pages><issn>0168-1605</issn><eissn>1879-3460</eissn><coden>IJFMDD</coden><abstract>Due to changes in the design of industrial food processing and increasing international trade, highly thermoresistant spore-forming bacteria are an emerging problem in food production. Minimally processed foods and products with extended shelf life, such as milk products, are at special risk for contamination and subsequent product damages, but information about origin and food quality related properties of highly heat-resistant spore-formers is still limited. Therefore, the aim of this study was to determine the biodiversity, heat resistance, and food quality and safety affecting characteristics of aerobic spore-formers in the dairy sector. Thus, a comprehensive panel of strains (n=467), which originated from dairy processing environments, raw materials and processed foods, was compiled. The set included isolates associated with recent food spoilage cases and product damages as well as isolates not linked to product spoilage. Identification of the isolates by means of Fourier-transform infrared spectroscopy and molecular methods revealed a large biodiversity of spore-formers, especially among the spoilage associated isolates. These could be assigned to 43 species, representing 11 genera, with Bacillus cereus s.l. and Bacillus licheniformis being predominant. A screening for isolates forming thermoresistant spores (TRS, surviving 100°C, 20min) showed that about one third of the tested spore-formers was heat-resistant, with Bacillus subtilis and Geobacillus stearothermophilus being the prevalent species. Strains producing highly thermoresistant spores (HTRS, surviving 125°C, 30min) were found among mesophilic as well as among thermophilic species. B. subtilis and Bacillus amyloliquefaciens were dominating the group of mesophilic HTRS, while Bacillus smithii and Geobacillus pallidus were dominating the group of thermophilic HTRS. Analysis of spoilage-related enzymes of the TRS isolates showed that mesophilic strains, belonging to the B. subtilis and B. cereus groups, were strongly proteolytic, whereas thermophilic strains displayed generally a low enzymatic activity and thus spoilage potential. Cytotoxicity was only detected in B. cereus, suggesting that the risk of food poisoning by aerobic, thermoresistant spore-formers outside of the B. cereus group is rather low.
•Great biodiversity of aerobic spore-formers associated with dairy product spoilage•Characterization of thermoresistant spores (TRS) from dairy production•Non-dairy ingredients are important TRS contamination sources in dairy production.•Mesophilic TRS show generally a higher spoilage potential than thermophilic TRS.•Spoilage potential of TRS is high, while toxigenic potential is in general low.</abstract><cop>Amsterdam</cop><pub>Elsevier B.V</pub><pmid>23973839</pmid><doi>10.1016/j.ijfoodmicro.2013.07.004</doi><tpages>10</tpages></addata></record> |
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subjects | Animals Bacillus amyloliquefaciens Bacillus cereus Bacillus licheniformis Bacillus smithii Bacillus subtilis Bacteria, Aerobic - classification Bacteria, Aerobic - enzymology Bacteria, Aerobic - isolation & purification Bacteria, Aerobic - physiology Bacterial Toxins - metabolism Bacterial Toxins - toxicity Biodiversity Biological and medical sciences Cell Survival - drug effects Cercopithecus aethiops Cytotoxic potential Dairy processing environment Dairy products Dairy Products - microbiology Dairying Food Handling Food industries Food Microbiology Food spoilage Fundamental and applied biological sciences. Psychology Geobacillus Hot Temperature Milk - microbiology Milk and cheese industries. Ice creams Phylogeny RNA, Ribosomal, 16S - genetics Spore heat resistance Spore-forming bacteria Spores, Bacterial - chemistry Spores, Bacterial - classification Spores, Bacterial - isolation & purification Vero Cells |
title | Characterization of aerobic spore-forming bacteria associated with industrial dairy processing environments and product spoilage |
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