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Long-read metagenomics of soil communities reveals phylum-specific secondary metabolite dynamics

Microbial biosynthetic gene clusters (BGCs) encoding secondary metabolites are thought to impact a plethora of biologically mediated environmental processes, yet their discovery and functional characterization in natural microbiomes remains challenging. Here we describe deep long-read sequencing and...

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Autores principales: Van Goethem, Marc W., Osborn, Andrew R., Bowen, Benjamin P., Andeer, Peter F., Swenson, Tami L., Clum, Alicia, Riley, Robert, He, Guifen, Koriabine, Maxim, Sandor, Laura, Yan, Mi, Daum, Chris G., Yoshinaga, Yuko, Makhalanyane, Thulani P., Garcia-Pichel, Ferran, Visel, Axel, Pennacchio, Len A., O’Malley, Ronan C., Northen, Trent R.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8602731/
https://www.ncbi.nlm.nih.gov/pubmed/34795375
http://dx.doi.org/10.1038/s42003-021-02809-4
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author Van Goethem, Marc W.
Osborn, Andrew R.
Bowen, Benjamin P.
Andeer, Peter F.
Swenson, Tami L.
Clum, Alicia
Riley, Robert
He, Guifen
Koriabine, Maxim
Sandor, Laura
Yan, Mi
Daum, Chris G.
Yoshinaga, Yuko
Makhalanyane, Thulani P.
Garcia-Pichel, Ferran
Visel, Axel
Pennacchio, Len A.
O’Malley, Ronan C.
Northen, Trent R.
author_facet Van Goethem, Marc W.
Osborn, Andrew R.
Bowen, Benjamin P.
Andeer, Peter F.
Swenson, Tami L.
Clum, Alicia
Riley, Robert
He, Guifen
Koriabine, Maxim
Sandor, Laura
Yan, Mi
Daum, Chris G.
Yoshinaga, Yuko
Makhalanyane, Thulani P.
Garcia-Pichel, Ferran
Visel, Axel
Pennacchio, Len A.
O’Malley, Ronan C.
Northen, Trent R.
author_sort Van Goethem, Marc W.
collection PubMed
description Microbial biosynthetic gene clusters (BGCs) encoding secondary metabolites are thought to impact a plethora of biologically mediated environmental processes, yet their discovery and functional characterization in natural microbiomes remains challenging. Here we describe deep long-read sequencing and assembly of metagenomes from biological soil crusts, a group of soil communities that are rich in BGCs. Taking advantage of the unusually long assemblies produced by this approach, we recovered nearly 3,000 BGCs for analysis, including 712 full-length BGCs. Functional exploration through metatranscriptome analysis of a 3-day wetting experiment uncovered phylum-specific BGC expression upon activation from dormancy, elucidating distinct roles and complex phylogenetic and temporal dynamics in wetting processes. For example, a pronounced increase in BGC transcription occurs at night primarily in cyanobacteria, implicating BGCs in nutrient scavenging roles and niche competition. Taken together, our results demonstrate that long-read metagenomic sequencing combined with metatranscriptomic analysis provides a direct view into the functional dynamics of BGCs in environmental processes and suggests a central role of secondary metabolites in maintaining phylogenetically conserved niches within biocrusts.
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spelling pubmed-86027312021-12-03 Long-read metagenomics of soil communities reveals phylum-specific secondary metabolite dynamics Van Goethem, Marc W. Osborn, Andrew R. Bowen, Benjamin P. Andeer, Peter F. Swenson, Tami L. Clum, Alicia Riley, Robert He, Guifen Koriabine, Maxim Sandor, Laura Yan, Mi Daum, Chris G. Yoshinaga, Yuko Makhalanyane, Thulani P. Garcia-Pichel, Ferran Visel, Axel Pennacchio, Len A. O’Malley, Ronan C. Northen, Trent R. Commun Biol Article Microbial biosynthetic gene clusters (BGCs) encoding secondary metabolites are thought to impact a plethora of biologically mediated environmental processes, yet their discovery and functional characterization in natural microbiomes remains challenging. Here we describe deep long-read sequencing and assembly of metagenomes from biological soil crusts, a group of soil communities that are rich in BGCs. Taking advantage of the unusually long assemblies produced by this approach, we recovered nearly 3,000 BGCs for analysis, including 712 full-length BGCs. Functional exploration through metatranscriptome analysis of a 3-day wetting experiment uncovered phylum-specific BGC expression upon activation from dormancy, elucidating distinct roles and complex phylogenetic and temporal dynamics in wetting processes. For example, a pronounced increase in BGC transcription occurs at night primarily in cyanobacteria, implicating BGCs in nutrient scavenging roles and niche competition. Taken together, our results demonstrate that long-read metagenomic sequencing combined with metatranscriptomic analysis provides a direct view into the functional dynamics of BGCs in environmental processes and suggests a central role of secondary metabolites in maintaining phylogenetically conserved niches within biocrusts. Nature Publishing Group UK 2021-11-18 /pmc/articles/PMC8602731/ /pubmed/34795375 http://dx.doi.org/10.1038/s42003-021-02809-4 Text en © The Author(s) 2021 https://creativecommons.org/licenses/by/4.0/Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Article
Van Goethem, Marc W.
Osborn, Andrew R.
Bowen, Benjamin P.
Andeer, Peter F.
Swenson, Tami L.
Clum, Alicia
Riley, Robert
He, Guifen
Koriabine, Maxim
Sandor, Laura
Yan, Mi
Daum, Chris G.
Yoshinaga, Yuko
Makhalanyane, Thulani P.
Garcia-Pichel, Ferran
Visel, Axel
Pennacchio, Len A.
O’Malley, Ronan C.
Northen, Trent R.
Long-read metagenomics of soil communities reveals phylum-specific secondary metabolite dynamics
title Long-read metagenomics of soil communities reveals phylum-specific secondary metabolite dynamics
title_full Long-read metagenomics of soil communities reveals phylum-specific secondary metabolite dynamics
title_fullStr Long-read metagenomics of soil communities reveals phylum-specific secondary metabolite dynamics
title_full_unstemmed Long-read metagenomics of soil communities reveals phylum-specific secondary metabolite dynamics
title_short Long-read metagenomics of soil communities reveals phylum-specific secondary metabolite dynamics
title_sort long-read metagenomics of soil communities reveals phylum-specific secondary metabolite dynamics
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8602731/
https://www.ncbi.nlm.nih.gov/pubmed/34795375
http://dx.doi.org/10.1038/s42003-021-02809-4
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