Biosynthetic potential of the global ocean microbiome

Lucas Paoli, Hans-Joachim Ruscheweyh, Clarissa C. Forneris, Florian Hubrich, Satria Kautsar, Agneya Bhushan, Alessandro Lotti, Quentin Clayssen, Guillem Salazar, Alessio Milanese, Charlotte I. Carlström, Chrysa Papadopoulou, Daniel Gehrig, Mikhail Karasikov, Harun Mustafa, Martin Larralde, Laura M. Carroll, Pablo Sánchez, Ahmed A. Zayed, Dylan R. Cronin, Silvia G. Acinas, Peer Bork, Chris Bowler, Tom O. Delmont, Josep M. Gasol, Alvar D. Gossert, André Kahles, Matthew B. Sullivan, Patrick Wincker, Georg Zeller, Serina L. Robinson (), Jörn Piel () and Shinichi Sunagawa ()
Additional contact information
Lucas Paoli: ETH Zurich
Hans-Joachim Ruscheweyh: ETH Zurich
Clarissa C. Forneris: ETH Zurich
Florian Hubrich: ETH Zurich
Satria Kautsar: Wageningen University
Agneya Bhushan: ETH Zurich
Alessandro Lotti: ETH Zurich
Quentin Clayssen: ETH Zurich
Guillem Salazar: ETH Zurich
Alessio Milanese: ETH Zurich
Charlotte I. Carlström: ETH Zurich
Chrysa Papadopoulou: ETH Zurich
Daniel Gehrig: ETH Zurich
Mikhail Karasikov: ETH Zurich
Harun Mustafa: ETH Zurich
Martin Larralde: European Molecular Biology Laboratory
Laura M. Carroll: European Molecular Biology Laboratory
Pablo Sánchez: Institute of Marine Sciences ICM-CSIC
Ahmed A. Zayed: The Ohio State University
Dylan R. Cronin: The Ohio State University
Silvia G. Acinas: Institute of Marine Sciences ICM-CSIC
Peer Bork: European Molecular Biology Laboratory
Chris Bowler: Université PSL
Tom O. Delmont: Research Federation for the Study of Global Ocean Systems Ecology and Evolution, FR2022/Tara Oceans GOSEE
Josep M. Gasol: Institute of Marine Sciences ICM-CSIC
Alvar D. Gossert: ETH Zurich
André Kahles: ETH Zurich
Matthew B. Sullivan: Institute of Marine Sciences ICM-CSIC
Patrick Wincker: Research Federation for the Study of Global Ocean Systems Ecology and Evolution, FR2022/Tara Oceans GOSEE
Georg Zeller: European Molecular Biology Laboratory
Serina L. Robinson: ETH Zurich
Jörn Piel: ETH Zurich
Shinichi Sunagawa: ETH Zurich

Nature, 2022, vol. 607, issue 7917, 111-118

Abstract: Abstract Natural microbial communities are phylogenetically and metabolically diverse. In addition to underexplored organismal groups1, this diversity encompasses a rich discovery potential for ecologically and biotechnologically relevant enzymes and biochemical compounds2,3. However, studying this diversity to identify genomic pathways for the synthesis of such compounds4 and assigning them to their respective hosts remains challenging. The biosynthetic potential of microorganisms in the open ocean remains largely uncharted owing to limitations in the analysis of genome-resolved data at the global scale. Here we investigated the diversity and novelty of biosynthetic gene clusters in the ocean by integrating around 10,000 microbial genomes from cultivated and single cells with more than 25,000 newly reconstructed draft genomes from more than 1,000 seawater samples. These efforts revealed approximately 40,000 putative mostly new biosynthetic gene clusters, several of which were found in previously unsuspected phylogenetic groups. Among these groups, we identified a lineage rich in biosynthetic gene clusters (‘Candidatus Eudoremicrobiaceae’) that belongs to an uncultivated bacterial phylum and includes some of the most biosynthetically diverse microorganisms in this environment. From these, we characterized the phospeptin and pythonamide pathways, revealing cases of unusual bioactive compound structure and enzymology, respectively. Together, this research demonstrates how microbiomics-driven strategies can enable the investigation of previously undescribed enzymes and natural products in underexplored microbial groups and environments.

Date: 2022
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Citations: View citations in EconPapers (10)

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DOI: 10.1038/s41586-022-04862-3

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