Spatial Molecular Architecture of the Microbial Community of a <italic toggle="yes">Peltigera</italic> Lichen

ABSTRACT Microbes are commonly studied as individual species, but they exist as mixed assemblages in nature. At present, we know very little about the spatial organization of the molecules, including natural products that are produced within these microbial networks. Lichens represent a particularly...

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Autores principales:	Neha Garg, Yi Zeng, Anna Edlund, Alexey V. Melnik, Laura M. Sanchez, Hosein Mohimani, Alexey Gurevich, Vivian Miao, Stefan Schiffler, Yan Wei Lim, Tal Luzzatto-Knaan, Shengxin Cai, Forest Rohwer, Pavel A. Pevzner, Robert H. Cichewicz, Theodore Alexandrov, Pieter C. Dorrestein
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2016
Materias:	lichen mass spectrometry microbial assemblages natural products metagenomics Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/0f29fc077bfb4feaa8afff827c3c6564
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spelling	oai:doaj.org-article:0f29fc077bfb4feaa8afff827c3c65642021-12-02T18:15:43ZSpatial Molecular Architecture of the Microbial Community of a <italic toggle="yes">Peltigera</italic> Lichen10.1128/mSystems.00139-162379-5077https://doaj.org/article/0f29fc077bfb4feaa8afff827c3c65642016-12-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSystems.00139-16https://doaj.org/toc/2379-5077ABSTRACT Microbes are commonly studied as individual species, but they exist as mixed assemblages in nature. At present, we know very little about the spatial organization of the molecules, including natural products that are produced within these microbial networks. Lichens represent a particularly specialized type of symbiotic microbial assemblage in which the component microorganisms exist together. These composite microbial assemblages are typically comprised of several types of microorganisms representing phylogenetically diverse life forms, including fungi, photosymbionts, bacteria, and other microbes. Here, we employed matrix-assisted laser desorption ionization–time of flight (MALDI-TOF) imaging mass spectrometry to characterize the distributions of small molecules within a Peltigera lichen. In order to probe how small molecules are organized and localized within the microbial consortium, analytes were annotated and assigned to their respective producer microorganisms using mass spectrometry-based molecular networking and metagenome sequencing. The spatial analysis of the molecules not only reveals an ordered layering of molecules within the lichen but also supports the compartmentalization of unique functions attributed to various layers. These functions include chemical defense (e.g., antibiotics), light-harvesting functions associated with the cyanobacterial outer layer (e.g., chlorophyll), energy transfer (e.g., sugars) surrounding the sun-exposed cyanobacterial layer, and carbohydrates that may serve a structural or storage function and are observed with higher intensities in the non-sun-exposed areas (e.g., complex carbohydrates). IMPORTANCE Microbial communities have evolved over centuries to live symbiotically. The direct visualization of such communities at the chemical and functional level presents a challenge. Overcoming this challenge may allow one to visualize the spatial distributions of specific molecules involved in symbiosis and to define their functional roles in shaping the community structure. In this study, we examined the diversity of microbial genes and taxa and the presence of biosynthetic gene clusters by metagenomic sequencing and the compartmentalization of organic chemical components within a lichen using mass spectrometry. This approach allowed the identification of chemically distinct sections within this composite organism. Using our multipronged approach, various fungal natural products, not previously reported from lichens, were identified and two different fungal layers were visualized at the chemical level.Neha GargYi ZengAnna EdlundAlexey V. MelnikLaura M. SanchezHosein MohimaniAlexey GurevichVivian MiaoStefan SchifflerYan Wei LimTal Luzzatto-KnaanShengxin CaiForest RohwerPavel A. PevznerRobert H. CichewiczTheodore AlexandrovPieter C. DorresteinAmerican Society for Microbiologyarticlelichenmass spectrometrymicrobial assemblagesnatural productsmetagenomicsMicrobiologyQR1-502ENmSystems, Vol 1, Iss 6 (2016)
institution	DOAJ
collection	DOAJ
language	EN
topic	lichen mass spectrometry microbial assemblages natural products metagenomics Microbiology QR1-502
spellingShingle	lichen mass spectrometry microbial assemblages natural products metagenomics Microbiology QR1-502 Neha Garg Yi Zeng Anna Edlund Alexey V. Melnik Laura M. Sanchez Hosein Mohimani Alexey Gurevich Vivian Miao Stefan Schiffler Yan Wei Lim Tal Luzzatto-Knaan Shengxin Cai Forest Rohwer Pavel A. Pevzner Robert H. Cichewicz Theodore Alexandrov Pieter C. Dorrestein Spatial Molecular Architecture of the Microbial Community of a <italic toggle="yes">Peltigera</italic> Lichen
description	ABSTRACT Microbes are commonly studied as individual species, but they exist as mixed assemblages in nature. At present, we know very little about the spatial organization of the molecules, including natural products that are produced within these microbial networks. Lichens represent a particularly specialized type of symbiotic microbial assemblage in which the component microorganisms exist together. These composite microbial assemblages are typically comprised of several types of microorganisms representing phylogenetically diverse life forms, including fungi, photosymbionts, bacteria, and other microbes. Here, we employed matrix-assisted laser desorption ionization–time of flight (MALDI-TOF) imaging mass spectrometry to characterize the distributions of small molecules within a Peltigera lichen. In order to probe how small molecules are organized and localized within the microbial consortium, analytes were annotated and assigned to their respective producer microorganisms using mass spectrometry-based molecular networking and metagenome sequencing. The spatial analysis of the molecules not only reveals an ordered layering of molecules within the lichen but also supports the compartmentalization of unique functions attributed to various layers. These functions include chemical defense (e.g., antibiotics), light-harvesting functions associated with the cyanobacterial outer layer (e.g., chlorophyll), energy transfer (e.g., sugars) surrounding the sun-exposed cyanobacterial layer, and carbohydrates that may serve a structural or storage function and are observed with higher intensities in the non-sun-exposed areas (e.g., complex carbohydrates). IMPORTANCE Microbial communities have evolved over centuries to live symbiotically. The direct visualization of such communities at the chemical and functional level presents a challenge. Overcoming this challenge may allow one to visualize the spatial distributions of specific molecules involved in symbiosis and to define their functional roles in shaping the community structure. In this study, we examined the diversity of microbial genes and taxa and the presence of biosynthetic gene clusters by metagenomic sequencing and the compartmentalization of organic chemical components within a lichen using mass spectrometry. This approach allowed the identification of chemically distinct sections within this composite organism. Using our multipronged approach, various fungal natural products, not previously reported from lichens, were identified and two different fungal layers were visualized at the chemical level.
format	article
author	Neha Garg Yi Zeng Anna Edlund Alexey V. Melnik Laura M. Sanchez Hosein Mohimani Alexey Gurevich Vivian Miao Stefan Schiffler Yan Wei Lim Tal Luzzatto-Knaan Shengxin Cai Forest Rohwer Pavel A. Pevzner Robert H. Cichewicz Theodore Alexandrov Pieter C. Dorrestein
author_facet	Neha Garg Yi Zeng Anna Edlund Alexey V. Melnik Laura M. Sanchez Hosein Mohimani Alexey Gurevich Vivian Miao Stefan Schiffler Yan Wei Lim Tal Luzzatto-Knaan Shengxin Cai Forest Rohwer Pavel A. Pevzner Robert H. Cichewicz Theodore Alexandrov Pieter C. Dorrestein
author_sort	Neha Garg
title	Spatial Molecular Architecture of the Microbial Community of a <italic toggle="yes">Peltigera</italic> Lichen
title_short	Spatial Molecular Architecture of the Microbial Community of a <italic toggle="yes">Peltigera</italic> Lichen
title_full	Spatial Molecular Architecture of the Microbial Community of a <italic toggle="yes">Peltigera</italic> Lichen
title_fullStr	Spatial Molecular Architecture of the Microbial Community of a <italic toggle="yes">Peltigera</italic> Lichen
title_full_unstemmed	Spatial Molecular Architecture of the Microbial Community of a <italic toggle="yes">Peltigera</italic> Lichen
title_sort	spatial molecular architecture of the microbial community of a <italic toggle="yes">peltigera</italic> lichen
publisher	American Society for Microbiology
publishDate	2016
url	https://doaj.org/article/0f29fc077bfb4feaa8afff827c3c6564
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Spatial Molecular Architecture of the Microbial Community of a <italic toggle="yes">Peltigera</italic> Lichen

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