Microbial colonization and resistome dynamics in food processing environments of a newly opened pork cutting industry during 1.5 years of activity
Abstract Background The microorganisms that inhabit food processing environments (FPE) can strongly influence the associated food quality and safety. In particular, the possibility that FPE may act as a reservoir of antibiotic-resistant microorganisms, and a hotspot for the transmission of antibioti...
| Main Authors: | , , , , , , , , , , , , , , , |
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| Format: | Article |
| Language: | English |
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BMC
2021-10-01
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| Series: | Microbiome |
| Subjects: | |
| Online Access: | https://doi.org/10.1186/s40168-021-01131-9 |
| _version_ | 1819009086073602048 |
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| author | José F. Cobo-Díaz Adrián Alvarez-Molina Elena A. Alexa Calum J. Walsh Oscar Mencía-Ares Paula Puente-Gómez Eleni Likotrafiti Paula Fernández-Gómez Bernardo Prieto Fiona Crispie Lorena Ruiz Montserrat González-Raurich Mercedes López Miguel Prieto Paul Cotter Avelino Alvarez-Ordóñez |
| author_facet | José F. Cobo-Díaz Adrián Alvarez-Molina Elena A. Alexa Calum J. Walsh Oscar Mencía-Ares Paula Puente-Gómez Eleni Likotrafiti Paula Fernández-Gómez Bernardo Prieto Fiona Crispie Lorena Ruiz Montserrat González-Raurich Mercedes López Miguel Prieto Paul Cotter Avelino Alvarez-Ordóñez |
| author_sort | José F. Cobo-Díaz |
| collection | DOAJ |
| description | Abstract Background The microorganisms that inhabit food processing environments (FPE) can strongly influence the associated food quality and safety. In particular, the possibility that FPE may act as a reservoir of antibiotic-resistant microorganisms, and a hotspot for the transmission of antibiotic resistance genes (ARGs) is a concern in meat processing plants. Here, we monitor microbial succession and resistome dynamics relating to FPE through a detailed analysis of a newly opened pork cutting plant over 1.5 years of activity. Results We identified a relatively restricted principal microbiota dominated by Pseudomonas during the first 2 months, while a higher taxonomic diversity, an increased representation of other taxa (e.g., Acinetobacter, Psychrobacter), and a certain degree of microbiome specialization on different surfaces was recorded later on. An increase in total abundance, alpha diversity, and β-dispersion of ARGs, which were predominantly assigned to Acinetobacter and associated with resistance to certain antimicrobials frequently used on pig farms of the region, was detected over time. Moreover, a sharp increase in the occurrence of extended-spectrum β-lactamase-producing Enterobacteriaceae and vancomycin-resistant Enterococcaceae was observed when cutting activities started. ARGs associated with resistance to β-lactams, tetracyclines, aminoglycosides, and sulphonamides frequently co-occurred, and mobile genetic elements (i.e., plasmids, integrons) and lateral gene transfer events were mainly detected at the later sampling times in drains. Conclusions The observations made suggest that pig carcasses were a source of resistant bacteria that then colonized FPE and that drains, together with some food-contact surfaces, such as equipment and table surfaces, represented a reservoir for the spread of ARGs in the meat processing facility. Video Abstract |
| first_indexed | 2024-12-21T00:50:46Z |
| format | Article |
| id | doaj.art-415ec0cec96549a3ae525f9b47a45fd8 |
| institution | Directory Open Access Journal |
| issn | 2049-2618 |
| language | English |
| last_indexed | 2024-12-21T00:50:46Z |
| publishDate | 2021-10-01 |
| publisher | BMC |
| record_format | Article |
| series | Microbiome |
| spelling | doaj.art-415ec0cec96549a3ae525f9b47a45fd82022-12-21T19:21:24ZengBMCMicrobiome2049-26182021-10-019111910.1186/s40168-021-01131-9Microbial colonization and resistome dynamics in food processing environments of a newly opened pork cutting industry during 1.5 years of activityJosé F. Cobo-Díaz0Adrián Alvarez-Molina1Elena A. Alexa2Calum J. Walsh3Oscar Mencía-Ares4Paula Puente-Gómez5Eleni Likotrafiti6Paula Fernández-Gómez7Bernardo Prieto8Fiona Crispie9Lorena Ruiz10Montserrat González-Raurich11Mercedes López12Miguel Prieto13Paul Cotter14Avelino Alvarez-Ordóñez15Department of Food Hygiene and Technology, Universidad de LeónDepartment of Food Hygiene and Technology, Universidad de LeónDepartment of Food Hygiene and Technology, Universidad de LeónTeagasc Food Research Centre, FermoyDepartment of Animal Health, Universidad de LeónDepartment of Food Hygiene and Technology, Universidad de LeónDepartment of Food Science & Technology, International Hellenic UniversityDepartment of Food Hygiene and Technology, Universidad de LeónDepartment of Food Hygiene and Technology, Universidad de LeónTeagasc Food Research Centre, FermoyDairy Research Institute, Spanish National Research Council, Instituto de Productos Lácteos de Asturias-CSICDepartment of Food Hygiene and Technology, Universidad de LeónDepartment of Food Hygiene and Technology, Universidad de LeónDepartment of Food Hygiene and Technology, Universidad de LeónTeagasc Food Research Centre, FermoyDepartment of Food Hygiene and Technology, Universidad de LeónAbstract Background The microorganisms that inhabit food processing environments (FPE) can strongly influence the associated food quality and safety. In particular, the possibility that FPE may act as a reservoir of antibiotic-resistant microorganisms, and a hotspot for the transmission of antibiotic resistance genes (ARGs) is a concern in meat processing plants. Here, we monitor microbial succession and resistome dynamics relating to FPE through a detailed analysis of a newly opened pork cutting plant over 1.5 years of activity. Results We identified a relatively restricted principal microbiota dominated by Pseudomonas during the first 2 months, while a higher taxonomic diversity, an increased representation of other taxa (e.g., Acinetobacter, Psychrobacter), and a certain degree of microbiome specialization on different surfaces was recorded later on. An increase in total abundance, alpha diversity, and β-dispersion of ARGs, which were predominantly assigned to Acinetobacter and associated with resistance to certain antimicrobials frequently used on pig farms of the region, was detected over time. Moreover, a sharp increase in the occurrence of extended-spectrum β-lactamase-producing Enterobacteriaceae and vancomycin-resistant Enterococcaceae was observed when cutting activities started. ARGs associated with resistance to β-lactams, tetracyclines, aminoglycosides, and sulphonamides frequently co-occurred, and mobile genetic elements (i.e., plasmids, integrons) and lateral gene transfer events were mainly detected at the later sampling times in drains. Conclusions The observations made suggest that pig carcasses were a source of resistant bacteria that then colonized FPE and that drains, together with some food-contact surfaces, such as equipment and table surfaces, represented a reservoir for the spread of ARGs in the meat processing facility. Video Abstracthttps://doi.org/10.1186/s40168-021-01131-9MetagenomicsFood processing environmentsAntimicrobial resistanceMicrobial ecology |
| spellingShingle | José F. Cobo-Díaz Adrián Alvarez-Molina Elena A. Alexa Calum J. Walsh Oscar Mencía-Ares Paula Puente-Gómez Eleni Likotrafiti Paula Fernández-Gómez Bernardo Prieto Fiona Crispie Lorena Ruiz Montserrat González-Raurich Mercedes López Miguel Prieto Paul Cotter Avelino Alvarez-Ordóñez Microbial colonization and resistome dynamics in food processing environments of a newly opened pork cutting industry during 1.5 years of activity Microbiome Metagenomics Food processing environments Antimicrobial resistance Microbial ecology |
| title | Microbial colonization and resistome dynamics in food processing environments of a newly opened pork cutting industry during 1.5 years of activity |
| title_full | Microbial colonization and resistome dynamics in food processing environments of a newly opened pork cutting industry during 1.5 years of activity |
| title_fullStr | Microbial colonization and resistome dynamics in food processing environments of a newly opened pork cutting industry during 1.5 years of activity |
| title_full_unstemmed | Microbial colonization and resistome dynamics in food processing environments of a newly opened pork cutting industry during 1.5 years of activity |
| title_short | Microbial colonization and resistome dynamics in food processing environments of a newly opened pork cutting industry during 1.5 years of activity |
| title_sort | microbial colonization and resistome dynamics in food processing environments of a newly opened pork cutting industry during 1 5 years of activity |
| topic | Metagenomics Food processing environments Antimicrobial resistance Microbial ecology |
| url | https://doi.org/10.1186/s40168-021-01131-9 |
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