Identification of trypsin-degrading commensals in the large intestine

Increased levels of proteases, such as trypsin, in the distal intestine have been implicated in intestinal pathological conditions 1 – 3 . However, the players and mechanisms that underlie protease regulation in the intestinal lumen have remained unclear. Here we show that Paraprevotella strains iso...

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Published inNature (London) Vol. 609; no. 7927; pp. 582 - 589
Main Authors Li, Youxian, Watanabe, Eiichiro, Kawashima, Yusuke, Plichta, Damian R., Wang, Zhujun, Ujike, Makoto, Ang, Qi Yan, Wu, Runrun, Furuichi, Munehiro, Takeshita, Kozue, Yoshida, Koji, Nishiyama, Keita, Kearney, Sean M., Suda, Wataru, Hattori, Masahira, Sasajima, Satoshi, Matsunaga, Takahiro, Zhang, Xiaoxi, Watanabe, Kazuto, Fujishiro, Jun, Norman, Jason M., Olle, Bernat, Matsuyama, Shutoku, Namkoong, Ho, Uwamino, Yoshifumi, Ishii, Makoto, Fukunaga, Koichi, Hasegawa, Naoki, Ohara, Osamu, Xavier, Ramnik J., Atarashi, Koji, Honda, Kenya
Format Journal Article
LanguageEnglish
Published London Nature Publishing Group UK 15.09.2022
Nature Publishing Group
Nature Portfolio
Subjects
101/28
13/1
42/41
631/250/347
631/326/2565/2134
64/60
82/16
82/29
82/58
82/83
Antibiotics
Autolysis
Citrobacter
Colonization
Commensals
Coronaviruses
Degradation
Diarrhea
Enzymes
Hepatitis
Homeostasis
Humanities and Social Sciences
Immunoglobulin A
Infections
Intestinal microflora
Intestine
Large intestine
Microbiomes
Microbiota
multidisciplinary
Pathogens
Polysaccharides
Proteins
Science
Science (multidisciplinary)
Severe acute respiratory syndrome coronavirus 2
Trypsin
Viral diseases
Online AccessGet full text
ISSN0028-0836
1476-4687
1476-4687
DOI10.1038/s41586-022-05181-3

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Abstract Increased levels of proteases, such as trypsin, in the distal intestine have been implicated in intestinal pathological conditions 1 – 3 . However, the players and mechanisms that underlie protease regulation in the intestinal lumen have remained unclear. Here we show that Paraprevotella strains isolated from the faecal microbiome of healthy human donors are potent trypsin-degrading commensals. Mechanistically, Paraprevotella recruit trypsin to the bacterial surface through type IX secretion system-dependent polysaccharide-anchoring proteins to promote trypsin autolysis. Paraprevotella colonization protects IgA from trypsin degradation and enhances the effectiveness of oral vaccines against Citrobacter rodentium . Moreover, Paraprevotella colonization inhibits lethal infection with murine hepatitis virus-2, a mouse coronavirus that is dependent on trypsin and trypsin-like proteases for entry into host cells 4 , 5 . Consistently, carriage of putative genes involved in trypsin degradation in the gut microbiome was associated with reduced severity of diarrhoea in patients with SARS-CoV-2 infection. Thus, trypsin-degrading commensal colonization may contribute to the maintenance of intestinal homeostasis and protection from pathogen infection. Colonization of trypsin-degrading commensal bacteria may contribute to the maintenance of intestinal homeostasis and protection against pathogen infection in humans and mice.
AbstractList Increased levels of proteases, such as trypsin, in the distal intestine have been implicated in intestinal pathological conditions 1–3 . However, the players and mechanisms that underlie protease regulation in the intestinal lumen have remained unclear. Here we show that Paraprevotella strains isolated from the faecal microbiome of healthy human donors are potent trypsin-degrading commensals. Mechanistically, Paraprevotella recruit trypsin to the bacterial surface through type IX secretion system-dependent polysaccharide-anchoring proteins to promote trypsin autolysis. Paraprevotella colonization protects IgA from trypsin degradation and enhances the effectiveness of oral vaccines against Citrobacter rodentium . Moreover, Paraprevotella colonization inhibits lethal infection with murine hepatitis virus-2, a mouse coronavirus that is dependent on trypsin and trypsin-like proteases for entry into host cells 4,5 . Consistently, carriage of putative genes involved in trypsin degradation in the gut microbiome was associated with reduced severity of diarrhoea in patients with SARS-CoV-2 infection. Thus, trypsin-degrading commensal colonization may contribute to the maintenance of intestinal homeostasis and protection from pathogen infection.
Increased levels of proteases, such as trypsin, in the distal intestine have been implicated in intestinal pathological conditions1-3. However, the players and mechanisms that underlie protease regulation in the intestinal lumen have remained unclear. Here we show that Paraprevotella strains isolated from the faecal microbiome of healthy human donors are potent trypsin-degrading commensals. Mechanistically, Paraprevotella recruit trypsin to the bacterial surface through type IX secretion system-dependent polysaccharide-anchoring proteins to promote trypsin autolysis. Paraprevotella colonization protects IgA from trypsin degradation and enhances the effectiveness of oral vaccines against Citrobacter rodentium. Moreover, Paraprevotella colonization inhibits lethal infection with murine hepatitis virus-2, a mouse coronavirus that is dependent on trypsin and trypsin-like proteases for entry into host cells4,5. Consistently, carriage of putative genes involved in trypsin degradation in the gut microbiome was associated with reduced severity of diarrhoea in patients with SARS-CoV-2 infection. Thus, trypsin-degrading commensal colonization may contribute to the maintenance of intestinal homeostasis and protection from pathogen infection.Increased levels of proteases, such as trypsin, in the distal intestine have been implicated in intestinal pathological conditions1-3. However, the players and mechanisms that underlie protease regulation in the intestinal lumen have remained unclear. Here we show that Paraprevotella strains isolated from the faecal microbiome of healthy human donors are potent trypsin-degrading commensals. Mechanistically, Paraprevotella recruit trypsin to the bacterial surface through type IX secretion system-dependent polysaccharide-anchoring proteins to promote trypsin autolysis. Paraprevotella colonization protects IgA from trypsin degradation and enhances the effectiveness of oral vaccines against Citrobacter rodentium. Moreover, Paraprevotella colonization inhibits lethal infection with murine hepatitis virus-2, a mouse coronavirus that is dependent on trypsin and trypsin-like proteases for entry into host cells4,5. Consistently, carriage of putative genes involved in trypsin degradation in the gut microbiome was associated with reduced severity of diarrhoea in patients with SARS-CoV-2 infection. Thus, trypsin-degrading commensal colonization may contribute to the maintenance of intestinal homeostasis and protection from pathogen infection.
Abstract Increased levels of proteases, such as trypsin, in the distal intestine have been implicated in intestinal pathological conditions 1–3 . However, the players and mechanisms that underlie protease regulation in the intestinal lumen have remained unclear. Here we show that Paraprevotella strains isolated from the faecal microbiome of healthy human donors are potent trypsin-degrading commensals. Mechanistically, Paraprevotella recruit trypsin to the bacterial surface through type IX secretion system-dependent polysaccharide-anchoring proteins to promote trypsin autolysis. Paraprevotella colonization protects IgA from trypsin degradation and enhances the effectiveness of oral vaccines against Citrobacter rodentium . Moreover, Paraprevotella colonization inhibits lethal infection with murine hepatitis virus-2, a mouse coronavirus that is dependent on trypsin and trypsin-like proteases for entry into host cells 4,5 . Consistently, carriage of putative genes involved in trypsin degradation in the gut microbiome was associated with reduced severity of diarrhoea in patients with SARS-CoV-2 infection. Thus, trypsin-degrading commensal colonization may contribute to the maintenance of intestinal homeostasis and protection from pathogen infection.
Increased levels of proteases, such as trypsin, in the distal intestine have been implicated in intestinal pathological conditions 1 – 3 . However, the players and mechanisms that underlie protease regulation in the intestinal lumen have remained unclear. Here we show that Paraprevotella strains isolated from the faecal microbiome of healthy human donors are potent trypsin-degrading commensals. Mechanistically, Paraprevotella recruit trypsin to the bacterial surface through type IX secretion system-dependent polysaccharide-anchoring proteins to promote trypsin autolysis. Paraprevotella colonization protects IgA from trypsin degradation and enhances the effectiveness of oral vaccines against Citrobacter rodentium . Moreover, Paraprevotella colonization inhibits lethal infection with murine hepatitis virus-2, a mouse coronavirus that is dependent on trypsin and trypsin-like proteases for entry into host cells 4 , 5 . Consistently, carriage of putative genes involved in trypsin degradation in the gut microbiome was associated with reduced severity of diarrhoea in patients with SARS-CoV-2 infection. Thus, trypsin-degrading commensal colonization may contribute to the maintenance of intestinal homeostasis and protection from pathogen infection. Colonization of trypsin-degrading commensal bacteria may contribute to the maintenance of intestinal homeostasis and protection against pathogen infection in humans and mice.
Increased levels of proteases, such as trypsin, in the distal intestine have been implicated in intestinal pathological conditions1-3. However, the players and mechanisms that underlie protease regulation in the intestinal lumen have remained unclear. Here we show that Paraprevotella strains isolated from the faecal microbiome of healthy human donors are potent trypsin-degrading commensals. Mechanistically, Paraprevotella recruit trypsin to the bacterial surface through type IX secretion system-dependent polysaccharide-anchoring proteins to promote trypsin autolysis. Paraprevotella colonization protects IgA from trypsin degradation and enhances the effectiveness of oral vaccines against Citrobacter rodentium. Moreover, Paraprevotella colonization inhibits lethal infection with murine hepatitis virus-2, a mouse coronavirus that is dependent on trypsin and trypsin-like proteases for entry into host cells4,5. Consistently, carriage of putative genes involved in trypsin degradation in the gut microbiome was associated with reduced severity of diarrhoea in patients with SARS-CoV-2 infection. Thus, trypsin-degrading commensal colonization may contribute to the maintenance of intestinal homeostasis and protection from pathogen infection.
Author Fukunaga, Koichi
Furuichi, Munehiro
Hattori, Masahira
Ujike, Makoto
Wang, Zhujun
Matsunaga, Takahiro
Uwamino, Yoshifumi
Kearney, Sean M.
Plichta, Damian R.
Olle, Bernat
Watanabe, Kazuto
Yoshida, Koji
Honda, Kenya
Norman, Jason M.
Atarashi, Koji
Watanabe, Eiichiro
Zhang, Xiaoxi
Li, Youxian
Sasajima, Satoshi
Hasegawa, Naoki
Takeshita, Kozue
Ishii, Makoto
Ohara, Osamu
Kawashima, Yusuke
Matsuyama, Shutoku
Xavier, Ramnik J.
Suda, Wataru
Namkoong, Ho
Fujishiro, Jun
Wu, Runrun
Nishiyama, Keita
Ang, Qi Yan
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ContentType Journal Article
Copyright The Author(s) 2022
Copyright Nature Publishing Group Sep 15, 2022
2022. The Author(s).
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– notice: Copyright Nature Publishing Group Sep 15, 2022
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Snippet Increased levels of proteases, such as trypsin, in the distal intestine have been implicated in intestinal pathological conditions 1 – 3 . However, the players...
Increased levels of proteases, such as trypsin, in the distal intestine have been implicated in intestinal pathological conditions 1–3 . However, the players...
Increased levels of proteases, such as trypsin, in the distal intestine have been implicated in intestinal pathological conditions1-3. However, the players and...
Abstract Increased levels of proteases, such as trypsin, in the distal intestine have been implicated in intestinal pathological conditions 1–3 . However, the...
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SubjectTerms 101/28
13/1
42/41
631/250/347
631/326/2565/2134
64/60
82/16
82/29
82/58
82/83
Antibiotics
Autolysis
Citrobacter
Colonization
Commensals
Coronaviruses
Degradation
Diarrhea
Enzymes
Hepatitis
Homeostasis
Humanities and Social Sciences
Immunoglobulin A
Infections
Intestinal microflora
Intestine
Large intestine
Microbiomes
Microbiota
multidisciplinary
Pathogens
Polysaccharides
Proteins
Science
Science (multidisciplinary)
Severe acute respiratory syndrome coronavirus 2
Trypsin
Viral diseases
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Title Identification of trypsin-degrading commensals in the large intestine
URI https://link.springer.com/article/10.1038/s41586-022-05181-3
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