New approaches to secondary metabolite discovery from anaerobic gut microbes

Butkovich, Lazarina V.; Vining, Oliver B.; O’Malley, Michelle A.

doi:10.1007/s00253-024-13393-y

Title: New approaches to secondary metabolite discovery from anaerobic gut microbes

Journal Article · 20 January 2025 · Applied Microbiology and Biotechnology (Online)

DOI: https://doi.org/10.1007/s00253-024-13393-y · OSTI ID:2504027

Butkovich, Lazarina V.; Vining, Oliver B.;

Abstract The animal gut microbiome is a complex system of diverse, predominantly anaerobic microbiota with secondary metabolite potential. These metabolites likely play roles in shaping microbial community membership and influencing animal host health. As such, novel secondary metabolites from gut microbes hold significant biotechnological and therapeutic interest. Despite their potential, gut microbes are largely untapped for secondary metabolites, with gut fungi and obligate anaerobes being particularly under-explored. To advance understanding of these metabolites, culture-based and (meta)genome-based approaches are essential. Culture-based approaches enable isolation, cultivation, and direct study of gut microbes, and (meta)genome-based approaches utilize in silico tools to mine biosynthetic gene clusters (BGCs) from microbes that have not yet been successfully cultured. In this mini-review, we highlight recent innovations in this area, including anaerobic biofoundries like ExFAB, the NSF BioFoundry for Extreme & Exceptional Fungi, Archaea, and Bacteria. These facilities enable high-throughput workflows to study oxygen-sensitive microbes and biosynthetic machinery. Such recent advances promise to improve our understanding of the gut microbiome and its secondary metabolism. Key points • Gut microbial secondary metabolites have therapeutic and biotechnological potential • Culture- and (meta)genome-based workflows drive gut anaerobe metabolite discovery • Anaerobic biofoundries enable high-throughput workflows for metabolite discovery Graphical abstract

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Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER)

Grant/Contract Number:: AC02-05CH11231; SC0020420; SC0022142

OSTI ID:: 2504027

Journal Information:: Applied Microbiology and Biotechnology (Online), Journal Name: Applied Microbiology and Biotechnology (Online) Journal Issue: 1 Vol. 109; ISSN 1432-0614

Publisher:: Springer Science + Business MediaCopyright Statement

Country of Publication:: Germany

Language:: English

References (132)

Big Effects from Small Changes: Possible Ways to Explore Nature's Chemical Diversity Bode, Helge Björn; Bethe, Barbara; Höfs, Regina ChemBioChem, Vol. 3, Issue 7 https://doi.org/10.1002/1439-7633(20020703)3:7<619::AID-CBIC619>3.0.CO;2-9	journal	July 2002
Closthioamide: An Unprecedented Polythioamide Antibiotic from the Strictly Anaerobic Bacterium Clostridium cellulolyticum Lincke, Thorger; Behnken, Swantje; Ishida, Keishi Angewandte Chemie, Vol. 122, Issue 11 https://doi.org/10.1002/ange.200906114	journal	February 2010
Discovery of Clostrubin, an Exceptional Polyphenolic Polyketide Antibiotic from a Strictly Anaerobic Bacterium Pidot, Sacha; Ishida, Keishi; Cyrulies, Michael Angewandte Chemie, Vol. 126, Issue 30 https://doi.org/10.1002/ange.201402632	journal	May 2014
Biosynthesis of the Enterotoxic Pyrrolobenzodiazepine Natural Product Tilivalline Dornisch, Elisabeth; Pletz, Jakob; Glabonjat, Ronald A. Angewandte Chemie International Edition, Vol. 56, Issue 46 https://doi.org/10.1002/anie.201707737	journal	October 2017
Unlocking Nature's Biosynthetic Power—Metabolic Engineering for the Fermentative Production of Chemicals Hoff, Birgit; Plassmeier, Jens; Blankschien, Matthew Angewandte Chemie International Edition, Vol. 60, Issue 5 https://doi.org/10.1002/anie.202004248	journal	October 2020
Single‐cell microliter‐droplet screening system (MISS Cell): An integrated platform for automated high‐throughput microbial monoclonal cultivation and picking Jian, Xingjin; Guo, Xiaojie; Cai, Zhengshuo Biotechnology and Bioengineering, Vol. 120, Issue 3 https://doi.org/10.1002/bit.28300	journal	December 2022
An efficient cre‐based workflow for genomic integration and expression of large biosynthetic pathways in Eubacterium limosum Sanford, Patrick A.; Blaby, Ian; Yoshikuni, Yasuo Biotechnology and Bioengineering, Vol. 121, Issue 10 https://doi.org/10.1002/bit.28796	journal	July 2024
Induced Production, Synthesis, and Immunomodulatory Action of Clostrisulfone, a Diarylsulfone from Clostridium acetobutylicum Neuwirth, Toni; Letzel, Anne‐Catrin; Tank, Cedric Chemistry – A European Journal, Vol. 26, Issue 68 https://doi.org/10.1002/chem.202003500	journal	November 2020
Principles of Enrichment, Isolation, Cultivation, and Preservation of Prokaryotes Overmann, Jörg The Prokaryotes https://doi.org/10.1007/978-3-642-30194-0_7	book	January 2013
Antimicrobial secondary metabolites from agriculturally important bacteria as next-generation pesticides Keswani, Chetan; Singh, Harikesh B.; García-Estrada, Carlos Applied Microbiology and Biotechnology, Vol. 104, Issue 3 https://doi.org/10.1007/s00253-019-10300-8	journal	December 2019
Gut bacteria of animals living in polluted environments exhibit broad-spectrum antibacterial activities Akbar, Noor; Siddiqui, Ruqaiyyah; Sagathevan, K. International Microbiology, Vol. 23, Issue 4 https://doi.org/10.1007/s10123-020-00123-3	journal	March 2020
Co-cultivation of the anaerobic fungus Anaeromyces robustus with Methanobacterium bryantii enhances transcription of carbohydrate active enzymes Swift, Candice L.; Brown, Jennifer L.; Seppälä, Susanna Journal of Industrial Microbiology & Biotechnology, Vol. 46, Issue 9-10 https://doi.org/10.1007/s10295-019-02188-0	journal	May 2019
Frontier studies on natural products: moving toward paradigm shifts Zhao, Jin-Xin; Yue, Jian-Min Science China Chemistry, Vol. 66, Issue 4 https://doi.org/10.1007/s11426-022-1512-0	journal	January 2023
Chemical communication in the gut: Effects of microbiota-generated metabolites on gastrointestinal bacterial pathogens Vogt, Stefanie L.; Peña-Díaz, Jorge; Finlay, B. Brett Anaerobe, Vol. 34 https://doi.org/10.1016/j.anaerobe.2015.05.002	journal	August 2015
The role of gut microbiota in health and disease: In vitro modeling of host-microbe interactions at the aerobe-anaerobe interphase of the human gut von Martels, Julius Z. H.; Sadaghian Sadabad, Mehdi; Bourgonje, Arno R. Anaerobe, Vol. 44 https://doi.org/10.1016/j.anaerobe.2017.01.001	journal	April 2017
Biosynthesis of lovastatin and (+)-geodin by Aspergillus terreus in batch and fed-batch culture in the stirred tank bioreactor Bizukojc, Marcin; Ledakowicz, Stanislaw Biochemical Engineering Journal, Vol. 42, Issue 3 https://doi.org/10.1016/j.bej.2008.06.022	journal	December 2008
Aeration costs in stirred-tank and bubble column bioreactors Humbird, D.; Davis, R.; McMillan, J. D. Biochemical Engineering Journal, Vol. 127 https://doi.org/10.1016/j.bej.2017.08.006	journal	November 2017
Lovastatin production: From molecular basis to industrial process optimization Mulder, Kelly C. L.; Mulinari, Flávia; Franco, Octávio L. Biotechnology Advances, Vol. 33, Issue 6 https://doi.org/10.1016/j.biotechadv.2015.04.001	journal	November 2015
Synthetic biology-inspired strategies and tools for engineering of microbial natural product biosynthetic pathways Alam, Khorshed; Hao, Jinfang; Zhang, Youming Biotechnology Advances, Vol. 49 https://doi.org/10.1016/j.biotechadv.2021.107759	journal	July 2021
Accessing hidden microbial biosynthetic potential from underexplored sources for novel drug discovery Li, Lei Biotechnology Advances, Vol. 66 https://doi.org/10.1016/j.biotechadv.2023.108176	journal	September 2023
Role of oxygen gradients in shaping redox relationships between the human intestine and its microbiota Espey, Michael Graham Free Radical Biology and Medicine, Vol. 55 https://doi.org/10.1016/j.freeradbiomed.2012.10.554	journal	February 2013
The Natural Product Domain Seeker version 2 (NaPDoS2) webtool relates ketosynthase phylogeny to biosynthetic function Klau, Leesa J.; Podell, Sheila; Creamer, Kaitlin E. Journal of Biological Chemistry, Vol. 298, Issue 10 https://doi.org/10.1016/j.jbc.2022.102480	journal	October 2022
RiPPMiner-Genome: A Web Resource for Automated Prediction of Crosslinked Chemical Structures of RiPPs by Genome Mining Agrawal, Priyesh; Amir, Sana Journal of Molecular Biology, Vol. 433, Issue 11 https://doi.org/10.1016/j.jmb.2021.166887	journal	May 2021
The phenomenon of microbial uncultivability Epstein, Ss Current Opinion in Microbiology, Vol. 16, Issue 5 https://doi.org/10.1016/j.mib.2013.08.003	journal	October 2013
A method to analyze, sort, and retain viability of obligate anaerobic microorganisms from complex microbial communities Thompson, Anne W.; Crow, Matthew J.; Wadey, Brian Journal of Microbiological Methods, Vol. 117 https://doi.org/10.1016/j.mimet.2015.07.009	journal	October 2015
Automating the design-build-test-learn cycle towards next-generation bacterial cell factories Gurdo, Nicolás; Volke, Daniel C.; McCloskey, Douglas New Biotechnology, Vol. 74 https://doi.org/10.1016/j.nbt.2023.01.002	journal	May 2023
The unsung roles of microbial secondary metabolite effectors in the plant disease cacophony Rangel, Lorena I.; Bolton, Melvin D. Current Opinion in Plant Biology, Vol. 68 https://doi.org/10.1016/j.pbi.2022.102233	journal	August 2022
A review of technologies for in-situ sulfide control in anaerobic digestion Jung, Heejung; Kim, Danbee; Choi, Hyungmin Renewable and Sustainable Energy Reviews, Vol. 157 https://doi.org/10.1016/j.rser.2021.112068	journal	April 2022
Practical guide on MALDI-TOF MS method development for high throughput profiling of pharmaceutically relevant, small molecule chemical reactions Blincoe, William D.; Lin, Shishi; Dreher, Spencer D. Tetrahedron, Vol. 76, Issue 36 https://doi.org/10.1016/j.tet.2020.131434	journal	September 2020
Microbial production of bulk chemicals: development of anaerobic processes Weusthuis, Ruud A.; Lamot, Ischa; van der Oost, John Trends in Biotechnology, Vol. 29, Issue 4 https://doi.org/10.1016/j.tibtech.2010.12.007	journal	April 2011
Thermodynamics-based design of microbial cell factories for anaerobic product formation Cueto-Rojas, Hugo F.; van Maris, A. J. A.; Wahl, S. Aljoscha Trends in Biotechnology, Vol. 33, Issue 9 https://doi.org/10.1016/j.tibtech.2015.06.010	journal	September 2015
Natural Products from Mammalian Gut Microbiota Wang, Leli; Ravichandran, Vinothkannan; Yin, Yulong Trends in Biotechnology, Vol. 37, Issue 5 https://doi.org/10.1016/j.tibtech.2018.10.003	journal	May 2019
Development of a clostridia-based cell-free system for prototyping genetic parts and metabolic pathways Krüger, Antje; Mueller, Alexander P.; Rybnicky, Grant A. Metabolic Engineering, Vol. 62 https://doi.org/10.1016/j.ymben.2020.06.004	journal	November 2020
Automated engineering of synthetic metabolic pathways for efficient biomanufacturing Otero-Muras, Irene; Carbonell, Pablo Metabolic Engineering, Vol. 63 https://doi.org/10.1016/j.ymben.2020.11.012	journal	January 2021
Metabolic engineering of commensal bacteria for gut butyrate delivery and dissection of host-microbe interaction Gong, Xu; Geng, Hongwei; Yang, Yun Metabolic Engineering, Vol. 80 https://doi.org/10.1016/j.ymben.2023.09.008	journal	November 2023
Acoustic Ejection Mass Spectrometry for High-Throughput Analysis Zhang, Hui; Liu, Chang; Hua, Wenyi Analytical Chemistry, Vol. 93, Issue 31 https://doi.org/10.1021/acs.analchem.1c01137	journal	July 2021
Ozone Decontamination of Medical and Nonmedical Devices: An Assessment of Design and Implementation Considerations Epelle, Emmanuel I.; Macfarlane, Andrew; Cusack, Michael Industrial & Engineering Chemistry Research, Vol. 62, Issue 10 https://doi.org/10.1021/acs.iecr.2c03754	journal	March 2023
Natural Products as Sources of New Drugs over the Nearly Four Decades from 01/1981 to 09/2019 Newman, David J.; Cragg, Gordon M. Journal of Natural Products, Vol. 83, Issue 3 https://doi.org/10.1021/acs.jnatprod.9b01285	journal	March 2020
AutoBioTech─A Versatile Biofoundry for Automated Strain Engineering Rosch, Tobias Michael; Tenhaef, Julia; Stoltmann, Tim ACS Synthetic Biology, Vol. 13, Issue 7 https://doi.org/10.1021/acssynbio.4c00298	journal	July 2024
Top-Down Enrichment Guides in Formation of Synthetic Microbial Consortia for Biomass Degradation Gilmore, Sean P.; Lankiewicz, Thomas S.; Wilken, St. Elmo ACS Synthetic Biology, Vol. 8, Issue 9 https://doi.org/10.1021/acssynbio.9b00271	journal	August 2019
Towards a new science of secondary metabolism Craney, Arryn; Ahmed, Salman; Nodwell, Justin The Journal of Antibiotics, Vol. 66, Issue 7 https://doi.org/10.1038/ja.2013.25	journal	April 2013
Production of the antimalarial drug precursor artemisinic acid in engineered yeast Ro, Dae-Kyun; Paradise, Eric M.; Ouellet, Mario Nature, Vol. 440, Issue 7086, p. 940-943 https://doi.org/10.1038/nature04640	journal	April 2006
A framework for human microbiome research Nature, Vol. 486, Issue 7402, p. 215-221 https://doi.org/10.1038/nature11209	journal	June 2012
Structure, function and diversity of the healthy human microbiome Nature, Vol. 486, Issue 7402, p. 207-214 https://doi.org/10.1038/nature11234	journal	June 2012
A metagenome-wide association study of gut microbiota in type 2 diabetes Qin, Junjie; Li, Yingrui; Cai, Zhiming Nature, Vol. 490, Issue 7418 https://doi.org/10.1038/nature11450	journal	September 2012
Cultivation and sequencing of rumen microbiome members from the Hungate1000 Collection Seshadri, Rekha; Leahy, Sinead C.; Attwood, Graeme T. Nature Biotechnology, Vol. 36, Issue 4 https://doi.org/10.1038/nbt.4110	journal	March 2018
Microbial metabolic exchange—the chemotype-to-phenotype link Phelan, Vanessa V.; Liu, Wei-Ting; Pogliano, Kit Nature Chemical Biology, Vol. 8, Issue 1 https://doi.org/10.1038/nchembio.739	journal	December 2011
Symptomatic atherosclerosis is associated with an altered gut metagenome Karlsson, Fredrik H.; Fåk, Frida; Nookaew, Intawat Nature Communications, Vol. 3, Issue 1 https://doi.org/10.1038/ncomms2266	journal	January 2012
Current understanding of the human microbiome Gilbert, Jack A.; Blaser, Martin J.; Caporaso, J. Gregory Nature Medicine, Vol. 24, Issue 4 https://doi.org/10.1038/nm.4517	journal	April 2018
Semi-synthetic artemisinin: a model for the use of synthetic biology in pharmaceutical development Paddon, Chris J.; Keasling, Jay D. Nature Reviews Microbiology, Vol. 12, Issue 5 https://doi.org/10.1038/nrmicro3240	journal	April 2014
Gut microbiota-derived metabolites in the regulation of host immune responses and immune-related inflammatory diseases Yang, Wenjing; Cong, Yingzi Cellular & Molecular Immunology, Vol. 18, Issue 4 https://doi.org/10.1038/s41423-021-00661-4	journal	March 2021
Discovery of antifungal secondary metabolites from an intestinal fungus Fusarium sp. Zhang, Mingkai; Chen, Baosong; Dai, Huanqin The Journal of Antibiotics, Vol. 77, Issue 3 https://doi.org/10.1038/s41429-023-00692-1	journal	December 2023
Building a global alliance of biofoundries Hillson, Nathan; Caddick, Mark; Cai, Yizhi Nature Communications, Vol. 10, Issue 1 https://doi.org/10.1038/s41467-019-10079-2	journal	May 2019
An anaerobic bacterium host system for heterologous expression of natural product biosynthetic gene clusters Hao, Tingting; Xie, Zhoujie; Wang, Min Nature Communications, Vol. 10, Issue 1 https://doi.org/10.1038/s41467-019-11673-0	journal	August 2019
Comprehensive prediction of secondary metabolite structure and biological activity from microbial genome sequences Skinnider, Michael A.; Johnston, Chad W.; Gunabalasingam, Mathusan Nature Communications, Vol. 11, Issue 1 https://doi.org/10.1038/s41467-020-19986-1	journal	November 2020
A versatile genetic engineering toolkit for E. coli based on CRISPR-prime editing Tong, Yaojun; Jørgensen, Tue S.; Whitford, Christopher M. Nature Communications, Vol. 12, Issue 1 https://doi.org/10.1038/s41467-021-25541-3	journal	September 2021
Microbial production of advanced biofuels Keasling, Jay; Garcia Martin, Hector; Lee, Taek Soon Nature Reviews Microbiology, Vol. 19, Issue 11 https://doi.org/10.1038/s41579-021-00577-w	journal	June 2021
When anaerobes encounter oxygen: mechanisms of oxygen toxicity, tolerance and defence Lu, Zheng; Imlay, James A. Nature Reviews Microbiology, Vol. 19, Issue 12 https://doi.org/10.1038/s41579-021-00583-y	journal	June 2021
The gut microbiota and its biogeography McCallum, Giselle; Tropini, Carolina Nature Reviews Microbiology, Vol. 22, Issue 2 https://doi.org/10.1038/s41579-023-00969-0	journal	September 2023
Identification of bioactive metabolites using activity metabolomics Rinschen, Markus M.; Ivanisevic, Julijana; Giera, Martin Nature Reviews Molecular Cell Biology, Vol. 20, Issue 6 https://doi.org/10.1038/s41580-019-0108-4	journal	February 2019
The Integrative Human Microbiome Project Consortium, iHMP Nature, Vol. 569, Issue 7758, p. 641-648 https://doi.org/10.1038/s41586-019-1238-8	journal	May 2019
A unified catalog of 204,938 reference genomes from the human gut microbiome Almeida, Alexandre; Nayfach, Stephen; Boland, Miguel Nature Biotechnology, Vol. 39, Issue 1 https://doi.org/10.1038/s41587-020-0603-3	journal	July 2020
Identification of antimicrobial peptides from the human gut microbiome using deep learning Ma, Yue; Guo, Zhengyan; Xia, Binbin Nature Biotechnology, Vol. 40, Issue 6 https://doi.org/10.1038/s41587-022-01226-0	journal	March 2022
High-throughput microbial culturomics using automation and machine learning Huang, Yiming; Sheth, Ravi U.; Zhao, Shijie Nature Biotechnology, Vol. 41, Issue 10 https://doi.org/10.1038/s41587-023-01674-2	journal	February 2023
gutSMASH predicts specialized primary metabolic pathways from the human gut microbiota Pascal Andreu, Victòria; Augustijn, Hannah E.; Chen, Lianmin Nature Biotechnology, Vol. 41, Issue 10 https://doi.org/10.1038/s41587-023-01675-1	journal	February 2023
Scalable, compressed phenotypic screening using pooled perturbations Liu, Nuo; Kattan, Walaa E.; Mead, Benjamin E. Nature Biotechnology https://doi.org/10.1038/s41587-024-02403-z	journal	October 2024
A genetics-free method for high-throughput discovery of cryptic microbial metabolites Xu, Fei; Wu, Yihan; Zhang, Chen Nature Chemical Biology, Vol. 15, Issue 2 https://doi.org/10.1038/s41589-018-0193-2	journal	January 2019
Prospecting for natural products by genome mining and microcrystal electron diffraction Kim, Lee Joon; Ohashi, Masao; Zhang, Zhuan Nature Chemical Biology, Vol. 17, Issue 8 https://doi.org/10.1038/s41589-021-00834-2	journal	July 2021
Machine learning-powered antibiotics phenotypic drug discovery Zoffmann, Sannah; Vercruysse, Maarten; Benmansour, Fethallah Scientific Reports, Vol. 9, Issue 1 https://doi.org/10.1038/s41598-019-39387-9	journal	March 2019
The human microbial exposome: expanding the Exposome-Explorer database with gut microbial metabolites Neveu, Vanessa; Nicolas, Geneviève; Amara, Adam Scientific Reports, Vol. 13, Issue 1 https://doi.org/10.1038/s41598-022-26366-w	journal	February 2023
A genomic approach to the cryptic secondary metabolome of the anaerobic world Letzel, Anne-Catrin; Pidot, Sacha J.; Hertweck, Christian Nat. Prod. Rep., Vol. 30, Issue 3 https://doi.org/10.1039/C2NP20103H	journal	January 2013
Connecting metabolome and phenotype: recent advances in functional metabolomics tools for the identification of bioactive natural products Vitale, Giovanni Andrea; Geibel, Christian; Minda, Vidit Natural Product Reports, Vol. 41, Issue 6 https://doi.org/10.1039/D3NP00050H	journal	January 2024
SlipChip Du, Wenbin; Li, Liang; Nichols, Kevin P. Lab on a Chip, Vol. 9, Issue 16 https://doi.org/10.1039/b908978k	journal	January 2009
Clostrindolin is an antimycobacterial pyrone alkaloid from Clostridium beijerinckii Schieferdecker, Sebastian; Shabuer, Gulimila; Knuepfer, Uwe Organic & Biomolecular Chemistry, Vol. 17, Issue 25 https://doi.org/10.1039/c9ob00968j	journal	January 2019
Molecular-phylogenetic characterization of microbial community imbalances in human inflammatory bowel diseases Frank, D. N.; St. Amand, A. L.; Feldman, R. A. Proceedings of the National Academy of Sciences, Vol. 104, Issue 34, p. 13780-13785 https://doi.org/10.1073/pnas.0706625104	journal	August 2007
Microbes vs. chemistry in the origin of the anaerobic gut lumen Friedman, Elliot S.; Bittinger, Kyle; Esipova, Tatiana V. Proceedings of the National Academy of Sciences, Vol. 115, Issue 16 https://doi.org/10.1073/pnas.1718635115	journal	April 2018
Anaerobic gut fungi are an untapped reservoir of natural products Swift, Candice L.; Louie, Katherine B.; Bowen, Benjamin P. Proceedings of the National Academy of Sciences, Vol. 118, Issue 18 https://doi.org/10.1073/pnas.2019855118	journal	April 2021
Microbiome composition modulates secondary metabolism in a multispecies bacterial community Chevrette, Marc G.; Thomas, Chris S.; Hurley, Amanda Proceedings of the National Academy of Sciences, Vol. 119, Issue 42 https://doi.org/10.1073/pnas.2212930119	journal	October 2022
Gut dysbiosis: Ecological causes and causative effects on human disease Winter, Sebastian E.; Bäumler, Andreas J. Proceedings of the National Academy of Sciences, Vol. 120, Issue 50 https://doi.org/10.1073/pnas.2316579120	journal	December 2023
Recent advances in genome mining and synthetic biology for discovery and biosynthesis of natural products Wang, Mingpeng; Chen, Lei; Zhang, Zhaojie Critical Reviews in Biotechnology, Vol. 45, Issue 1 https://doi.org/10.1080/07388551.2024.2383754	journal	August 2024
Gut microbiota as a source of novel antimicrobials Garcia-Gutierrez, Enriqueta; Mayer, Melinda J.; Cotter, Paul D. Gut Microbes, Vol. 10, Issue 1 https://doi.org/10.1080/19490976.2018.1455790	journal	May 2018
The protective role of commensal gut microbes and their metabolites against bacterial pathogens Cheng, Liqin; Correia, Mário S. P.; Higdon, Shawn M. Gut Microbes, Vol. 16, Issue 1 https://doi.org/10.1080/19490976.2024.2356275	journal	May 2024
Streptomyces, shared microbiome member of soil and gut, as ‘old friends’ against colon cancer Bolourian, Alireza; Mojtahedi, Zahra FEMS Microbiology Ecology, Vol. 94, Issue 8 https://doi.org/10.1093/FEMSEC/FIY120	journal	June 2018
sBGC-hm: an atlas of secondary metabolite biosynthetic gene clusters from the human gut microbiome Zou, Huixi; Sun, Tianli; Jin, Bangqun Bioinformatics, Vol. 39, Issue 3 https://doi.org/10.1093/bioinformatics/btad131	journal	March 2023
ARTS 2.0: feature updates and expansion of the Antibiotic Resistant Target Seeker for comparative genome mining Mungan, Mehmet Direnç; Alanjary, Mohammad; Blin, Kai Nucleic Acids Research, Vol. 48, Issue W1 https://doi.org/10.1093/nar/gkaa374	journal	May 2020
BiG-FAM: the biosynthetic gene cluster families database Kautsar, Satria A.; Blin, Kai; Shaw, Simon Nucleic Acids Research, Vol. 49, Issue D1 https://doi.org/10.1093/nar/gkaa812	journal	October 2020
AMDB: a database of animal gut microbial communities with manually curated metadata Yang, Junwon; Park, Jonghyun; Jung, Yeonjae Nucleic Acids Research, Vol. 50, Issue D1 https://doi.org/10.1093/nar/gkab1009	journal	November 2021
MIBiG 3.0: a community-driven effort to annotate experimentally validated biosynthetic gene clusters Terlouw, Barbara R.; Blin, Kai; Navarro-Muñoz, Jorge C. Nucleic Acids Research, Vol. 51, Issue D1 https://doi.org/10.1093/nar/gkac1049	journal	November 2022
Activating natural product synthesis using CRISPR interference and activation systems in Streptomyces Ameruoso, Andrea; Villegas Kcam, Maria Claudia; Cohen, Katherine Piper Nucleic Acids Research, Vol. 50, Issue 13 https://doi.org/10.1093/nar/gkac556	journal	July 2022
antiSMASH 7.0: new and improved predictions for detection, regulation, chemical structures and visualisation Blin, Kai; Shaw, Simon; Augustijn, Hannah E. Nucleic Acids Research, Vol. 51, Issue W1 https://doi.org/10.1093/nar/gkad344	journal	May 2023
Building a biofoundry Holowko, Maciej B.; Frow, Emma K.; Reid, Janet C. Synthetic Biology, Vol. 6, Issue 1 https://doi.org/10.1093/synbio/ysaa026	journal	December 2020
The role of animal hosts in shaping gut microbiome variation Maritan, Elisa; Quagliariello, Andrea; Frago, Enric Philosophical Transactions of the Royal Society B: Biological Sciences, Vol. 379, Issue 1901 https://doi.org/10.1098/rstb.2023.0071	journal	March 2024
Discovery of a novel lantibiotic nisin O from Blautia obeum A2-162, isolated from the human gastrointestinal tract Hatziioanou, Diane; Gherghisan-Filip, Cristina; Saalbach, Gerhard Microbiology, Vol. 163, Issue 9 https://doi.org/10.1099/mic.0.000515	journal	September 2017
An Evaluation of the Gaspak System in the Culture of Anaerobic Bacteria Collee, J. G.; Watt, B.; Fowler, Elizabeth B. Journal of Applied Bacteriology, Vol. 35, Issue 1 https://doi.org/10.1111/j.1365-2672.1972.tb03675.x	journal	March 1972
Biofilm-growing intestinal anaerobic bacteria Donelli, Gianfranco; Vuotto, Claudia; Cardines, Rita FEMS Immunology & Medical Microbiology, Vol. 65, Issue 2 https://doi.org/10.1111/j.1574-695X.2012.00962.x	journal	July 2012
Glycan Foraging in Vivo by an Intestine-Adapted Bacterial Symbiont Sonnenburg, J. L. Science, Vol. 307, Issue 5717 https://doi.org/10.1126/science.1109051	journal	March 2005
Small molecules from the human microbiota Donia, M. S.; Fischbach, M. A. Science, Vol. 349, Issue 6246 https://doi.org/10.1126/science.1254766	journal	July 2015
A metagenomic strategy for harnessing the chemical repertoire of the human microbiome Sugimoto, Yuki; Camacho, Francine R.; Wang, Shuo Science, Vol. 366, Issue 6471 https://doi.org/10.1126/science.aax9176	journal	October 2019
Evaluation of the AnaeroPack system for growth of clinically significant anaerobes Delaney, M. L.; Onderdonk, A. B. Journal of Clinical Microbiology, Vol. 35, Issue 3 https://doi.org/10.1128/jcm.35.3.558-562.1997	journal	March 1997
Broad-Host-Range Expression Reveals Native and Host Regulatory Elements That Influence Heterologous Antibiotic Production in Gram-Negative Bacteria Zhang, Jia Jia; Tang, Xiaoyu; Zhang, Michelle mBio, Vol. 8, Issue 5 https://doi.org/10.1128/mBio.01291-17	journal	September 2017
Cocultivation of Anaerobic Fungi with Rumen Bacteria Establishes an Antagonistic Relationship Swift, Candice L.; Louie, Katherine B.; Bowen, Benjamin P. mBio, Vol. 12, Issue 4 https://doi.org/10.1128/mbio.01442-21	journal	August 2021
TaxiBGC: a Taxonomy-Guided Approach for Profiling Experimentally Characterized Microbial Biosynthetic Gene Clusters and Secondary Metabolite Production Potential in Metagenomes Gupta, Vinod K.; Bakshi, Utpal; Chang, Daniel mSystems, Vol. 7, Issue 6 https://doi.org/10.1128/msystems.00925-22	journal	December 2022
International Cancer Microbiome Consortium consensus statement on the role of the human microbiome in carcinogenesis Scott, Alasdair J.; Alexander, James L.; Merrifield, Claire A. Gut, Vol. 68, Issue 9 https://doi.org/10.1136/gutjnl-2019-318556	journal	May 2019
A Natural Product Chemist's Guide to Unlocking Silent Biosynthetic Gene Clusters Covington, Brett C.; Xu, Fei; Seyedsayamdost, Mohammad R. Annual Review of Biochemistry, Vol. 90, Issue 1 https://doi.org/10.1146/annurev-biochem-081420-102432	journal	June 2021
A convenient and versatile culturomics platform to expand the human gut culturome of Lachnospiraceae and Oscillospiraceae Plomp, N.; Liu, L.; Walters, L. Beneficial Microbes, Vol. 16, Issue 1 https://doi.org/10.1163/18762891-bja00042	journal	October 2024
Automated High-Throughput System Combining Small-Scale Synthesis with Bioassays and Reaction Screening Morato, Nicolás M.; Le, MyPhuong T.; Holden, Dylan T. SLAS Technology, Vol. 26, Issue 6 https://doi.org/10.1177/24726303211047839	journal	December 2021
Genome mining for ribosomally synthesized and post-translationally modified peptides (RiPPs) in anaerobic bacteria Letzel, Anne-Catrin; Pidot, Sacha J.; Hertweck, Christian BMC Genomics, Vol. 15, Issue 1 https://doi.org/10.1186/1471-2164-15-983	journal	January 2014
Metabolic engineering of Clostridium ljungdahlii for the production of hexanol and butanol from CO2 and H2 Lauer, Ira; Philipps, Gabriele; Jennewein, Stefan Microbial Cell Factories, Vol. 21, Issue 1 https://doi.org/10.1186/s12934-022-01802-8	journal	May 2022
Human reference gut microbiome catalog including newly assembled genomes from under-represented Asian metagenomes Kim, Chan Yeong; Lee, Muyoung; Yang, Sunmo Genome Medicine, Vol. 13, Issue 1 https://doi.org/10.1186/s13073-021-00950-7	journal	August 2021
UmetaFlow: an untargeted metabolomics workflow for high-throughput data processing and analysis Kontou, Eftychia E.; Walter, Axel; Alka, Oliver Journal of Cheminformatics, Vol. 15, Issue 1 https://doi.org/10.1186/s13321-023-00724-w	journal	May 2023
Stress and defense responses in plant secondary metabolites production Isah, Tasiu Biological Research, Vol. 52, Issue 1 https://doi.org/10.1186/s40659-019-0246-3	journal	July 2019
Advances in the isolation, cultivation, and identification of gut microbes Xu, Meng-Qi; Pan, Fei; Peng, Li-Hua Military Medical Research, Vol. 11, Issue 1 https://doi.org/10.1186/s40779-024-00534-7	journal	June 2024
Revised Estimates for the Number of Human and Bacteria Cells in the Body Sender, Ron; Fuchs, Shai; Milo, Ron PLOS Biology, Vol. 14, Issue 8 https://doi.org/10.1371/journal.pbio.1002533	journal	August 2016
A design of experiments approach for the rapid formulation of a chemically defined medium for metabolic profiling of industrially important microbes Singleton, Chloe; Gilman, James; Rollit, Jessica PLOS ONE, Vol. 14, Issue 6 https://doi.org/10.1371/journal.pone.0218208	journal	June 2019
Expression of biosynthetic gene clusters in heterologous hosts for natural product production and combinatorial biosynthesis Galm, Ute; Shen, Ben Expert Opinion on Drug Discovery, Vol. 1, Issue 5 https://doi.org/10.1517/17460441.1.5.409	journal	October 2006
Advances in high‐throughput mass spectrometry in drug discovery Dueñas, Maria Emilia; Peltier‐Heap, Rachel E.; Leveridge, Melanie EMBO Molecular Medicine, Vol. 15, Issue 1 https://doi.org/10.15252/emmm.202114850	journal	December 2022
Phylogenomic Analyses of Non-Dikarya Fungi Supports Horizontal Gene Transfer Driving Diversification of Secondary Metabolism in the Amphibian Gastrointestinal Symbiont, Basidiobolus Tabima, Javier F.; Trautman, Ian A.; Chang, Ying G3 Genes\|Genomes\|Genetics, Vol. 10, Issue 9 https://doi.org/10.1534/g3.120.401516	journal	September 2020
Mass Spectrometric Analysis of Bioactive Conditioned Media of Bacteria Isolated From Reptilian Gut Siddiqui, Ruqaiyyah; Akbar, Noor; Soares, Nelson Cruz Future Science OA, Vol. 9, Issue 5 https://doi.org/10.2144/fsoa-2023-0030	journal	May 2023
Engineered acetogenic bacteria as microbial cell factory for diversified biochemicals Zhang, Jun-Zhe; Li, Yu-Zhen; Xi, Zhi-Ning Frontiers in Bioengineering and Biotechnology, Vol. 12 https://doi.org/10.3389/fbioe.2024.1395540	journal	July 2024
Gas Fermentation—A Flexible Platform for Commercial Scale Production of Low-Carbon-Fuels and Chemicals from Waste and Renewable Feedstocks Liew, FungMin; Martin, Michael E.; Tappel, Ryan C. Frontiers in Microbiology, Vol. 7 https://doi.org/10.3389/fmicb.2016.00694	journal	May 2016
Fungal and Bacterial Pigments: Secondary Metabolites with Wide Applications Narsing Rao, Manik Prabhu; Xiao, Min; Li, Wen-Jun Frontiers in Microbiology, Vol. 8 https://doi.org/10.3389/fmicb.2017.01113	journal	June 2017
Exploring Structural Diversity of Microbe Secondary Metabolites Using OSMAC Strategy: A Literature Review Pan, Rui; Bai, Xuelian; Chen, Jianwei Frontiers in Microbiology, Vol. 10 https://doi.org/10.3389/fmicb.2019.00294	journal	February 2019
Enhancing chemical and biological diversity by co-cultivation Selegato, Denise M.; Castro-Gamboa, Ian Frontiers in Microbiology, Vol. 14 https://doi.org/10.3389/fmicb.2023.1117559	journal	February 2023
Untargeted MS-Based Metabolomic Analysis of Termite Gut-Associated Streptomycetes with Antifungal Activity against Pyrrhoderma noxium Adra, Cherrihan; Tran, Trong D.; Foster, Keith Antibiotics, Vol. 12, Issue 9 https://doi.org/10.3390/antibiotics12091373	journal	August 2023
Links between Diet, Intestinal Anaerobes, Microbial Metabolites and Health Duncan, Sylvia H.; Conti, Elena; Ricci, Liviana Biomedicines, Vol. 11, Issue 5 https://doi.org/10.3390/biomedicines11051338	journal	May 2023
Ligiamycins A and B, Decalin-Amino-Maleimides from the Co-Culture of Streptomyces sp. and Achromobacter sp. Isolated from the Marine Wharf Roach, Ligia exotica Lim, Hyung-Ju; An, Joon Soo; Bae, Eun Seo Marine Drugs, Vol. 20, Issue 2 https://doi.org/10.3390/md20020083	journal	January 2022
Advanced Methods for Natural Products Discovery: Bioactivity Screening, Dereplication, Metabolomics Profiling, Genomic Sequencing, Databases and Informatic Tools, and Structure Elucidation Gaudêncio, Susana P.; Bayram, Engin; Lukić Bilela, Lada Marine Drugs, Vol. 21, Issue 5 https://doi.org/10.3390/md21050308	journal	May 2023
Proteobacteria Overgrowth and Butyrate-Producing Taxa Depletion in the Gut Microbiota of Glycogen Storage Disease Type 1 Patients Ceccarani, Camilla; Bassanini, Giulia; Montanari, Chiara Metabolites, Vol. 10, Issue 4 https://doi.org/10.3390/metabo10040133	journal	March 2020
Pentaminomycins C–E: Cyclic Pentapeptides as Autophagy Inducers from a Mealworm Beetle Gut Bacterium Hwang, Sunghoon; Le, Ly Thi Huong Luu; Jo, Shin-Il Microorganisms, Vol. 8, Issue 9 https://doi.org/10.3390/microorganisms8091390	journal	September 2020
Terpenes and Terpenoids: Building Blocks to Produce Biopolymers Mosquera, Marta. E. G.; Jiménez, Gerardo; Tabernero, Vanessa Sustainable Chemistry, Vol. 2, Issue 3 https://doi.org/10.3390/suschem2030026	journal	August 2021
Medium Preparation for the Cultivation of Microorganisms under Strictly Anaerobic/Anoxic Conditions Wagner, Andreas O.; Markt, Rudolf; Mutschlechner, Mira Journal of Visualized Experiments, Issue 150 https://doi.org/10.3791/60155	journal	August 2019
Droplet-based high-throughput cultivation for accurate screening of antibiotic resistant gut microbes Watterson, William J.; Tanyeri, Melikhan; Watson, Andrea R. eLife, Vol. 9 https://doi.org/10.7554/eLife.56998	journal	June 2020

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