Calf Diarrhea Caused by Prolonged Expansion of Autochthonous Gut <italic toggle="yes">Enterobacteriaceae</italic> and Their Lytic Bacteriophages

ABSTRACT Neonatal calf diarrhea is a common disease leading to a major economic loss for cattle producers worldwide. Several infectious and noninfectious factors are implicated in calf diarrhea, but disease control remains problematic because of the multifactorial etiology of the disease. Here, we c...

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Autores principales:	Tae Woong Whon, Hyun Sik Kim, Na-Ri Shin, Hojun Sung, Min-Soo Kim, Joon Yong Kim, Woorim Kang, Pil Soo Kim, Dong-Wook Hyun, Hoon Je Seong, Woo Jun Sul, Seong Woon Roh, Jin-Woo Bae
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2021
Materias:	calf diarrhea gut microbiome dysbiosis Enterobacteriaceae bacteriophages Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/d6f735f1fa424644a9af3236f2494936
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spelling	oai:doaj.org-article:d6f735f1fa424644a9af3236f24949362021-12-02T19:36:39ZCalf Diarrhea Caused by Prolonged Expansion of Autochthonous Gut <italic toggle="yes">Enterobacteriaceae</italic> and Their Lytic Bacteriophages10.1128/mSystems.00816-202379-5077https://doaj.org/article/d6f735f1fa424644a9af3236f24949362021-04-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSystems.00816-20https://doaj.org/toc/2379-5077ABSTRACT Neonatal calf diarrhea is a common disease leading to a major economic loss for cattle producers worldwide. Several infectious and noninfectious factors are implicated in calf diarrhea, but disease control remains problematic because of the multifactorial etiology of the disease. Here, we conducted diagnostic multiplex PCR assay and meta-omics analysis (16S rRNA gene-based metataxonomics and untargeted transcriptional profiling) of rectal content of normal and diarrheic beef calves (n = 111). In the diarrheic calf gut, we detected both microbial compositional dysbiosis (i.e., increased abundances of the family Enterobacteriaceae members and their lytic bacteriophages) and functional dysbiosis (i.e., elevated levels of aerobic respiration and virulence potential). The calf diarrheic transcriptome mirrored the gene expression of the bovine host and was enriched in cellular pathways of sulfur metabolism, innate immunity, and gut motility. We then isolated 12 nontoxigenic Enterobacteriaceae strains from the gut of diarrheic calves. Feeding a strain mixture to preweaning mice resulted in a significantly higher level of fecal moisture content, with decreased body weight gain and shortened colon length. The presented findings suggest that gut inflammation followed by a prolonged expansion of nontoxigenic autochthonous Enterobacteriaceae contributes to the onset of diarrhea in preweaning animals. IMPORTANCE Calf diarrhea is the leading cause of death of neonatal calves worldwide. Several infectious and noninfectious factors are implicated in calf diarrhea, but disease control remains problematic because of the multifactorial etiology of the disease. The major finding of the current study centers around the observation of microbial compositional and functional dysbiosis in rectal samples from diarrheic calves. These results highlight the notion that gut inflammation followed by a prolonged expansion of autochthonous Enterobacteriaceae contributes to the onset of calf diarrhea. Moreover, this condition possibly potentiates the risk of invasion of notorious enteric pathogens, including Salmonella spp., and the emergence of inflammation-resistant (or antibiotic-resistant) microbiota via active horizontal gene transfer mediated by lytic bacteriophages.Tae Woong WhonHyun Sik KimNa-Ri ShinHojun SungMin-Soo KimJoon Yong KimWoorim KangPil Soo KimDong-Wook HyunHoon Je SeongWoo Jun SulSeong Woon RohJin-Woo BaeAmerican Society for Microbiologyarticlecalf diarrheagut microbiomedysbiosisEnterobacteriaceaebacteriophagesMicrobiologyQR1-502ENmSystems, Vol 6, Iss 2 (2021)
institution	DOAJ
collection	DOAJ
language	EN
topic	calf diarrhea gut microbiome dysbiosis Enterobacteriaceae bacteriophages Microbiology QR1-502
spellingShingle	calf diarrhea gut microbiome dysbiosis Enterobacteriaceae bacteriophages Microbiology QR1-502 Tae Woong Whon Hyun Sik Kim Na-Ri Shin Hojun Sung Min-Soo Kim Joon Yong Kim Woorim Kang Pil Soo Kim Dong-Wook Hyun Hoon Je Seong Woo Jun Sul Seong Woon Roh Jin-Woo Bae Calf Diarrhea Caused by Prolonged Expansion of Autochthonous Gut <italic toggle="yes">Enterobacteriaceae</italic> and Their Lytic Bacteriophages
description	ABSTRACT Neonatal calf diarrhea is a common disease leading to a major economic loss for cattle producers worldwide. Several infectious and noninfectious factors are implicated in calf diarrhea, but disease control remains problematic because of the multifactorial etiology of the disease. Here, we conducted diagnostic multiplex PCR assay and meta-omics analysis (16S rRNA gene-based metataxonomics and untargeted transcriptional profiling) of rectal content of normal and diarrheic beef calves (n = 111). In the diarrheic calf gut, we detected both microbial compositional dysbiosis (i.e., increased abundances of the family Enterobacteriaceae members and their lytic bacteriophages) and functional dysbiosis (i.e., elevated levels of aerobic respiration and virulence potential). The calf diarrheic transcriptome mirrored the gene expression of the bovine host and was enriched in cellular pathways of sulfur metabolism, innate immunity, and gut motility. We then isolated 12 nontoxigenic Enterobacteriaceae strains from the gut of diarrheic calves. Feeding a strain mixture to preweaning mice resulted in a significantly higher level of fecal moisture content, with decreased body weight gain and shortened colon length. The presented findings suggest that gut inflammation followed by a prolonged expansion of nontoxigenic autochthonous Enterobacteriaceae contributes to the onset of diarrhea in preweaning animals. IMPORTANCE Calf diarrhea is the leading cause of death of neonatal calves worldwide. Several infectious and noninfectious factors are implicated in calf diarrhea, but disease control remains problematic because of the multifactorial etiology of the disease. The major finding of the current study centers around the observation of microbial compositional and functional dysbiosis in rectal samples from diarrheic calves. These results highlight the notion that gut inflammation followed by a prolonged expansion of autochthonous Enterobacteriaceae contributes to the onset of calf diarrhea. Moreover, this condition possibly potentiates the risk of invasion of notorious enteric pathogens, including Salmonella spp., and the emergence of inflammation-resistant (or antibiotic-resistant) microbiota via active horizontal gene transfer mediated by lytic bacteriophages.
format	article
author	Tae Woong Whon Hyun Sik Kim Na-Ri Shin Hojun Sung Min-Soo Kim Joon Yong Kim Woorim Kang Pil Soo Kim Dong-Wook Hyun Hoon Je Seong Woo Jun Sul Seong Woon Roh Jin-Woo Bae
author_facet	Tae Woong Whon Hyun Sik Kim Na-Ri Shin Hojun Sung Min-Soo Kim Joon Yong Kim Woorim Kang Pil Soo Kim Dong-Wook Hyun Hoon Je Seong Woo Jun Sul Seong Woon Roh Jin-Woo Bae
author_sort	Tae Woong Whon
title	Calf Diarrhea Caused by Prolonged Expansion of Autochthonous Gut <italic toggle="yes">Enterobacteriaceae</italic> and Their Lytic Bacteriophages
title_short	Calf Diarrhea Caused by Prolonged Expansion of Autochthonous Gut <italic toggle="yes">Enterobacteriaceae</italic> and Their Lytic Bacteriophages
title_full	Calf Diarrhea Caused by Prolonged Expansion of Autochthonous Gut <italic toggle="yes">Enterobacteriaceae</italic> and Their Lytic Bacteriophages
title_fullStr	Calf Diarrhea Caused by Prolonged Expansion of Autochthonous Gut <italic toggle="yes">Enterobacteriaceae</italic> and Their Lytic Bacteriophages
title_full_unstemmed	Calf Diarrhea Caused by Prolonged Expansion of Autochthonous Gut <italic toggle="yes">Enterobacteriaceae</italic> and Their Lytic Bacteriophages
title_sort	calf diarrhea caused by prolonged expansion of autochthonous gut <italic toggle="yes">enterobacteriaceae</italic> and their lytic bacteriophages
publisher	American Society for Microbiology
publishDate	2021
url	https://doaj.org/article/d6f735f1fa424644a9af3236f2494936
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Calf Diarrhea Caused by Prolonged Expansion of Autochthonous Gut <italic toggle="yes">Enterobacteriaceae</italic> and Their Lytic Bacteriophages

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