Cooperation, Competition, and Specialized Metabolism in a Simplified Root Nodule Microbiome

ABSTRACT Microbiomes associated with various plant structures often contain members with the potential to make specialized metabolites, e.g., molecules with antibacterial, antifungal, or siderophore activities. However, when and where microbes associated with plants produce specialized metabolites,...

Descripción completa

Guardado en:

Detalles Bibliográficos
Autores principales:	Bridget L. Hansen, Rita de Cassia Pessotti, Monika S. Fischer, Alyssa Collins, Laila El-Hifnawi, Mira D. Liu, Matthew F. Traxler
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2020
Materias:	antibiotic microbial interactions microbiome root nodule specialized metabolism Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/60b3ce32aa7f45339f1383b63e8e7d88
Etiquetas:	Agregar Etiqueta Sin Etiquetas, Sea el primero en etiquetar este registro!

id	oai:doaj.org-article:60b3ce32aa7f45339f1383b63e8e7d88
record_format	dspace
spelling	oai:doaj.org-article:60b3ce32aa7f45339f1383b63e8e7d882021-11-15T15:56:43ZCooperation, Competition, and Specialized Metabolism in a Simplified Root Nodule Microbiome10.1128/mBio.01917-202150-7511https://doaj.org/article/60b3ce32aa7f45339f1383b63e8e7d882020-08-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.01917-20https://doaj.org/toc/2150-7511ABSTRACT Microbiomes associated with various plant structures often contain members with the potential to make specialized metabolites, e.g., molecules with antibacterial, antifungal, or siderophore activities. However, when and where microbes associated with plants produce specialized metabolites, and the potential role of these molecules in mediating intramicrobiome interactions, is not well understood. Root nodules of legume plants are organs devoted to hosting symbiotic bacteria that fix atmospheric nitrogen and have recently been shown to harbor a relatively simple accessory microbiome containing members with the ability to produce specialized metabolites in vitro. On the basis of these observations, we sought to develop a model nodule microbiome system for evaluating specialized microbial metabolism in planta. Starting with an inoculum derived from field-grown Medicago sativa nodules, serial passaging through gnotobiotic nodules yielded a simplified accessory community composed of four members: Brevibacillus brevis, Paenibacillus sp., Pantoea agglomerans, and Pseudomonas sp. Some members of this community exhibited clear cooperation in planta, while others were antagonistic and capable of disrupting cooperation between other partners. Using matrix-assisted laser desorption ionization–imaging mass spectrometry, we found that metabolites associated with individual taxa had unique distributions, indicating that some members of the nodule community were spatially segregated. Finally, we identified two families of molecules produced by B. brevis in planta as the antibacterial tyrocidines and a novel set of gramicidin-type molecules, which we term the britacidins. Collectively, these results indicate that in addition to nitrogen fixation, legume root nodules are likely also sites of active antimicrobial production.Bridget L. HansenRita de Cassia PessottiMonika S. FischerAlyssa CollinsLaila El-HifnawiMira D. LiuMatthew F. TraxlerAmerican Society for Microbiologyarticleantibioticmicrobial interactionsmicrobiomeroot nodulespecialized metabolismMicrobiologyQR1-502ENmBio, Vol 11, Iss 4 (2020)
institution	DOAJ
collection	DOAJ
language	EN
topic	antibiotic microbial interactions microbiome root nodule specialized metabolism Microbiology QR1-502
spellingShingle	antibiotic microbial interactions microbiome root nodule specialized metabolism Microbiology QR1-502 Bridget L. Hansen Rita de Cassia Pessotti Monika S. Fischer Alyssa Collins Laila El-Hifnawi Mira D. Liu Matthew F. Traxler Cooperation, Competition, and Specialized Metabolism in a Simplified Root Nodule Microbiome
description	ABSTRACT Microbiomes associated with various plant structures often contain members with the potential to make specialized metabolites, e.g., molecules with antibacterial, antifungal, or siderophore activities. However, when and where microbes associated with plants produce specialized metabolites, and the potential role of these molecules in mediating intramicrobiome interactions, is not well understood. Root nodules of legume plants are organs devoted to hosting symbiotic bacteria that fix atmospheric nitrogen and have recently been shown to harbor a relatively simple accessory microbiome containing members with the ability to produce specialized metabolites in vitro. On the basis of these observations, we sought to develop a model nodule microbiome system for evaluating specialized microbial metabolism in planta. Starting with an inoculum derived from field-grown Medicago sativa nodules, serial passaging through gnotobiotic nodules yielded a simplified accessory community composed of four members: Brevibacillus brevis, Paenibacillus sp., Pantoea agglomerans, and Pseudomonas sp. Some members of this community exhibited clear cooperation in planta, while others were antagonistic and capable of disrupting cooperation between other partners. Using matrix-assisted laser desorption ionization–imaging mass spectrometry, we found that metabolites associated with individual taxa had unique distributions, indicating that some members of the nodule community were spatially segregated. Finally, we identified two families of molecules produced by B. brevis in planta as the antibacterial tyrocidines and a novel set of gramicidin-type molecules, which we term the britacidins. Collectively, these results indicate that in addition to nitrogen fixation, legume root nodules are likely also sites of active antimicrobial production.
format	article
author	Bridget L. Hansen Rita de Cassia Pessotti Monika S. Fischer Alyssa Collins Laila El-Hifnawi Mira D. Liu Matthew F. Traxler
author_facet	Bridget L. Hansen Rita de Cassia Pessotti Monika S. Fischer Alyssa Collins Laila El-Hifnawi Mira D. Liu Matthew F. Traxler
author_sort	Bridget L. Hansen
title	Cooperation, Competition, and Specialized Metabolism in a Simplified Root Nodule Microbiome
title_short	Cooperation, Competition, and Specialized Metabolism in a Simplified Root Nodule Microbiome
title_full	Cooperation, Competition, and Specialized Metabolism in a Simplified Root Nodule Microbiome
title_fullStr	Cooperation, Competition, and Specialized Metabolism in a Simplified Root Nodule Microbiome
title_full_unstemmed	Cooperation, Competition, and Specialized Metabolism in a Simplified Root Nodule Microbiome
title_sort	cooperation, competition, and specialized metabolism in a simplified root nodule microbiome
publisher	American Society for Microbiology
publishDate	2020
url	https://doaj.org/article/60b3ce32aa7f45339f1383b63e8e7d88
work_keys_str_mv	AT bridgetlhansen cooperationcompetitionandspecializedmetabolisminasimplifiedrootnodulemicrobiome AT ritadecassiapessotti cooperationcompetitionandspecializedmetabolisminasimplifiedrootnodulemicrobiome AT monikasfischer cooperationcompetitionandspecializedmetabolisminasimplifiedrootnodulemicrobiome AT alyssacollins cooperationcompetitionandspecializedmetabolisminasimplifiedrootnodulemicrobiome AT lailaelhifnawi cooperationcompetitionandspecializedmetabolisminasimplifiedrootnodulemicrobiome AT miradliu cooperationcompetitionandspecializedmetabolisminasimplifiedrootnodulemicrobiome AT matthewftraxler cooperationcompetitionandspecializedmetabolisminasimplifiedrootnodulemicrobiome
_version_	1718427151819079680

Cooperation, Competition, and Specialized Metabolism in a Simplified Root Nodule Microbiome

Ejemplares similares