Spatial molecular architecture of the microbial community of a Peltigera lichen

Neha Garg, Yi Zeng, Anna Edlund, Alexey V. Melnik, Laura Sanchez, Hosein Mohimani, Алексей Александрович Гуревич, Vivian Miao, Stefan Schiffler, Yan Wei Lim, Tal Luzzatto-Knaan, Shengxin Cai, Forest Rohwer, Павел Аркадьевич Певзнер, Robert H. Cichewicz, Theodore Alexandrov, Pieter C Dorrestein

Research output

11 Citations (Scopus)

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.
Original languageEnglish
JournalmSystems
Volume1
Issue number6
DOIs
Publication statusPublished - 27 Dec 2016

Fingerprint

Peltigera
Lichens
lichen
lichens
microbial communities
microbial community
Molecules
microorganisms
Microorganisms
Mass Spectrometry
compartmentalization
mass spectrometry
microorganism
Mass spectrometry
Biological Products
Carbohydrates
carbohydrate
Microbial Genes
Sequencing
Microbial Consortia

Scopus subject areas

  • Biochemistry, Genetics and Molecular Biology (miscellaneous)

Cite this

Garg, N., Zeng, Y., Edlund, A., Melnik, A. V., Sanchez, L., Mohimani, H., ... Dorrestein, P. C. (2016). Spatial molecular architecture of the microbial community of a Peltigera lichen. mSystems, 1(6). https://doi.org/10.1128/mSystems.00139-16
Garg, Neha ; Zeng, Yi ; Edlund, Anna ; Melnik, Alexey V. ; Sanchez, Laura ; Mohimani, Hosein ; Гуревич, Алексей Александрович ; Miao, Vivian ; Schiffler, Stefan ; Lim, Yan Wei ; Luzzatto-Knaan, Tal ; Cai, Shengxin ; Rohwer, Forest ; Певзнер, Павел Аркадьевич ; Cichewicz, Robert H. ; Alexandrov, Theodore ; Dorrestein, Pieter C. / Spatial molecular architecture of the microbial community of a Peltigera lichen. In: mSystems. 2016 ; Vol. 1, No. 6.
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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.",
author = "Neha Garg and Yi Zeng and Anna Edlund and Melnik, {Alexey V.} and Laura Sanchez and Hosein Mohimani and Гуревич, {Алексей Александрович} and Vivian Miao and Stefan Schiffler and Lim, {Yan Wei} and Tal Luzzatto-Knaan and Shengxin Cai and Forest Rohwer and Певзнер, {Павел Аркадьевич} and Cichewicz, {Robert H.} and Theodore Alexandrov and Dorrestein, {Pieter C}",
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Garg, N, Zeng, Y, Edlund, A, Melnik, AV, Sanchez, L, Mohimani, H, Гуревич, АА, Miao, V, Schiffler, S, Lim, YW, Luzzatto-Knaan, T, Cai, S, Rohwer, F, Певзнер, ПА, Cichewicz, RH, Alexandrov, T & Dorrestein, PC 2016, 'Spatial molecular architecture of the microbial community of a Peltigera lichen', mSystems, vol. 1, no. 6. https://doi.org/10.1128/mSystems.00139-16

Spatial molecular architecture of the microbial community of a Peltigera lichen. / Garg, Neha; Zeng, Yi; Edlund, Anna; Melnik, Alexey V.; Sanchez, Laura; Mohimani, Hosein; Гуревич, Алексей Александрович; Miao, Vivian; Schiffler, Stefan; Lim, Yan Wei; Luzzatto-Knaan, Tal; Cai, Shengxin; Rohwer, Forest; Певзнер, Павел Аркадьевич; Cichewicz, Robert H.; Alexandrov, Theodore; Dorrestein, Pieter C.

In: mSystems, Vol. 1, No. 6, 27.12.2016.

Research output

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T1 - Spatial molecular architecture of the microbial community of a Peltigera lichen

AU - Garg, Neha

AU - Zeng, Yi

AU - Edlund, Anna

AU - Melnik, Alexey V.

AU - Sanchez, Laura

AU - Mohimani, Hosein

AU - Гуревич, Алексей Александрович

AU - Miao, Vivian

AU - Schiffler, Stefan

AU - Lim, Yan Wei

AU - Luzzatto-Knaan, Tal

AU - Cai, Shengxin

AU - Rohwer, Forest

AU - Певзнер, Павел Аркадьевич

AU - Cichewicz, Robert H.

AU - Alexandrov, Theodore

AU - Dorrestein, Pieter C

PY - 2016/12/27

Y1 - 2016/12/27

N2 - 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.

AB - 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.

U2 - 10.1128/mSystems.00139-16

DO - 10.1128/mSystems.00139-16

M3 - Article

VL - 1

JO - mSystems

JF - mSystems

SN - 2379-5077

IS - 6

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Garg N, Zeng Y, Edlund A, Melnik AV, Sanchez L, Mohimani H et al. Spatial molecular architecture of the microbial community of a Peltigera lichen. mSystems. 2016 Dec 27;1(6). https://doi.org/10.1128/mSystems.00139-16