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Lactobacillus ruminis strains cluster according to their mammalian gut source

BACKGROUND: Lactobacillus ruminis is a motile Lactobacillus that is autochthonous to the human gut, and which may also be isolated from other mammals. Detailed characterization of L. ruminis has previously been restricted to strains of human and bovine origin. We therefore sought to expand our bio-b...

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Autores principales: O’ Donnell, Michelle M, Harris, Hugh Michael B, Lynch, Denise B, Ross, Reynolds Paul, O’Toole, Paul W
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2015
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4393605/
https://www.ncbi.nlm.nih.gov/pubmed/25879663
http://dx.doi.org/10.1186/s12866-015-0403-y
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author O’ Donnell, Michelle M
Harris, Hugh Michael B
Lynch, Denise B
Ross, Reynolds Paul
O’Toole, Paul W
author_facet O’ Donnell, Michelle M
Harris, Hugh Michael B
Lynch, Denise B
Ross, Reynolds Paul
O’Toole, Paul W
author_sort O’ Donnell, Michelle M
collection PubMed
description BACKGROUND: Lactobacillus ruminis is a motile Lactobacillus that is autochthonous to the human gut, and which may also be isolated from other mammals. Detailed characterization of L. ruminis has previously been restricted to strains of human and bovine origin. We therefore sought to expand our bio-bank of strains to identify and characterise isolates of porcine and equine origin by comparative genomics. RESULTS: We isolated five strains from the faeces of horses and two strains from pigs, and compared their motility, biochemistry and genetic relatedness to six human isolates and three bovine isolates including the type strain 27780(T). Multilocus sequence typing analysis based on concatenated sequence data for six individual loci separated the 16 L. ruminis strains into three clades concordant with human, bovine or porcine, and equine sources. Sequencing the genomes of four additional strains of human, bovine, equine and porcine origin revealed a high level of genome synteny, independent of the source animal. Analysis of carbohydrate utilization, stress survival and technological robustness in a combined panel of sixteen L. ruminis isolates identified strains with optimal survival characteristics suitable for future investigation as candidate probiotics. Under laboratory conditions, six human isolates of L. ruminis tested were aflagellate and non-motile, whereas all 10 strains of bovine, equine and porcine origin were motile. Interestingly the equine and porcine strains were hyper-flagellated compared to bovine isolates, and this hyper-flagellate phenotype correlated with the ability to swarm on solid medium containing up to 1.8% agar. Analysis by RNA sequencing and qRT-PCR identified genes for the biosynthesis of flagella, genes for carbohydrate metabolism and genes of unknown function that were differentially expressed in swarming cells of an equine isolate of L. ruminis. CONCLUSIONS: We suggest that Lactobacillus ruminis isolates have potential to be used in the functional food industry. We have also identified a MLST scheme able to distinguish between strains of L. ruminis of different origin. Genes for non-digestible oligosaccharide metabolism were identified with a putative role in swarming behaviour. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12866-015-0403-y) contains supplementary material, which is available to authorized users.
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spelling pubmed-43936052015-04-12 Lactobacillus ruminis strains cluster according to their mammalian gut source O’ Donnell, Michelle M Harris, Hugh Michael B Lynch, Denise B Ross, Reynolds Paul O’Toole, Paul W BMC Microbiol Research Article BACKGROUND: Lactobacillus ruminis is a motile Lactobacillus that is autochthonous to the human gut, and which may also be isolated from other mammals. Detailed characterization of L. ruminis has previously been restricted to strains of human and bovine origin. We therefore sought to expand our bio-bank of strains to identify and characterise isolates of porcine and equine origin by comparative genomics. RESULTS: We isolated five strains from the faeces of horses and two strains from pigs, and compared their motility, biochemistry and genetic relatedness to six human isolates and three bovine isolates including the type strain 27780(T). Multilocus sequence typing analysis based on concatenated sequence data for six individual loci separated the 16 L. ruminis strains into three clades concordant with human, bovine or porcine, and equine sources. Sequencing the genomes of four additional strains of human, bovine, equine and porcine origin revealed a high level of genome synteny, independent of the source animal. Analysis of carbohydrate utilization, stress survival and technological robustness in a combined panel of sixteen L. ruminis isolates identified strains with optimal survival characteristics suitable for future investigation as candidate probiotics. Under laboratory conditions, six human isolates of L. ruminis tested were aflagellate and non-motile, whereas all 10 strains of bovine, equine and porcine origin were motile. Interestingly the equine and porcine strains were hyper-flagellated compared to bovine isolates, and this hyper-flagellate phenotype correlated with the ability to swarm on solid medium containing up to 1.8% agar. Analysis by RNA sequencing and qRT-PCR identified genes for the biosynthesis of flagella, genes for carbohydrate metabolism and genes of unknown function that were differentially expressed in swarming cells of an equine isolate of L. ruminis. CONCLUSIONS: We suggest that Lactobacillus ruminis isolates have potential to be used in the functional food industry. We have also identified a MLST scheme able to distinguish between strains of L. ruminis of different origin. Genes for non-digestible oligosaccharide metabolism were identified with a putative role in swarming behaviour. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12866-015-0403-y) contains supplementary material, which is available to authorized users. BioMed Central 2015-04-01 /pmc/articles/PMC4393605/ /pubmed/25879663 http://dx.doi.org/10.1186/s12866-015-0403-y Text en © O' Donnell et al.; licensee BioMed Central. 2015 This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly credited. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
spellingShingle Research Article
O’ Donnell, Michelle M
Harris, Hugh Michael B
Lynch, Denise B
Ross, Reynolds Paul
O’Toole, Paul W
Lactobacillus ruminis strains cluster according to their mammalian gut source
title Lactobacillus ruminis strains cluster according to their mammalian gut source
title_full Lactobacillus ruminis strains cluster according to their mammalian gut source
title_fullStr Lactobacillus ruminis strains cluster according to their mammalian gut source
title_full_unstemmed Lactobacillus ruminis strains cluster according to their mammalian gut source
title_short Lactobacillus ruminis strains cluster according to their mammalian gut source
title_sort lactobacillus ruminis strains cluster according to their mammalian gut source
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4393605/
https://www.ncbi.nlm.nih.gov/pubmed/25879663
http://dx.doi.org/10.1186/s12866-015-0403-y
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