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Editor's Pick Research Article | Novel Systems Biology Techniques

Spatial Molecular Architecture of the Microbial Community of a Peltigera Lichen

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
Janet K. Jansson, Editor
Neha Garg
aSkaggs School of Pharmacy and Pharmaceutical Sciences, University of California, San Diego, California, USA
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Yi Zeng
bDepartment of Chemistry and Biochemistry, University of California, San Diego, California, USA
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Anna Edlund
cGenomic Medicine, J. Craig Venter Institute, La Jolla, California, USA
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Alexey V. Melnik
aSkaggs School of Pharmacy and Pharmaceutical Sciences, University of California, San Diego, California, USA
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Laura M. Sanchez
aSkaggs School of Pharmacy and Pharmaceutical Sciences, University of California, San Diego, California, USA
dDepartment of Medicinal Chemistry and Pharmacognosy, College of Pharmacy, University of Illinois at Chicago, Chicago, Illinois, USA
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  • ORCID record for Laura M. Sanchez
Hosein Mohimani
kDepartment of Computer Science and Engineering, University of California San Diego, La Jolla, California, USA
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Alexey Gurevich
lCenter for Algorithmic Biotechnology, Institute of Translational Biomedicine, St. Petersburg State University, St. Petersburg, Russia
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Vivian Miao
eDepartment of Microbiology and Immunology, University of British Columbia, Vancouver, Canada
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Stefan Schiffler
fSCiLS GmbH, Bremen, Germany
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Yan Wei Lim
gDepartment of Biology, San Diego State University, San Diego, California, USA
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Tal Luzzatto-Knaan
aSkaggs School of Pharmacy and Pharmaceutical Sciences, University of California, San Diego, California, USA
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Shengxin Cai
hNatural Products Discovery Group, Department of Chemistry and Biochemistry, Institute for Natural Products Applications and Research Technologies, Stephenson Life Sciences Research Center, University of Oklahoma, Norman, Oklahoma, USA
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Forest Rohwer
gDepartment of Biology, San Diego State University, San Diego, California, USA
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Pavel A. Pevzner
kDepartment of Computer Science and Engineering, University of California San Diego, La Jolla, California, USA
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Robert H. Cichewicz
hNatural Products Discovery Group, Department of Chemistry and Biochemistry, Institute for Natural Products Applications and Research Technologies, Stephenson Life Sciences Research Center, University of Oklahoma, Norman, Oklahoma, USA
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Theodore Alexandrov
aSkaggs School of Pharmacy and Pharmaceutical Sciences, University of California, San Diego, California, USA
fSCiLS GmbH, Bremen, Germany
iEuropean Molecular Biology Laboratory (EMBL), Heidelberg, Germany
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Pieter C. Dorrestein
aSkaggs School of Pharmacy and Pharmaceutical Sciences, University of California, San Diego, California, USA
bDepartment of Chemistry and Biochemistry, University of California, San Diego, California, USA
jCenter for Computational Mass Spectrometry and Department of Computer Science and Engineering, University of California San Diego, La Jolla, California, USA
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Janet K. Jansson
Pacific Northwest National Laboratory
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DOI: 10.1128/mSystems.00139-16
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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.

  • Copyright © 2016 Garg et al.

This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license .

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Spatial Molecular Architecture of the Microbial Community of a Peltigera Lichen
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
mSystems Dec 2016, 1 (6) e00139-16; DOI: 10.1128/mSystems.00139-16

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Spatial Molecular Architecture of the Microbial Community of a Peltigera Lichen
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
mSystems Dec 2016, 1 (6) e00139-16; DOI: 10.1128/mSystems.00139-16
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KEYWORDS

lichen
mass spectrometry
microbial assemblages
natural products
metagenomics

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