A Distinct Contractile Injection System Gene Cluster Found in a Majority of Healthy Adult Human Microbiomes

ABSTRACT Many commensal bacteria antagonize each other or their host by producing syringe-like secretion systems called contractile injection systems (CIS). Members of the Bacteroidales family have been shown to produce only one type of CIS—a contact-dependent type 6 secretion system that mediates b...

Descripción completa

Guardado en:

Detalles Bibliográficos
Autores principales:	Maria I. Rojas, Giselle S. Cavalcanti, Katelyn McNair, Sean Benler, Amanda T. Alker, Ana G. Cobián-Güemes, Melissa Giluso, Kyle Levi, Forest Rohwer, Barbara A. Bailey, Sinem Beyhan, Robert A. Edwards, Nicholas J. Shikuma
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2020
Materias:	CIS microbiome secretion system T6SS bacteriophage eCIS Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/0e039b7dce5c4db2a12161517387aa3e
Etiquetas:	Agregar Etiqueta Sin Etiquetas, Sea el primero en etiquetar este registro!

id	oai:doaj.org-article:0e039b7dce5c4db2a12161517387aa3e
record_format	dspace
spelling	oai:doaj.org-article:0e039b7dce5c4db2a12161517387aa3e2021-12-02T19:46:20ZA Distinct Contractile Injection System Gene Cluster Found in a Majority of Healthy Adult Human Microbiomes10.1128/mSystems.00648-202379-5077https://doaj.org/article/0e039b7dce5c4db2a12161517387aa3e2020-08-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSystems.00648-20https://doaj.org/toc/2379-5077ABSTRACT Many commensal bacteria antagonize each other or their host by producing syringe-like secretion systems called contractile injection systems (CIS). Members of the Bacteroidales family have been shown to produce only one type of CIS—a contact-dependent type 6 secretion system that mediates bacterium-bacterium interactions. Here, we show that a second distinct cluster of genes from Bacteroidales bacteria from the human microbiome may encode yet-uncharacterized injection systems that we term Bacteroidales injection systems (BIS). We found that BIS genes are present in the gut microbiomes of 99% of individuals from the United States and Europe and that BIS genes are more prevalent in the gut microbiomes of healthy individuals than in those individuals suffering from inflammatory bowel disease. Gene clusters similar to that of the BIS mediate interactions between bacteria and diverse eukaryotes, like amoeba, insects, and tubeworms. Our findings highlight the ubiquity of the BIS gene cluster in the human gut and emphasize the relevance of the gut microbiome to the human host. These results warrant investigations into the structure and function of the BIS and how they might mediate interactions between Bacteroidales bacteria and the human host or microbiome. IMPORTANCE To engage with host cells, diverse pathogenic bacteria produce syringe-like structures called contractile injection systems (CIS). CIS are evolutionarily related to the contractile tails of bacteriophages and are specialized to puncture membranes, often delivering effectors to target cells. Although CIS are key for pathogens to cause disease, paradoxically, similar injection systems have been identified within healthy human microbiome bacteria. Here, we show that gene clusters encoding a predicted CIS, which we term Bacteroidales injection systems (BIS), are present in the microbiomes of nearly all adult humans tested from Western countries. BIS genes are enriched within human gut microbiomes and are expressed both in vitro and in vivo. Further, a greater abundance of BIS genes is present within healthy gut microbiomes than in those humans with with inflammatory bowel disease (IBD). Our discovery provides a potentially distinct means by which our microbiome interacts with the human host or its microbiome.Maria I. RojasGiselle S. CavalcantiKatelyn McNairSean BenlerAmanda T. AlkerAna G. Cobián-GüemesMelissa GilusoKyle LeviForest RohwerBarbara A. BaileySinem BeyhanRobert A. EdwardsNicholas J. ShikumaAmerican Society for MicrobiologyarticleCISmicrobiomesecretion systemT6SSbacteriophageeCISMicrobiologyQR1-502ENmSystems, Vol 5, Iss 4 (2020)
institution	DOAJ
collection	DOAJ
language	EN
topic	CIS microbiome secretion system T6SS bacteriophage eCIS Microbiology QR1-502
spellingShingle	CIS microbiome secretion system T6SS bacteriophage eCIS Microbiology QR1-502 Maria I. Rojas Giselle S. Cavalcanti Katelyn McNair Sean Benler Amanda T. Alker Ana G. Cobián-Güemes Melissa Giluso Kyle Levi Forest Rohwer Barbara A. Bailey Sinem Beyhan Robert A. Edwards Nicholas J. Shikuma A Distinct Contractile Injection System Gene Cluster Found in a Majority of Healthy Adult Human Microbiomes
description	ABSTRACT Many commensal bacteria antagonize each other or their host by producing syringe-like secretion systems called contractile injection systems (CIS). Members of the Bacteroidales family have been shown to produce only one type of CIS—a contact-dependent type 6 secretion system that mediates bacterium-bacterium interactions. Here, we show that a second distinct cluster of genes from Bacteroidales bacteria from the human microbiome may encode yet-uncharacterized injection systems that we term Bacteroidales injection systems (BIS). We found that BIS genes are present in the gut microbiomes of 99% of individuals from the United States and Europe and that BIS genes are more prevalent in the gut microbiomes of healthy individuals than in those individuals suffering from inflammatory bowel disease. Gene clusters similar to that of the BIS mediate interactions between bacteria and diverse eukaryotes, like amoeba, insects, and tubeworms. Our findings highlight the ubiquity of the BIS gene cluster in the human gut and emphasize the relevance of the gut microbiome to the human host. These results warrant investigations into the structure and function of the BIS and how they might mediate interactions between Bacteroidales bacteria and the human host or microbiome. IMPORTANCE To engage with host cells, diverse pathogenic bacteria produce syringe-like structures called contractile injection systems (CIS). CIS are evolutionarily related to the contractile tails of bacteriophages and are specialized to puncture membranes, often delivering effectors to target cells. Although CIS are key for pathogens to cause disease, paradoxically, similar injection systems have been identified within healthy human microbiome bacteria. Here, we show that gene clusters encoding a predicted CIS, which we term Bacteroidales injection systems (BIS), are present in the microbiomes of nearly all adult humans tested from Western countries. BIS genes are enriched within human gut microbiomes and are expressed both in vitro and in vivo. Further, a greater abundance of BIS genes is present within healthy gut microbiomes than in those humans with with inflammatory bowel disease (IBD). Our discovery provides a potentially distinct means by which our microbiome interacts with the human host or its microbiome.
format	article
author	Maria I. Rojas Giselle S. Cavalcanti Katelyn McNair Sean Benler Amanda T. Alker Ana G. Cobián-Güemes Melissa Giluso Kyle Levi Forest Rohwer Barbara A. Bailey Sinem Beyhan Robert A. Edwards Nicholas J. Shikuma
author_facet	Maria I. Rojas Giselle S. Cavalcanti Katelyn McNair Sean Benler Amanda T. Alker Ana G. Cobián-Güemes Melissa Giluso Kyle Levi Forest Rohwer Barbara A. Bailey Sinem Beyhan Robert A. Edwards Nicholas J. Shikuma
author_sort	Maria I. Rojas
title	A Distinct Contractile Injection System Gene Cluster Found in a Majority of Healthy Adult Human Microbiomes
title_short	A Distinct Contractile Injection System Gene Cluster Found in a Majority of Healthy Adult Human Microbiomes
title_full	A Distinct Contractile Injection System Gene Cluster Found in a Majority of Healthy Adult Human Microbiomes
title_fullStr	A Distinct Contractile Injection System Gene Cluster Found in a Majority of Healthy Adult Human Microbiomes
title_full_unstemmed	A Distinct Contractile Injection System Gene Cluster Found in a Majority of Healthy Adult Human Microbiomes
title_sort	distinct contractile injection system gene cluster found in a majority of healthy adult human microbiomes
publisher	American Society for Microbiology
publishDate	2020
url	https://doaj.org/article/0e039b7dce5c4db2a12161517387aa3e
work_keys_str_mv	AT mariairojas adistinctcontractileinjectionsystemgeneclusterfoundinamajorityofhealthyadulthumanmicrobiomes AT gisellescavalcanti adistinctcontractileinjectionsystemgeneclusterfoundinamajorityofhealthyadulthumanmicrobiomes AT katelynmcnair adistinctcontractileinjectionsystemgeneclusterfoundinamajorityofhealthyadulthumanmicrobiomes AT seanbenler adistinctcontractileinjectionsystemgeneclusterfoundinamajorityofhealthyadulthumanmicrobiomes AT amandatalker adistinctcontractileinjectionsystemgeneclusterfoundinamajorityofhealthyadulthumanmicrobiomes AT anagcobianguemes adistinctcontractileinjectionsystemgeneclusterfoundinamajorityofhealthyadulthumanmicrobiomes AT melissagiluso adistinctcontractileinjectionsystemgeneclusterfoundinamajorityofhealthyadulthumanmicrobiomes AT kylelevi adistinctcontractileinjectionsystemgeneclusterfoundinamajorityofhealthyadulthumanmicrobiomes AT forestrohwer adistinctcontractileinjectionsystemgeneclusterfoundinamajorityofhealthyadulthumanmicrobiomes AT barbaraabailey adistinctcontractileinjectionsystemgeneclusterfoundinamajorityofhealthyadulthumanmicrobiomes AT sinembeyhan adistinctcontractileinjectionsystemgeneclusterfoundinamajorityofhealthyadulthumanmicrobiomes AT robertaedwards adistinctcontractileinjectionsystemgeneclusterfoundinamajorityofhealthyadulthumanmicrobiomes AT nicholasjshikuma adistinctcontractileinjectionsystemgeneclusterfoundinamajorityofhealthyadulthumanmicrobiomes AT mariairojas distinctcontractileinjectionsystemgeneclusterfoundinamajorityofhealthyadulthumanmicrobiomes AT gisellescavalcanti distinctcontractileinjectionsystemgeneclusterfoundinamajorityofhealthyadulthumanmicrobiomes AT katelynmcnair distinctcontractileinjectionsystemgeneclusterfoundinamajorityofhealthyadulthumanmicrobiomes AT seanbenler distinctcontractileinjectionsystemgeneclusterfoundinamajorityofhealthyadulthumanmicrobiomes AT amandatalker distinctcontractileinjectionsystemgeneclusterfoundinamajorityofhealthyadulthumanmicrobiomes AT anagcobianguemes distinctcontractileinjectionsystemgeneclusterfoundinamajorityofhealthyadulthumanmicrobiomes AT melissagiluso distinctcontractileinjectionsystemgeneclusterfoundinamajorityofhealthyadulthumanmicrobiomes AT kylelevi distinctcontractileinjectionsystemgeneclusterfoundinamajorityofhealthyadulthumanmicrobiomes AT forestrohwer distinctcontractileinjectionsystemgeneclusterfoundinamajorityofhealthyadulthumanmicrobiomes AT barbaraabailey distinctcontractileinjectionsystemgeneclusterfoundinamajorityofhealthyadulthumanmicrobiomes AT sinembeyhan distinctcontractileinjectionsystemgeneclusterfoundinamajorityofhealthyadulthumanmicrobiomes AT robertaedwards distinctcontractileinjectionsystemgeneclusterfoundinamajorityofhealthyadulthumanmicrobiomes AT nicholasjshikuma distinctcontractileinjectionsystemgeneclusterfoundinamajorityofhealthyadulthumanmicrobiomes
_version_	1718376005789286400

A Distinct Contractile Injection System Gene Cluster Found in a Majority of Healthy Adult Human Microbiomes

Ejemplares similares