Species Deletions from Microbiome Consortia Reveal Key Metabolic Interactions between Gut Microbes

ABSTRACT The gut microbiome is a complex microbial community that plays a key role in human health. Diet is an important factor dictating gut microbiome composition. This is mediated by multiple microbe-microbe interactions that result in the fermentation of nondigestible carbohydrates and the produ...

Descripción completa

Guardado en:

Detalles Bibliográficos
Autores principales:	Natalia Gutiérrez, Daniel Garrido
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2019
Materias:	bioreactor keystone species microbiome butyrate metabolic interaction Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/bb844e34fb0842b5a812dccc57c408d1
Etiquetas:	Agregar Etiqueta Sin Etiquetas, Sea el primero en etiquetar este registro!

id	oai:doaj.org-article:bb844e34fb0842b5a812dccc57c408d1
record_format	dspace
spelling	oai:doaj.org-article:bb844e34fb0842b5a812dccc57c408d12021-12-02T19:47:34ZSpecies Deletions from Microbiome Consortia Reveal Key Metabolic Interactions between Gut Microbes10.1128/mSystems.00185-192379-5077https://doaj.org/article/bb844e34fb0842b5a812dccc57c408d12019-08-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSystems.00185-19https://doaj.org/toc/2379-5077ABSTRACT The gut microbiome is a complex microbial community that plays a key role in human health. Diet is an important factor dictating gut microbiome composition. This is mediated by multiple microbe-microbe interactions that result in the fermentation of nondigestible carbohydrates and the production of short-chain fatty acids. Certain species play key metabolic roles in the microbiome, and their disappearance could result in dysbiosis. In this work, a synthetic consortium of 14 gut microbes was studied during the utilization of prebiotic inulin in batch bioreactors. Fermentations were repeated leaving one species out every time, in order to evaluate the impact of their elimination on the system. Substrate consumption, microbial composition, and metabolite production were determined. Single deletions never resulted in a complete loss of bacterial growth or inulin consumption, suggesting functional redundancy. Deletions of Bacteroides dorei and Lachnoclostridium clostridioforme resulted in lower biomass and higher residual inulin. The absence of B. dorei impacted the abundance of the other 10 species negatively. Lachnoclostridium symbiosum, a butyrate producer, appeared to be the most sensitive species to deletions, being stimulated by the presence of Escherichia coli, Bifidobacterium adolescentis, B. dorei, and Lactobacillus plantarum. Conversely, bioreactors without these species did not show butyrate production. L. clostridioforme was observed to be essential for propionate production, and B. dorei for lactate production. Our analysis identified specific members that were essential for the function of the consortium. In conclusion, species deletions from microbial consortia could be a useful approach to identify relevant interactions between microorganisms and defining metabolic roles in the gut microbiome. IMPORTANCE Gut microbes associate, compete for, and specialize in specific metabolic tasks. These interactions are dictated by the cross-feeding of degradation or fermentation products. However, the individual contribution of microbes to the function of the gut microbiome is difficult to evaluate. It is essential to understand the complexity of microbial interactions and how the presence or absence of specific microorganisms affects the stability and functioning of the gut microbiome. The experimental approach of this study could be used for identifying keystone species, in addition to redundant functions and conditions that contribute to community stability. Redundancy is an important feature of the microbiome, and its reduction could be useful for the design of microbial consortia with desired metabolic properties enhancing the tasks of the keystone species.Natalia GutiérrezDaniel GarridoAmerican Society for Microbiologyarticlebioreactorkeystone speciesmicrobiomebutyratemetabolic interactionMicrobiologyQR1-502ENmSystems, Vol 4, Iss 4 (2019)
institution	DOAJ
collection	DOAJ
language	EN
topic	bioreactor keystone species microbiome butyrate metabolic interaction Microbiology QR1-502
spellingShingle	bioreactor keystone species microbiome butyrate metabolic interaction Microbiology QR1-502 Natalia Gutiérrez Daniel Garrido Species Deletions from Microbiome Consortia Reveal Key Metabolic Interactions between Gut Microbes
description	ABSTRACT The gut microbiome is a complex microbial community that plays a key role in human health. Diet is an important factor dictating gut microbiome composition. This is mediated by multiple microbe-microbe interactions that result in the fermentation of nondigestible carbohydrates and the production of short-chain fatty acids. Certain species play key metabolic roles in the microbiome, and their disappearance could result in dysbiosis. In this work, a synthetic consortium of 14 gut microbes was studied during the utilization of prebiotic inulin in batch bioreactors. Fermentations were repeated leaving one species out every time, in order to evaluate the impact of their elimination on the system. Substrate consumption, microbial composition, and metabolite production were determined. Single deletions never resulted in a complete loss of bacterial growth or inulin consumption, suggesting functional redundancy. Deletions of Bacteroides dorei and Lachnoclostridium clostridioforme resulted in lower biomass and higher residual inulin. The absence of B. dorei impacted the abundance of the other 10 species negatively. Lachnoclostridium symbiosum, a butyrate producer, appeared to be the most sensitive species to deletions, being stimulated by the presence of Escherichia coli, Bifidobacterium adolescentis, B. dorei, and Lactobacillus plantarum. Conversely, bioreactors without these species did not show butyrate production. L. clostridioforme was observed to be essential for propionate production, and B. dorei for lactate production. Our analysis identified specific members that were essential for the function of the consortium. In conclusion, species deletions from microbial consortia could be a useful approach to identify relevant interactions between microorganisms and defining metabolic roles in the gut microbiome. IMPORTANCE Gut microbes associate, compete for, and specialize in specific metabolic tasks. These interactions are dictated by the cross-feeding of degradation or fermentation products. However, the individual contribution of microbes to the function of the gut microbiome is difficult to evaluate. It is essential to understand the complexity of microbial interactions and how the presence or absence of specific microorganisms affects the stability and functioning of the gut microbiome. The experimental approach of this study could be used for identifying keystone species, in addition to redundant functions and conditions that contribute to community stability. Redundancy is an important feature of the microbiome, and its reduction could be useful for the design of microbial consortia with desired metabolic properties enhancing the tasks of the keystone species.
format	article
author	Natalia Gutiérrez Daniel Garrido
author_facet	Natalia Gutiérrez Daniel Garrido
author_sort	Natalia Gutiérrez
title	Species Deletions from Microbiome Consortia Reveal Key Metabolic Interactions between Gut Microbes
title_short	Species Deletions from Microbiome Consortia Reveal Key Metabolic Interactions between Gut Microbes
title_full	Species Deletions from Microbiome Consortia Reveal Key Metabolic Interactions between Gut Microbes
title_fullStr	Species Deletions from Microbiome Consortia Reveal Key Metabolic Interactions between Gut Microbes
title_full_unstemmed	Species Deletions from Microbiome Consortia Reveal Key Metabolic Interactions between Gut Microbes
title_sort	species deletions from microbiome consortia reveal key metabolic interactions between gut microbes
publisher	American Society for Microbiology
publishDate	2019
url	https://doaj.org/article/bb844e34fb0842b5a812dccc57c408d1
work_keys_str_mv	AT nataliagutierrez speciesdeletionsfrommicrobiomeconsortiarevealkeymetabolicinteractionsbetweengutmicrobes AT danielgarrido speciesdeletionsfrommicrobiomeconsortiarevealkeymetabolicinteractionsbetweengutmicrobes
_version_	1718375986728271872

Species Deletions from Microbiome Consortia Reveal Key Metabolic Interactions between Gut Microbes

Ejemplares similares