Metaproteomic Analysis of Gut Resistome in the Cecal Microbiota of Fattening Pigs Raised without Antibiotics
ABSTRACT Improper use of antibiotics in swine could reduce commensal bacteria and possibly increase pathogen infections via the gut resistome. This study aimed to compare the metaproteomic profiles of the gut resistome and related metabolism in the cecal microbiota of fattening pigs raised under ant...
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| Format: | Article |
| Language: | English |
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American Society for Microbiology
2023-08-01
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| Series: | Microbiology Spectrum |
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| Online Access: | https://journals.asm.org/doi/10.1128/spectrum.02223-23 |
| _version_ | 1797741761283489792 |
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| author | Pamornya Buthasane Sittiruk Roytrakul Narumon Phaonakrop Paiboon Tunsagool Wannapol Buthasane Nutthee Am-in Gunnaporn Suriyaphol |
| author_facet | Pamornya Buthasane Sittiruk Roytrakul Narumon Phaonakrop Paiboon Tunsagool Wannapol Buthasane Nutthee Am-in Gunnaporn Suriyaphol |
| author_sort | Pamornya Buthasane |
| collection | DOAJ |
| description | ABSTRACT Improper use of antibiotics in swine could reduce commensal bacteria and possibly increase pathogen infections via the gut resistome. This study aimed to compare the metaproteomic profiles of the gut resistome and related metabolism in the cecal microbiota of fattening pigs raised under antibiotic-free (ABF) conditions with those of ordinary industrial pigs (controls [CTRL]). The top three relatively abundant microbes in both groups were Escherichia coli, Ruminococcus, and Lactobacillus, followed by Bacteroides and Bifidobacterium. E. coli, Lactobacillus, and Bacteroides were found to be increased in the CTRL group, whereas Ruminococcus and Clostridium were greater in the ABF group. The highest abundances of antibiotic resistance proteins (log2 expression levels [ELs] of >10) were found to be for tetracycline resistance (Tetr) and aminoglycoside resistance (AMGr) proteins found in Bacteroides, with a significant increase in the CTRL group. High Tetr (ELs of 5.32) was found in Ruminococcus in the CTRL group, although pigs in both groups had never received tetracycline, possibly reflecting the influence of environments in farms. In E. coli, AMGr and β-lactamase family proteins were observed in both groups (ELs of 3 to 6), whereas multidrug resistance protein MdtL was significantly expressed in the CTRL group (ELs of around 3). In the ABF group, CRISPR-associated endonucleases Cas1 and Cas9, which function to defend against viruses, were markedly observed in Ruminococcus and Lactobacillus, respectively, with ELs of 8.6 and 4.15, respectively. In conclusion, this study demonstrated that CRISPR-associated endonucleases were markedly observed in the ABF group, whereas higher levels of Tetr, AMGr, and multidrug resistance protein MdtL was markedly observed in dominant bacterial species in the CTRL group. IMPORTANCE In order to control and reduce antibiotic use in animals, the Department of Livestock Development, Thailand, has launched a campaign for antibiotic-free livestock production. The present study has shown for the first time that CRISPR-associated endonucleases Cas1 and Cas9, which function to defend against viruses, were markedly observed in Ruminococcus and Lactobacillus, respectively, in ceca of pigs raised without antibiotics (ABF). The highest abundances of antibiotic resistance proteins were for tetracycline (Tetr) and aminoglycoside resistance (AMGr) proteins found in Bacteroides, with a significant increase in the controls. In E. coli, the microbe with the highest relative abundance, AMGr and β-lactamase family proteins were observed in both groups, whereas multidrug resistance protein MdtL was significantly expressed in the controls. Pigs in both ABF and control groups had never received tetracycline, possibly reflecting the influence of farm environments. We suggest that pigs raised without antibiotics may have more beneficial microorganisms for the gut than pigs raised with antibiotics. |
| first_indexed | 2024-03-12T14:31:19Z |
| format | Article |
| id | doaj.art-5b97a35aa5504b5d9134c97863c6a42e |
| institution | Directory Open Access Journal |
| issn | 2165-0497 |
| language | English |
| last_indexed | 2024-03-12T14:31:19Z |
| publishDate | 2023-08-01 |
| publisher | American Society for Microbiology |
| record_format | Article |
| series | Microbiology Spectrum |
| spelling | doaj.art-5b97a35aa5504b5d9134c97863c6a42e2023-08-17T13:04:14ZengAmerican Society for MicrobiologyMicrobiology Spectrum2165-04972023-08-0111410.1128/spectrum.02223-23Metaproteomic Analysis of Gut Resistome in the Cecal Microbiota of Fattening Pigs Raised without AntibioticsPamornya Buthasane0Sittiruk Roytrakul1Narumon Phaonakrop2Paiboon Tunsagool3Wannapol Buthasane4Nutthee Am-in5Gunnaporn Suriyaphol6Biochemistry Unit, Department of Physiology, Faculty of Veterinary Science, Chulalongkorn University, Bangkok, ThailandFunctional Proteomics Technology Laboratory, Functional Ingredients and Food Innovation Research Group, National Center for Genetic Engineering and Biotechnology, National Science and Technology Development Agency, Pathum Thani, ThailandFunctional Proteomics Technology Laboratory, Functional Ingredients and Food Innovation Research Group, National Center for Genetic Engineering and Biotechnology, National Science and Technology Development Agency, Pathum Thani, ThailandDepartment of Biotechnology, Faculty of Agro-Industry, Kasetsart University, Bangkok, ThailandBiochemistry Unit, Department of Physiology, Faculty of Veterinary Science, Chulalongkorn University, Bangkok, ThailandDepartment of Obstetrics, Gynaecology and Reproduction, Faculty of Veterinary Science, Chulalongkorn University, Bangkok, ThailandBiochemistry Unit, Department of Physiology, Faculty of Veterinary Science, Chulalongkorn University, Bangkok, ThailandABSTRACT Improper use of antibiotics in swine could reduce commensal bacteria and possibly increase pathogen infections via the gut resistome. This study aimed to compare the metaproteomic profiles of the gut resistome and related metabolism in the cecal microbiota of fattening pigs raised under antibiotic-free (ABF) conditions with those of ordinary industrial pigs (controls [CTRL]). The top three relatively abundant microbes in both groups were Escherichia coli, Ruminococcus, and Lactobacillus, followed by Bacteroides and Bifidobacterium. E. coli, Lactobacillus, and Bacteroides were found to be increased in the CTRL group, whereas Ruminococcus and Clostridium were greater in the ABF group. The highest abundances of antibiotic resistance proteins (log2 expression levels [ELs] of >10) were found to be for tetracycline resistance (Tetr) and aminoglycoside resistance (AMGr) proteins found in Bacteroides, with a significant increase in the CTRL group. High Tetr (ELs of 5.32) was found in Ruminococcus in the CTRL group, although pigs in both groups had never received tetracycline, possibly reflecting the influence of environments in farms. In E. coli, AMGr and β-lactamase family proteins were observed in both groups (ELs of 3 to 6), whereas multidrug resistance protein MdtL was significantly expressed in the CTRL group (ELs of around 3). In the ABF group, CRISPR-associated endonucleases Cas1 and Cas9, which function to defend against viruses, were markedly observed in Ruminococcus and Lactobacillus, respectively, with ELs of 8.6 and 4.15, respectively. In conclusion, this study demonstrated that CRISPR-associated endonucleases were markedly observed in the ABF group, whereas higher levels of Tetr, AMGr, and multidrug resistance protein MdtL was markedly observed in dominant bacterial species in the CTRL group. IMPORTANCE In order to control and reduce antibiotic use in animals, the Department of Livestock Development, Thailand, has launched a campaign for antibiotic-free livestock production. The present study has shown for the first time that CRISPR-associated endonucleases Cas1 and Cas9, which function to defend against viruses, were markedly observed in Ruminococcus and Lactobacillus, respectively, in ceca of pigs raised without antibiotics (ABF). The highest abundances of antibiotic resistance proteins were for tetracycline (Tetr) and aminoglycoside resistance (AMGr) proteins found in Bacteroides, with a significant increase in the controls. In E. coli, the microbe with the highest relative abundance, AMGr and β-lactamase family proteins were observed in both groups, whereas multidrug resistance protein MdtL was significantly expressed in the controls. Pigs in both ABF and control groups had never received tetracycline, possibly reflecting the influence of farm environments. We suggest that pigs raised without antibiotics may have more beneficial microorganisms for the gut than pigs raised with antibiotics.https://journals.asm.org/doi/10.1128/spectrum.02223-23antibiotic freececumgut microbiotagut resistomemetaproteomicspig |
| spellingShingle | Pamornya Buthasane Sittiruk Roytrakul Narumon Phaonakrop Paiboon Tunsagool Wannapol Buthasane Nutthee Am-in Gunnaporn Suriyaphol Metaproteomic Analysis of Gut Resistome in the Cecal Microbiota of Fattening Pigs Raised without Antibiotics Microbiology Spectrum antibiotic free cecum gut microbiota gut resistome metaproteomics pig |
| title | Metaproteomic Analysis of Gut Resistome in the Cecal Microbiota of Fattening Pigs Raised without Antibiotics |
| title_full | Metaproteomic Analysis of Gut Resistome in the Cecal Microbiota of Fattening Pigs Raised without Antibiotics |
| title_fullStr | Metaproteomic Analysis of Gut Resistome in the Cecal Microbiota of Fattening Pigs Raised without Antibiotics |
| title_full_unstemmed | Metaproteomic Analysis of Gut Resistome in the Cecal Microbiota of Fattening Pigs Raised without Antibiotics |
| title_short | Metaproteomic Analysis of Gut Resistome in the Cecal Microbiota of Fattening Pigs Raised without Antibiotics |
| title_sort | metaproteomic analysis of gut resistome in the cecal microbiota of fattening pigs raised without antibiotics |
| topic | antibiotic free cecum gut microbiota gut resistome metaproteomics pig |
| url | https://journals.asm.org/doi/10.1128/spectrum.02223-23 |
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