Substantial Extracellular Metabolic Differences Found Between Phylogenetically Closely Related Probiotic and Pathogenic Strains of Escherichia coli
Since its first isolation a century ago, the gut inhabitant Escherichia coli strain Nissle 1917 has been shown to have probiotic activities; however, it is yet not fully elucidated which differential factors play key roles in its beneficial interactions with the host. To date, no metabolomics studie...
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| Format: | Article |
| Language: | English |
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Frontiers Media S.A.
2019-02-01
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| Series: | Frontiers in Microbiology |
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| Online Access: | https://www.frontiersin.org/article/10.3389/fmicb.2019.00252/full |
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| author | Justin J. J. van der Hooft Robert J. Goldstone Susan Harris Karl E. V. Burgess David G. E. Smith |
| author_facet | Justin J. J. van der Hooft Robert J. Goldstone Susan Harris Karl E. V. Burgess David G. E. Smith |
| author_sort | Justin J. J. van der Hooft |
| collection | DOAJ |
| description | Since its first isolation a century ago, the gut inhabitant Escherichia coli strain Nissle 1917 has been shown to have probiotic activities; however, it is yet not fully elucidated which differential factors play key roles in its beneficial interactions with the host. To date, no metabolomics studies have been reported investigating the potential role of small molecules in functional strain differentiation of Nissle from its genetically close neighbors. Here, we present results of liquid chromatography coupled to high-resolution mass spectrometry characterization of extracellular metabolomes of E. coli strains as a proxy of their bioactivity potential. We found that phylogroup B2 strains exported a more diverse arsenal of metabolites than strains of other phylogroups. Zooming into the phylogroup B2 metabolome identified consistent substantial differences between metabolic output of E. coli Nissle and other strains, particularly in metabolites associated to the Argimine biosynthesis pathway. Nissle was found to release higher levels of Ornithine and Citrulline whilst depleting greater amounts of Arginine from the medium. Moreover, a novel Nissle-specific metabolite not reported before in bacteria, 5-(Carbamoylamino)-2-hydroxypentanoic acid (Citrulline/Arginic Acid related) was observed. Finally, Nissle, CFT073 and NCTC12241/ATCC25922 shared the excretion of N5-Acetylornithine, whereas other strains released N2-Acetylornithine or no N-Acetylornithine at all. Thus, we found substantial metabolic differences in phylogenetically very similar E. coli strains, an observation which suggests that it is justified to further investigate roles of small molecules as potential modulators of the gut environment by probiotic, commensal, and pathogenic strains, including E. coli Nissle 1917. |
| first_indexed | 2024-12-12T19:10:18Z |
| format | Article |
| id | doaj.art-3c07f394ecef40fda06c5cd2e8b55fa5 |
| institution | Directory Open Access Journal |
| issn | 1664-302X |
| language | English |
| last_indexed | 2024-12-12T19:10:18Z |
| publishDate | 2019-02-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Microbiology |
| spelling | doaj.art-3c07f394ecef40fda06c5cd2e8b55fa52022-12-22T00:14:52ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2019-02-011010.3389/fmicb.2019.00252425012Substantial Extracellular Metabolic Differences Found Between Phylogenetically Closely Related Probiotic and Pathogenic Strains of Escherichia coliJustin J. J. van der Hooft0Robert J. Goldstone1Susan Harris2Karl E. V. Burgess3David G. E. Smith4Bioinformatics Group, Wageningen University, Wageningen, NetherlandsThe Francis Crick Institute, London, United KingdomInstitute of Biological Chemistry, Biophysics and Bioengineering, Heriot-Watt University, Edinburgh, United KingdomGlasgow Polyomics, College of Medical, Veterinary and Life Sciences, University of Glasgow, Glasgow, United KingdomInstitute of Biological Chemistry, Biophysics and Bioengineering, Heriot-Watt University, Edinburgh, United KingdomSince its first isolation a century ago, the gut inhabitant Escherichia coli strain Nissle 1917 has been shown to have probiotic activities; however, it is yet not fully elucidated which differential factors play key roles in its beneficial interactions with the host. To date, no metabolomics studies have been reported investigating the potential role of small molecules in functional strain differentiation of Nissle from its genetically close neighbors. Here, we present results of liquid chromatography coupled to high-resolution mass spectrometry characterization of extracellular metabolomes of E. coli strains as a proxy of their bioactivity potential. We found that phylogroup B2 strains exported a more diverse arsenal of metabolites than strains of other phylogroups. Zooming into the phylogroup B2 metabolome identified consistent substantial differences between metabolic output of E. coli Nissle and other strains, particularly in metabolites associated to the Argimine biosynthesis pathway. Nissle was found to release higher levels of Ornithine and Citrulline whilst depleting greater amounts of Arginine from the medium. Moreover, a novel Nissle-specific metabolite not reported before in bacteria, 5-(Carbamoylamino)-2-hydroxypentanoic acid (Citrulline/Arginic Acid related) was observed. Finally, Nissle, CFT073 and NCTC12241/ATCC25922 shared the excretion of N5-Acetylornithine, whereas other strains released N2-Acetylornithine or no N-Acetylornithine at all. Thus, we found substantial metabolic differences in phylogenetically very similar E. coli strains, an observation which suggests that it is justified to further investigate roles of small molecules as potential modulators of the gut environment by probiotic, commensal, and pathogenic strains, including E. coli Nissle 1917.https://www.frontiersin.org/article/10.3389/fmicb.2019.00252/fullEscherichia coliNissle 1917probioticpathogenicextracellular metabolomemass spectrometry |
| spellingShingle | Justin J. J. van der Hooft Robert J. Goldstone Susan Harris Karl E. V. Burgess David G. E. Smith Substantial Extracellular Metabolic Differences Found Between Phylogenetically Closely Related Probiotic and Pathogenic Strains of Escherichia coli Frontiers in Microbiology Escherichia coli Nissle 1917 probiotic pathogenic extracellular metabolome mass spectrometry |
| title | Substantial Extracellular Metabolic Differences Found Between Phylogenetically Closely Related Probiotic and Pathogenic Strains of Escherichia coli |
| title_full | Substantial Extracellular Metabolic Differences Found Between Phylogenetically Closely Related Probiotic and Pathogenic Strains of Escherichia coli |
| title_fullStr | Substantial Extracellular Metabolic Differences Found Between Phylogenetically Closely Related Probiotic and Pathogenic Strains of Escherichia coli |
| title_full_unstemmed | Substantial Extracellular Metabolic Differences Found Between Phylogenetically Closely Related Probiotic and Pathogenic Strains of Escherichia coli |
| title_short | Substantial Extracellular Metabolic Differences Found Between Phylogenetically Closely Related Probiotic and Pathogenic Strains of Escherichia coli |
| title_sort | substantial extracellular metabolic differences found between phylogenetically closely related probiotic and pathogenic strains of escherichia coli |
| topic | Escherichia coli Nissle 1917 probiotic pathogenic extracellular metabolome mass spectrometry |
| url | https://www.frontiersin.org/article/10.3389/fmicb.2019.00252/full |
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