Mapping microhabitats of lignocellulose decomposition by a microbial consortium
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Published:2024-02-01
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ISSN:1552-4450
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Container-title:Nature Chemical Biology
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language:en
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Short-container-title:Nat Chem Biol
Author:
Veličković Marija, Wu RuonanORCID, Gao Yuqian, Thairu Margaret W., Veličković Dušan, Munoz NathalieORCID, Clendinen Chaevien S., Bilbao AivettORCID, Chu Rosalie K.ORCID, Lalli Priscila M., Zemaitis Kevin, Nicora Carrie D.ORCID, Kyle Jennifer E., Orton DanielORCID, Williams Sarai, Zhu YingORCID, Zhao Rui, Monroe Matthew E.ORCID, Moore Ronald J.ORCID, Webb-Robertson Bobbie-Jo M.ORCID, Bramer Lisa M.ORCID, Currie Cameron R.ORCID, Piehowski Paul D.ORCID, Burnum-Johnson Kristin E.ORCID
Abstract
AbstractThe leaf-cutter ant fungal garden ecosystem is a naturally evolved model system for efficient plant biomass degradation. Degradation processes mediated by the symbiotic fungus Leucoagaricus gongylophorus are difficult to characterize due to dynamic metabolisms and spatial complexity of the system. Herein, we performed microscale imaging across 12-µm-thick adjacent sections of Atta cephalotes fungal gardens and applied a metabolome-informed proteome imaging approach to map lignin degradation. This approach combines two spatial multiomics mass spectrometry modalities that enabled us to visualize colocalized metabolites and proteins across and through the fungal garden. Spatially profiled metabolites revealed an accumulation of lignin-related products, outlining morphologically unique lignin microhabitats. Metaproteomic analyses of these microhabitats revealed carbohydrate-degrading enzymes, indicating a prominent fungal role in lignocellulose decomposition. Integration of metabolome-informed proteome imaging data provides a comprehensive view of underlying biological pathways to inform our understanding of metabolic fungal pathways in plant matter degradation within the micrometer-scale environment.
Publisher
Springer Science and Business Media LLC
Subject
Cell Biology,Molecular Biology
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