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Specific inhibition of Streptococcus bovis by endolysin LyJH307 supplementation shifts the rumen microbiota and metabolic pathways related to carbohydrate metabolism

BACKGROUND: Endolysins, the bacteriophage-originated peptidoglycan hydrolases, are a promising replacement for antibiotics due to immediate lytic activity and no antibiotic resistance. The objectives of this study were to investigate the lytic activity of endolysin LyJH307 against S. bovis and to ex...

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Autores principales: Kim, Hanbeen, Park, Tansol, Kwon, Inhyuk, Seo, Jakyeom
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8335910/
https://www.ncbi.nlm.nih.gov/pubmed/34344466
http://dx.doi.org/10.1186/s40104-021-00614-x
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author Kim, Hanbeen
Park, Tansol
Kwon, Inhyuk
Seo, Jakyeom
author_facet Kim, Hanbeen
Park, Tansol
Kwon, Inhyuk
Seo, Jakyeom
author_sort Kim, Hanbeen
collection PubMed
description BACKGROUND: Endolysins, the bacteriophage-originated peptidoglycan hydrolases, are a promising replacement for antibiotics due to immediate lytic activity and no antibiotic resistance. The objectives of this study were to investigate the lytic activity of endolysin LyJH307 against S. bovis and to explore changes in rumen fermentation and microbiota in an in vitro system. Two treatments were used: 1) control, corn grain without LyJH307; and 2) LyJH307, corn grain with LyJH307 (4 U/mL). An in vitro fermentation experiment was performed using mixture of rumen fluid collected from two cannulated Holstein steers (450 ± 30 kg) and artificial saliva buffer mixed as 1:3 ratio for 12 h incubation time. In vitro dry matter digestibility, pH, volatile fatty acids, and lactate concentration were estimated at 12 h, and the gas production was measured at 6, 9, and 12 h. The rumen bacterial community was analyzed using 16S rRNA amplicon sequencing. RESULTS: LyJH307 supplementation at 6 h incubation markedly decreased the absolute abundance of S. bovis (approximately 70% compared to control, P = 0.0289) and increased ruminal pH (P = 0.0335) at the 12 h incubation. The acetate proportion (P = 0.0362) was significantly increased after LyJH307 addition, whereas propionate (P = 0.0379) was decreased. LyJH307 supplementation increased D-lactate (P = 0.0340) without any change in L-lactate concentration (P > 0.10). There were no significant differences in Shannon’s index, Simpson’s index, Chao1 estimates, and evenness (P > 0.10). Based on Bray-Curtis dissimilarity matrices, the LyJH307 affected the overall shift in microbiota (P = 0.097). LyJH307 supplementation induced an increase of 11 genera containing Lachnoclostridium, WCHB1–41, unclassified genus Selenomonadaceae, Paraprevotella, vadinBE97, Ruminococcus gauvreauii group, Lactobacillus, Anaerorhabdus furcosa group, Victivallaceae, Desulfuromonadaceae, and Sediminispirochaeta. The predicted functional features represented by the Kyoto Encyclopedia of Genes and Genomes pathways were changed by LyJH307 toward a decrease of carbohydrate metabolism. CONCLUSIONS: LyJH307 caused a reduction of S. bovis and an increase of pH with shifts in minor microbiota and its metabolic pathways related to carbohydrate metabolism. This study provides the first insight into the availability of endolysin as a specific modulator for rumen and shows the possibility of endolysin degradation by rumen microbiota. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s40104-021-00614-x.
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spelling pubmed-83359102021-08-04 Specific inhibition of Streptococcus bovis by endolysin LyJH307 supplementation shifts the rumen microbiota and metabolic pathways related to carbohydrate metabolism Kim, Hanbeen Park, Tansol Kwon, Inhyuk Seo, Jakyeom J Anim Sci Biotechnol Research BACKGROUND: Endolysins, the bacteriophage-originated peptidoglycan hydrolases, are a promising replacement for antibiotics due to immediate lytic activity and no antibiotic resistance. The objectives of this study were to investigate the lytic activity of endolysin LyJH307 against S. bovis and to explore changes in rumen fermentation and microbiota in an in vitro system. Two treatments were used: 1) control, corn grain without LyJH307; and 2) LyJH307, corn grain with LyJH307 (4 U/mL). An in vitro fermentation experiment was performed using mixture of rumen fluid collected from two cannulated Holstein steers (450 ± 30 kg) and artificial saliva buffer mixed as 1:3 ratio for 12 h incubation time. In vitro dry matter digestibility, pH, volatile fatty acids, and lactate concentration were estimated at 12 h, and the gas production was measured at 6, 9, and 12 h. The rumen bacterial community was analyzed using 16S rRNA amplicon sequencing. RESULTS: LyJH307 supplementation at 6 h incubation markedly decreased the absolute abundance of S. bovis (approximately 70% compared to control, P = 0.0289) and increased ruminal pH (P = 0.0335) at the 12 h incubation. The acetate proportion (P = 0.0362) was significantly increased after LyJH307 addition, whereas propionate (P = 0.0379) was decreased. LyJH307 supplementation increased D-lactate (P = 0.0340) without any change in L-lactate concentration (P > 0.10). There were no significant differences in Shannon’s index, Simpson’s index, Chao1 estimates, and evenness (P > 0.10). Based on Bray-Curtis dissimilarity matrices, the LyJH307 affected the overall shift in microbiota (P = 0.097). LyJH307 supplementation induced an increase of 11 genera containing Lachnoclostridium, WCHB1–41, unclassified genus Selenomonadaceae, Paraprevotella, vadinBE97, Ruminococcus gauvreauii group, Lactobacillus, Anaerorhabdus furcosa group, Victivallaceae, Desulfuromonadaceae, and Sediminispirochaeta. The predicted functional features represented by the Kyoto Encyclopedia of Genes and Genomes pathways were changed by LyJH307 toward a decrease of carbohydrate metabolism. CONCLUSIONS: LyJH307 caused a reduction of S. bovis and an increase of pH with shifts in minor microbiota and its metabolic pathways related to carbohydrate metabolism. This study provides the first insight into the availability of endolysin as a specific modulator for rumen and shows the possibility of endolysin degradation by rumen microbiota. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s40104-021-00614-x. BioMed Central 2021-08-04 /pmc/articles/PMC8335910/ /pubmed/34344466 http://dx.doi.org/10.1186/s40104-021-00614-x Text en © The Author(s) 2021 https://creativecommons.org/licenses/by/4.0/Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research
Kim, Hanbeen
Park, Tansol
Kwon, Inhyuk
Seo, Jakyeom
Specific inhibition of Streptococcus bovis by endolysin LyJH307 supplementation shifts the rumen microbiota and metabolic pathways related to carbohydrate metabolism
title Specific inhibition of Streptococcus bovis by endolysin LyJH307 supplementation shifts the rumen microbiota and metabolic pathways related to carbohydrate metabolism
title_full Specific inhibition of Streptococcus bovis by endolysin LyJH307 supplementation shifts the rumen microbiota and metabolic pathways related to carbohydrate metabolism
title_fullStr Specific inhibition of Streptococcus bovis by endolysin LyJH307 supplementation shifts the rumen microbiota and metabolic pathways related to carbohydrate metabolism
title_full_unstemmed Specific inhibition of Streptococcus bovis by endolysin LyJH307 supplementation shifts the rumen microbiota and metabolic pathways related to carbohydrate metabolism
title_short Specific inhibition of Streptococcus bovis by endolysin LyJH307 supplementation shifts the rumen microbiota and metabolic pathways related to carbohydrate metabolism
title_sort specific inhibition of streptococcus bovis by endolysin lyjh307 supplementation shifts the rumen microbiota and metabolic pathways related to carbohydrate metabolism
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8335910/
https://www.ncbi.nlm.nih.gov/pubmed/34344466
http://dx.doi.org/10.1186/s40104-021-00614-x
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