Integrated Metabolomic–Genomic Workflows Accelerate Microbial Natural Product Discovery
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The pairing of analytical chemistry with genomic techniques represents a new wave in natural product chemistry. With an increase in the availability of sequencing and assembly of microbial genomes, interrogation into the biosynthetic capability of producers with valuable secondary metabolites is possible. However, without the development of robust, accessible, and medium to high throughput tools, the bottleneck in pairing metabolic potential and compound isolation will continue. Several innovative approaches have proven useful in the nascent stages of microbial genome-informed drug discovery. Here, we consider a number of these approaches which have led to prioritization of strain targets and have mitigated rediscovery rates. Likewise, we discuss integration of principles of comparative evolutionary studies and retrobiosynthetic predictions to better understand biosynthetic mechanistic details and link genome sequence to structure. Lastly, we discuss advances in engineering, chemistry, and molecular networking and other computational approaches that are accelerating progress in the field of omic-informed natural product drug discovery. Together, these strategies enhance the synergy between cutting edge omics, chemical characterization, and computational technologies that pitch the discovery of natural products with pharmaceutical and other potential applications to the crest of the wave where progress is ripe for rapid advances.
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Modern non-targeted metabolomics workflows have accelerated the annotation of known molecules and aided the discovery and structure elucidation of novel compounds in the natural product community.
“At the same time, these advances have also been leveraged by the natural product community, where modern non-targeted metabolomics workflow have accelerated the annotation of known molecules and aided the discovery and structure elucidation of novel compounds.174”
From Connecting metabolome and phenotype: recent advances in functional metabolomics tools for the identification of bioactive natural products (2024) · cites this paper as [174]
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Basic local alignment search tool
Altschul, S. F., Gish, W., Miller, W., Myers, E. W., & Lipman, D. J. (1990) · Journal of Molecular Biology · doi:10.1006/jmbi.1990.9999 · Cited by 98,669 · see citing works
Database resources of the National Center for Biotechnology Information: update
Wheeler, D. L. (2003) · Nucleic Acids Research · doi:10.1093/nar/gkh073 · Cited by 10,691 · see citing works
Natural Products as Sources of New Drugs over the Nearly Four Decades from 01/1981 to 09/2019
Newman, D. J., & Cragg, G. M. L. (2020) · Journal of Natural Products · doi:10.1021/acs.jnatprod.9b01285 · Cited by 7,153 · see citing works
Database resources of the National Center for Biotechnology Information
Agarwala, R., Barrett, T., Beck, J., Benson, D., Bollin, C., Bolton, E. E., Bourexis, D., Brister, J., Bryant, S. H., Canese, K., et al. (2017) · Nucleic Acids Res. · doi:10.1093/nar/gkx1095 · Cited by 6,277 · see citing works
Wang, M., Carver, J. J., Phelan, V. V., Sanchez, L. M., Garg, N., Peng, Y., Nguyen, D. D., Watrous, J., Kapono, C. A., Luzzatto-Knaan, T., et al. (2016) · Nature Biotechnology · doi:10.1038/nbt.3597 · Cited by 4,629 · see citing works
antiSMASH 5.0: updates to the secondary metabolite genome mining pipeline
Blin, K., Shaw, S., Steinke, K., Villebro, R., Ziemert, N., Lee, S. Y., Medema, M. H., & Weber, T. (2019) · Nucleic Acids Research · doi:10.1093/nar/gkz310 · Cited by 2,915 · see citing works
IMG: the integrated microbial genomes database and comparative analysis system
Markowitz, V. M., Chen, I.-M. A., Palaniappan, K., Chu, K., Szeto, E., Grechkin, Y., Ratner, A., Jacob, B., Huang, J., Williams, P. G., et al. (2011) · Nucleic Acids Research · doi:10.1093/nar/gkr1044 · Cited by 1,315 · see citing works
Lessons from natural molecules
Clardy, J., & Walsh, C. T. (2004) · Nature · doi:10.1038/nature03194 · Cited by 1,178 · see citing works
A computational framework to explore large-scale biosynthetic diversity
Navarro-Muñoz, J. C., Mojica, N. S., Mullowney, M. W., Kautsar, S. A., Tryon, J. H., Parkinson, E. I., Santos, E. L. C. D. L., Yeong, M., Cruz‐Morales, P., Abubucker, S., et al. (2019) · Nature Chemical Biology · doi:10.1038/s41589-019-0400-9 · Cited by 1,032 · see citing works
A genomic catalog of Earth’s microbiomes
Nayfach, S., Roux, S., Seshadri, R., Udwary, D., Varghese, N. J., Schulz, F., Wu, D., Páez-Espino, D., Chen, I.-M. A., Huntemann, M., et al. (2020) · Nature Biotechnology · doi:10.1038/s41587-020-0718-6 · Cited by 847 · see citing works
Self-citationHarnessing the Biosynthetic Code: Combinations, Permutations, and Mutations
Cane, D. E., Walsh, C. T., & Khosla, C. (1998) · Science · doi:10.1126/science.282.5386.63 · Cited by 605 · see citing works
MIBiG 2.0: a repository for biosynthetic gene clusters of known function
Kautsar, S. A., Blin, K., Shaw, S., Navarro-Muñoz, J. C., Terlouw, B. R., van der Hooft, J. J. J., van Santen, J. A., Tracanna, V., Duran, H. G. S., Andreu, V. P., et al. (2019) · Nucleic Acids Research · doi:10.1093/nar/gkz882 · Cited by 562 · see citing works
Close-Range Electrostatic Interactions in Proteins
Kumar, S., & Nussinov, R. (2002) · ChemBioChem · doi:10.1002/1439-7633(20020703)3:7 · Cited by 548 · see citing works
Biosynthesis of polyketides by trans-AT polyketide synthases
Helfrich, E. J. N., & Piel, J. (2015) · Natural Product Reports · doi:10.1039/c5np00125k · Cited by 478 · see citing works
Alanjary, M. M., Steinke, K., & Ziemert, N. (2019) · Nucleic Acids Research · doi:10.1093/nar/gkz282 · Cited by 469 · see citing works
Ziemert, N., Podell, S. B., Penn, K., Badger, J. H., Allen, E. E., & Jensen, P. R. (2012) · PLoS ONE · doi:10.1371/journal.pone.0034064 · Cited by 444 · see citing works
Marine Natural Products: A New Wave of Drugs?
Montaser, R., & Luesch, H. (2011) · Future Medicinal Chemistry · doi:10.4155/fmc.11.118 · Cited by 439 · see citing works
The Natural Products Atlas: An Open Access Knowledge Base for Microbial Natural Products Discovery
van Santen, J. A., Jacob, G., Singh, A. L., Aniebok, V., Balunas, M. J., Bunsko, D., Neto, F. C., Castaño-Espriu, L., Chang, C., Clark, T. N., et al. (2019) · ACS Central Science · doi:10.1021/acscentsci.9b00806 · Cited by 421 · see citing works
A mass spectrometry–guided genome mining approach for natural product peptidogenomics
Kersten, R. D., Yang, Y., Xu, Y., Cimermančič, P., Nam, S.-J., Fenical, W., Fischbach, M. A., Moore, B. S., & Dorrestein, P. C. (2011) · Nature Chemical Biology · doi:10.1038/nchembio.684 · Cited by 360 · see citing works
Sudek, S., Lopanik, N. B., Waggoner, L. E., Hildebrand, M., Bassis, C. M., Liu, H., Patel, A. U., Sherman, D. H., & Haygood, M. G. (2006) · Journal of Natural Products · doi:10.1021/np060361d · Cited by 314 · see citing works
Gross, H., Stockwell, V. O., Henkels, M. D., Nowak-Thompson, B., Loper, J. E., & Gerwick, W. H. (2007) · Chemistry & Biology · doi:10.1016/j.chembiol.2006.11.007 · Cited by 304 · see citing works
Inferring Horizontal Gene Transfer
Ravenhall, M., Škunca, N., Lassalle, F., & Dessimoz, C. (2015) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1004095 · Cited by 301 · see citing works
Luo, Y., Huang, H., Liang, J., Wang, M., Lu, L., Shao, Z., Cobb, R. E., & Zhao, H. (2013) · Nature Communications · doi:10.1038/ncomms3894 · Cited by 260 · see citing works
Bioinformatics and Drug Discovery
Xia, X. (2017) · Current Topics in Medicinal Chemistry · doi:10.2174/1568026617666161116143440 · Cited by 256 · see citing works
Mungan, M. D., Alanjary, M. M., Blin, K., Weber, T., Medema, M. H., & Ziemert, N. (2020) · Nucleic Acids Research · doi:10.1093/nar/gkaa374 · Cited by 199 · see citing works
Quirós, L. M., Aguirrezabalaga, I., Olano, C., Méndez, C., & Salas, J. A. (1998) · Molecular Microbiology · doi:10.1046/j.1365-2958.1998.00880.x · Cited by 179 · see citing works
Crossroads of Antibiotic Resistance and Biosynthesis
Wencewicz, T. A. (2019) · Journal of Molecular Biology · doi:10.1016/j.jmb.2019.06.033 · Cited by 170 · see citing works
Calyculin A, an inhibitor of protein phosphatases, a potent tumor promoter on CD-1 mouse skin.
Suganuma, M., Fujiki, H., Furuya‐Suguri, H., Yoshizawa, S., Yasumoto, S., Kato, Y., Fusetani, N., & Sügimura, T. (1990) · PubMed · Cited by 156 · see citing works
A Natural Product Chemist's Guide to Unlocking Silent Biosynthetic Gene Clusters
Covington, B. C., Xu, F. Y., & Seyedsayamdost, M. R. (2021) · Annual Review of Biochemistry · doi:10.1146/annurev-biochem-081420-102432 · Cited by 155 · see citing works
CRAGE enables rapid activation of biosynthetic gene clusters in undomesticated bacteria
Wang, G., Zhao, Z., Ke, J., Engel, Y., Shi, Y., Robinson, D., Bingol, K., Zhang, Z., Bowen, B. P., Louie, K., et al. (2019) · Nature Microbiology · doi:10.1038/s41564-019-0573-8 · Cited by 154 · see citing works
Genome Mining as New Challenge in Natural Products Discovery
Albarano, L., Esposito, R., Ruocco, N., & Costantini, M. (2020) · Marine Drugs · doi:10.3390/md18040199 · Cited by 152 · see citing works
Goering, A. W., McClure, R. A., Doroghazi, J. R., Albright, J. C., Haverland, N. A., Zhang, Y., Ju, K., Thomson, R. J., Metcalf, W. W., & Kelleher, N. L. (2016) · ACS Central Science · doi:10.1021/acscentsci.5b00331 · Cited by 148 · see citing works
Calyculin biogenesis from a pyrophosphate protoxin produced by a sponge symbiont
Wakimoto, T., Egami, Y., Nakashima, Y., Wakimoto, Y., Mori, T., Awakawa, T., Ito, T., Kenmoku, H., Asakawa, Y., Piel, J., et al. (2014) · Nature Chemical Biology · doi:10.1038/nchembio.1573 · Cited by 140 · see citing works
Cruz‐Morales, P., Kopp, J. F., Martínez-Guerrero, C. E., Yáñez-Guerra, L. A., Mojica, N. S., Ramos-Aboites, H. E., Feldmann, J., & Barona‐Gómez, F. (2016) · Genome Biology and Evolution · doi:10.1093/gbe/evw125 · Cited by 137 · see citing works
A community resource for paired genomic and metabolomic data mining
Schorn, M., Verhoeven, S., Ridder, L., Huber, F., Acharya, D. D., Aksenov, A. A., Aleti, G., Moghaddam, J. A., Aron, A. T., Aziz, S., et al. (2021) · Nature Chemical Biology · doi:10.1038/s41589-020-00724-z · Cited by 131 · see citing works
Ancient Horizontal Gene Transfer from Bacteria Enhances Biosynthetic Capabilities of Fungi
Schmitt, I., & Lumbsch, H. T. (2009) · PLoS ONE · doi:10.1371/journal.pone.0004437 · Cited by 130 · see citing works
Ross, A. C., Gulland, L. E. S., Dorrestein, P. C., & Moore, B. S. (2014) · ACS Synthetic Biology · doi:10.1021/sb500280q · Cited by 113 · see citing works
Pep2Path: Automated Mass Spectrometry-Guided Genome Mining of Peptidic Natural Products
Medema, M. H., Paalvast, Y., Nguyen, D. D., Melnik, A. V., Dorrestein, P. C., Eriko Takano, A., & Rainer Breitling, A. (2014) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1003822 · Cited by 109 · see citing works
Efficacy of Selected Natural Products as Therapeutic Agents against Cancer
Banerjee, S., Wang, Z., Mohammad, M., Sarkar, F. H., & Mohammad, R. M. (2008) · Journal of Natural Products · doi:10.1021/np0705716 · Cited by 105 · see citing works
The hidden enzymology of bacterial natural product biosynthesis
Scott, T. A., & Piel, J. (2019) · Nature Reviews Chemistry · doi:10.1038/s41570-019-0107-1 · Cited by 104 · see citing works
Gurevich, A. A., Mikheenko, A., Shlemov, A., Korobeynikov, A., Mohimani, H., & Pevzner, P. A. (2018) · Nature Microbiology · doi:10.1038/s41564-017-0094-2 · Cited by 99 · see citing works
IMG-ABC v.5.0: an update to the IMG/Atlas of Biosynthetic Gene Clusters Knowledgebase
Palaniappan, K., Chen, I.-M. A., Chu, K., Ratner, A., Seshadri, R., Kyrpides, N. C., Ivanova, N., & Mouncey, N. J. (2019) · Nucleic Acids Research · doi:10.1093/nar/gkz932 · Cited by 98 · see citing works
Neuroprotective versus tumorigenic protein kinase C activators
Nelson, T. J., & Alkon, D. L. (2009) · Trends in Biochemical Sciences · doi:10.1016/j.tibs.2008.11.006 · Cited by 97 · see citing works
NRPquest: Coupling Mass Spectrometry and Genome Mining for Nonribosomal Peptide Discovery
Mohimani, H., Liu, W.-T., Kersten, R. D., Moore, B. S., Dorrestein, P. C., & Pevzner, P. A. (2014) · Journal of Natural Products · doi:10.1021/np500370c · Cited by 96 · see citing works
Biosynthesis of the Myxobacterial Antibiotic Corallopyronin A
Erol, Ö., Schäberle, T. F., Schmitz, A., Rachid, S., Gurgui, C., Omari, M. E., Lohr, F., Kehraus, S., Piel, J., Müller, R., et al. (2010) · ChemBioChem · doi:10.1002/cbic.201000085 · Cited by 94 · see citing works
Almabruk, K. H., Dinh, L. K., & Philmus, B. J. (2018) · ACS Chemical Biology · doi:10.1021/acschembio.8b00173 · Cited by 92 · see citing works
Dual effects of bryostatin-1 on spatial memory and depression
Sun, M., & Alkon, D. L. (2005) · European Journal of Pharmacology · doi:10.1016/j.ejphar.2005.02.028 · Cited by 87 · see citing works
Microbial natural product databases: moving forward in the multi-omics era
van Santen, J. A., Kautsar, S. A., Medema, M. H., & Linington, R. G. (2020) · Natural Product Reports · doi:10.1039/d0np00053a · Cited by 79 · see citing works
Integrating genomics and metabolomics for scalable non-ribosomal peptide discovery
Behsaz, B., Bode, E., Gurevich, A. A., Shi, Y., Grundmann, F., Acharya, D. D., Caraballo‐Rodríguez, A. M., Bouslimani, A., Panitchpakdi, M. W., Linck, A., et al. (2021) · Nature Communications · doi:10.1038/s41467-021-23502-4 · Cited by 75 · see citing works
Cao, L., Gurevich, A. A., Alexander, K. L., Naman, C. B., Leão, T., Glukhov, E., Luzzatto‐Knaan, T., Vargas, F., Quinn, R., Bouslimani, A., et al. (2019) · Cell Systems · doi:10.1016/j.cels.2019.09.004 · Cited by 71 · see citing works
EvoMining reveals the origin and fate of natural product biosynthetic enzymes
Mojica, N. S., Aguilar, C., Gutiérrez-García, K., Martínez-Guerrero, C. E., & Barona‐Gómez, F. (2019) · Microbial Genomics · doi:10.1099/mgen.0.000260 · Cited by 69 · see citing works
The confluence of big data and evolutionary genome mining for the discovery of natural products
Chevrette, M. G., Gavrilidou, A., Mantri, S., Selem-Mojica, N., Ziemert, N., & Barona-Gómez, F. (2021) · Natural Product Reports · doi:10.1039/d1np00013f · Cited by 66 · see citing works
A Practical Guide to Metabolomics Software Development
Chang, H.-Y., Colby, S., Du, X., Gomez, J. D., Helf, M. J., Kechris, K. J., Kirkpatrick, C. R., Li, S., Patti, G. J., Renslow, R. S., et al. (2021) · Analytical Chemistry · doi:10.1021/acs.analchem.0c03581 · Cited by 56 · see citing works
Combinatorial biosynthesis of RiPPs: docking with marine life
Sardar, D., & Schmidt, E. W. (2015) · Current Opinion in Chemical Biology · doi:10.1016/j.cbpa.2015.11.016 · Cited by 55 · see citing works
Applied evolution: phylogeny-based approaches in natural products research
Adamek, M., Alanjary, M. M., & Ziemert, N. (2019) · Natural Product Reports · doi:10.1039/c9np00027e · Cited by 52 · see citing works
Jansen, R., Höfle, G., Irschik, H., & Reichenbach, H. (1985) · Liebigs Annalen der Chemie · doi:10.1002/jlac.198519850418 · Cited by 47 · see citing works
Genomic approaches to drug discovery
Ricke, D. O., Wang, S., Cai, R. L., & Cohen, D. (2006) · Current Opinion in Chemical Biology · doi:10.1016/j.cbpa.2006.06.024 · Cited by 45 · see citing works
Comparative Metabologenomics Analysis of Polar Actinomycetes
Soldatou, S., Eldjárn, G. H., Ramsay, A., van der Hooft, J. J. J., Hughes, A. H., Rogers, S., & Duncan, K. (2021) · Marine Drugs · doi:10.3390/md19020103 · Cited by 42 · see citing works
Heterologous Expression of Cryptomaldamide in a Cyanobacterial Host
Taton, A., Ecker, A. K., Diaz, B., Moss, N. A., Anderson, B., Reher, R., Leão, T., Simkovsky, R., Dorrestein, P. C., Gerwick, L. G., et al. (2020) · ACS Synthetic Biology · doi:10.1021/acssynbio.0c00431 · Cited by 39 · see citing works
An isotopic labeling approach linking natural products with biosynthetic gene clusters
McCaughey, C. S., van Santen, J. A., van der Hooft, J. J. J., Medema, M. H., & Linington, R. G. (2022) · Nature Chemical Biology · doi:10.1038/s41589-021-00949-6 · Cited by 39 · see citing works
Leão, T., Wang, M., Moss, N. A., Silva, R., Sanders, J. G., Nurk, S., Gurevich, A. A., Humphrey, G., Reher, R., Zhu, Q., et al. (2021) · Marine Drugs · doi:10.3390/md19010020 · Cited by 38 · see citing works
Buchholz, T. J., Rath, C. M. B., Lopanik, N. B., Gardner, N. P., Håkansson, K., & Sherman, D. H. (2010) · Chemistry & Biology · doi:10.1016/j.chembiol.2010.08.008 · Cited by 37 · see citing works
Kinnel, R. B., Esquenazi, E., Leão, T., Moss, N. A., Mevers, E. E., Pereira, A. R., Monroe, E. A., Korobeynikov, A., Murray, T. F., Sherman, D. H., et al. (2017) · Journal of Natural Products · doi:10.1021/acs.jnatprod.7b00019 · Cited by 35 · see citing works
Handayani, I., Saad, H. H., Ratnakomala, S., Lisdiyanti, P., Kusharyoto, W., Krause, J., Kulik, A., Wohlleben, W., Aziz, S., Gross, H., et al. (2021) · Marine Drugs · doi:10.3390/md19060316 · Cited by 32 · see citing works
Yushchuk, O., Ostash, I., Mösker, E., Vlasiuk, I., Deneka, M., Rückert, C., Busche, T., Fedorenko, V., Kalinowski, J., Süßmuth, R. D., et al. (2021) · Scientific Reports · doi:10.1038/s41598-021-82934-6 · Cited by 30 · see citing works
Park, O., Choi, H., Kim, G., & Kim, W. (2016) · ChemBioChem · doi:10.1002/cbic.201600241 · Cited by 29 · see citing works
Larson, C. B., Crüsemann, M., & Moore, B. S. (2017) · Journal of Natural Products · doi:10.1021/acs.jnatprod.6b01121 · Cited by 26 · see citing works
Co-occurrence of enzyme domains guides the discovery of an oxazolone synthetase
de Rond, T., Asay, J. E., & Moore, B. S. (2021) · Nature Chemical Biology · doi:10.1038/s41589-021-00808-4 · Cited by 26 · see citing works
Louwen, J. J. R., & van der Hooft, J. J. J. (2021) · mSystems · doi:10.1128/msystems.00726-21 · Cited by 25 · see citing works
Tan, B., Chen, S., Zhang, Q., Chen, Y., Zhu, Y., Khan, I., Zhang, W., & Zhang, C. (2020) · Organic Letters · doi:10.1021/acs.orglett.9b04597 · Cited by 23 · see citing works
Nogawa, T., Terai, A., Amagai, K., Hashimoto, J., Futamura, Y., Okano, A., Fujie, M., Satoh, N., Ikeda, H., Shin‐ya, K., et al. (2020) · Journal of Natural Products · doi:10.1021/acs.jnatprod.0c00755 · Cited by 20 · see citing works
Murray, A. E., Lo, C., Daligault, H. E., Avalon, N. E., Read, R. W., Davenport, K. W., Higham, M. L., Kunde, Y. A., Dichosa, A. E. K., Baker, B. J., et al. (2021) · mSphere · doi:10.1128/msphere.00759-21 · Cited by 18 · see citing works
Self-citationShi, Y., Gu, R., Li, Y., Wang, X., Ren, W., Li, X., Wang, L., Xie, Y., & Hong, B. (2019) · Microbial Cell Factories · doi:10.1186/s12934-019-1225-7 · Cited by 16 · see citing works
Murray, A. E., Avalon, N. E., Bishop, L., Davenport, K. W., Delage, E., Dichosa, A. E. K., Eveillard, D., Higham, M. L., Kokkaliari, S., Lo, C., et al. (2020) · Marine Drugs · doi:10.3390/md18060298 · Cited by 14 · see citing works
Self-citationAvalon, N. E., Murray, A. E., Daligault, H. E., Lo, C., Davenport, K. W., Dichosa, A. E. K., Chain, P., & Baker, B. J. (2021) · Frontiers in Chemistry · doi:10.3389/fchem.2021.802574 · Cited by 13 · see citing works
Self-citationIdentification of a solo acylhomoserine lactone synthase from the myxobacterium Archangium gephyra
Albataineh, H., Duke, M., Misra, S. K., Sharp, J. S., & Stevens, D. C. (2021) · Scientific Reports · doi:10.1038/s41598-021-82480-1 · Cited by 6 · see citing works
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Qiu, S., Cai, Y., Yao, H., Lin, C., Xie, Y., Tang, S., & Zhang, A. (2023) · Signal Transduction and Targeted Therapy · doi:10.1038/s41392-023-01399-3 · Cited by 939 · see citing works
Puig‐Castellví, F., Pacheco‐Tapia, R., Deslande, M., Jia, M., Andrikopoulos, P., Chechi, K., Bonnefond, A., Froguel, P., & Dumas, M. (2023) · TrAC Trends in Analytical Chemistry · doi:10.1016/j.trac.2023.117248 · Cited by 84 · see citing works
Impact of Marine Chemical Ecology Research on the Discovery and Development of New Pharmaceuticals
Tan, L. T. (2023) · Marine Drugs · doi:10.3390/md21030174 · Cited by 70 · see citing works
Vitale, G. A., Geibel, C., Minda, V., Wang, M., Aron, A. T., & Petras, D. (2024) · Natural Product Reports · doi:10.1039/d3np00050h · Cited by 66 · see citing works
Globally distributed marine Gemmatimonadota have unique genomic potentials
Gong, X., Xu, L., Langwig, M. V., Chen, Z., Huang, S., Zhao, D., Su, L., Zhang, Y., Francis, C. A., Liu, J., et al. (2024) · Microbiome · doi:10.1186/s40168-024-01871-4 · Cited by 53 · see citing works
Self-citationUnlocking the potential of bacterial endophytes from medicinal plants for drug discovery
Zotchev, S. B. (2024) · Microbial Biotechnology · doi:10.1111/1751-7915.14382 · Cited by 47 · see citing works
Scoary2: rapid association of phenotypic multi-omics data with microbial pan-genomes
Röder, T., Pimentel, G., Fuchsmann, P., Stern, M. T., von Ah, U., Vergères, G., Peischl, S., Brynildsrud, O. B., Bruggmann, R., & Bär, C. (2024) · Genome biology · doi:10.1186/s13059-024-03233-7 · Cited by 40 · see citing works
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Holland, D. C., & Carroll, A. R. (2023) · Natural Product Reports · doi:10.1039/d2np00085g · Cited by 29 · see citing works
Bacterial natural product discovery by heterologous expression
Kadjo, A. E., & Eustáquio, A. S. (2023) · Journal of Industrial Microbiology & Biotechnology · doi:10.1093/jimb/kuad044 · Cited by 26 · see citing works
Ragozzino, C., Casella, V., Coppola, A., Scarpato, S., Buonocore, C., Consiglio, A., Esposito, F. P., Galasso, C., Tedesco, P., Sala, G. D., et al. (2025) · Marine Drugs · doi:10.3390/md23030116 · Cited by 26 · see citing works
The insect microbiome is a vast source of bioactive small molecules
Grundmann, C. O., Guzman, J. D., Vilcinskas, A., & Pupo, M. T. (2024) · Natural Product Reports · doi:10.1039/d3np00054k · Cited by 23 · see citing works
Biodiversity-Driven Natural Products and Bioactive Metabolites
Flores, G. A., Cusumano, G., Venanzoni, R., & Angelini, P. (2025) · Plants · doi:10.3390/plants15010104 · Cited by 19 · see citing works
Yi, Y., Liang, L., de Jong, A., & Kuipers, O. P. (2024) · Genomics · doi:10.1016/j.ygeno.2024.110880 · Cited by 18 · see citing works
Harper, C. P., Day, A., Tsingos, M., Ding, E., Zeng, E., Stumpf, S. D., Qi, Y., Robinson, A., Greif, J., & Blodgett, J. A. V. (2024) · Applied and Environmental Microbiology · doi:10.1128/aem.00600-24 · Cited by 14 · see citing works
Surwase, A. J., & Thakur, N. L. (2024) · Biotechnology Advances · doi:10.1016/j.biotechadv.2024.108449 · Cited by 13 · see citing works
Ayon, N. J., Earp, C. E., Gupta, R., Butun, F. A., Clements, A. E., Lee, A. G., Dainko, D., Robey, M. T., Khin, M., Mardiana, L., et al. (2024) · Metabolomics · doi:10.1007/s11306-024-02153-8 · Cited by 12 · see citing works
Exploring microbial natural products through NMR-based metabolomics
Wang, D., Hu, J.-Q., Wang, C., Liu, T., Li, Y., & Wu, C. (2025) · Natural Product Reports · doi:10.1039/d4np00065j · Cited by 12 · see citing works
Li, X., Guo, Z., Wen, X., Li, M.-N., & Yang, H. Q. (2023) · Journal of Chromatography A · doi:10.1016/j.chroma.2023.464417 · Cited by 11 · see citing works
Makut, M. D., Mafe, A. N., Owuna, J. E., Călina, D. C., & Sharifi‐Rad, J. (2026) · Journal of the Science of Food and Agriculture · doi:10.1002/jsfa.70405 · Cited by 12 · see citing works
Molecules to medicine: advances in metabolomics for natural product drug discovery
Deleray, V., Dorrestein, P. C., & Avalon, N. E. (2025) · Current Opinion in Biotechnology · doi:10.1016/j.copbio.2025.103373 · Cited by 8 · see citing works
Self-citationBoruta, T. (2023) · Computational and Structural Biotechnology Journal · doi:10.1016/j.csbj.2023.08.011 · Cited by 8 · see citing works
Rakhmawatie, M. D., Marfu’ati, N., BARSALIPUTRI, B., Fikriyah, A. Z., & Ethica, S. N. (2023) · Biodiversitas Journal of Biological Diversity · doi:10.13057/biodiv/d240538 · Cited by 7 · see citing works
Kitikhun, S., Siriarchawatana, P., Chunhametha, S., Suriyachadkun, C., Rattanawaree, P., Phithakrotchanakoon, C., Harnpicharnchai, P., Eurwilaichitr, L., & Ingsriswang, S. (2023) · Diversity · doi:10.3390/d15050663 · Cited by 6 · see citing works
Chemodiversity and Anti-Leukemia Effect of Metabolites from Penicillium setosum CMLD 18
de Carvalho, A. C., Lima, C. S., Torquato, H. F. V., Domiciano, A. T., Silva, S. D. C., Abreu, L. M., Uemi, M., Paredes‐Gamero, E. J., Vieira, P. C., Veiga, T. A. M., et al. (2022) · Metabolites · doi:10.3390/metabo13010023 · Cited by 5 · see citing works
Sedeek, A. M., Hassan, M., Elsayed, T. R., & Ramadan, M. A. (2025) · Archives of Microbiology · doi:10.1007/s00203-025-04570-2 · Cited by 4 · see citing works
Ouchene, R., Zaatout, N., & Suzuki, M. T. (2024) · Journal of Basic Microbiology · doi:10.1002/jobm.202400046 · Cited by 4 · see citing works
Wohlgemuth, R. (2024) · Life · doi:10.3390/life14030364 · Cited by 3 · see citing works
Bao, Y., Deng, F., Dong, Y., Wang, R., & Li, H. (2025) · Analytical Chemistry · doi:10.1021/acs.analchem.5c02213 · Cited by 2 · see citing works
Methods and tools for OMICS data integration
Belalov, I. S., & Li, X. (2024) · Elsevier eBooks · doi:10.1016/b978-0-443-15568-0.00005-4 · Cited by 2 · see citing works
Gao, C. (2023) · CABI eBooks · doi:10.1079/9781800621954.0007 · Cited by 2 · see citing works
Wang, W., Luo, X., Qin, X., Tang, J., Xie, S., Shen, K., Zhu, G., & Zhao, P. (2025) · Chemistry & Biodiversity · doi:10.1002/cbdv.202502391 · Cited by 1 · see citing works
Omics technologies in natural compound profiling
Mishra, S. (2025) · Elsevier eBooks · doi:10.1016/b978-0-443-33351-4.00006-4 · Cited by 1 · see citing works
Globally distributed marine Gemmatimonadota have unique genomic potentialsPreprint
Baker, B. J., Gong, X., Xu, L., Langwig, M. V., Chen, Z., Huang, S. J., Zhao, D., Su, L., Zhang, Y., Francis, C. A., et al. (2024) · Research Square · doi:10.21203/rs.3.rs-3894446/v1
Self-citationRajesh, P., Ajore, R., & Kaur, H. (2025) · Springer eBooks · doi:10.1007/978-981-96-4824-5_10
Abdelrahman, S. M., Pratte, Z. A., Samak, M. E., Dosoky, N. S., Hanora, A., Stewart, F. J., & Lopanik, N. B. (2025) · Marine Drugs · doi:10.3390/md23100404
Microbial secondary metabolites
Javaid, A., & Mudavath, S. L. (2025) · Elsevier eBooks · doi:10.1016/b978-0-443-33959-2.00012-5
Han, J.-R., Li, S., Lian, W., Lü, X. C., Duan, L., Li, J., Shi, G.-Y., Wei, Q., Ali, M. A., Li, W., et al. (2025) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2025.11.08.687343
Röder, T., Pimentel, G., Fuchsmann, P., Stern, M. T., von Ah, U., Vergères, G., Peischl, S., Brynildsrud, O. B., Bruggmann, R., & Bär, C. (2024) · Figshare · doi:10.6084/m9.figshare.25591475
Röder, T., Pimentel, G., Fuchsmann, P., Stern, M. T., von Ah, U., Vergères, G., Peischl, S., Brynildsrud, O. B., Bruggmann, R., & Bär, C. (2024) · Figshare · doi:10.6084/m9.figshare.25591286
Han, J.-R., Li, S., Lian, W., Lu, X., Duan, L., Li, J.-L., Shi, G., Wei, Q., Ali, M., Li, W.-J., et al. (2026) · Applied and Environmental Microbiology · doi:10.1128/aem.02235-25
Exploring deep-sea Actinomycetota chemical diversity by using the OSMAC approach
Correia, S., Ribeiro, I., Braga‐Henriques, A., Leão, P. N., Urbatzka, R., & Carvalho, M. F. (2026) · Frontiers in Marine Science · doi:10.3389/fmars.2026.1754764
Cruz-Medrano, M. G., Sánchez‐Reyes, A., Manzanares‐Leal, G. L., & Ramirez-Durán, N. (2026) · Molecular Phylogenetics and Evolution · doi:10.1016/j.ympev.2026.108686
Orogu, J. O., Edo, G. I., Alamiery, A. A., Ainyanbhor, I. E., Afitijagun, I. P., Oghroro, E. E. A., Owheruo, J. O., Yousif, E., Jikah, A. N., Essaghah, A. E. A., et al. (2026) · Ecological Frontiers · doi:10.3724/j.ecofro-20260045
Bhowmick, P., Kumar, P., Panjabi, S., & Dhiman, S. (2026) · Folia Microbiologica · doi:10.1007/s12223-026-01568-1
Sena, S., Joseph, G. G., & Kumar, V. (2026) · Plant Cell Tissue and Organ Culture (PCTOC) · doi:10.1007/s11240-026-03570-4
Hassan, L., Khalaf, O., Jaber, R., & Mostafa, R. H. (2026) · Specialty journal of Pharmacognosy Phytochemistry and Biotechnology · doi:10.51847/lnaa54booi
Eshboev, F., Salihu, A. S., Khayrullaeva, L., Khamdamov, D., Gao, A. X., Mardieva, K., Salleh, W. M. N. H. W., Azimova, S. S., & Tsim, K. W. K. (2026) · Chemistry & Biodiversity · doi:10.1002/cbdv.71888
- Authors
- Avalon, N. E., Murray, A. E., & Baker, B. J.
- Affiliations
- University of South Florida (US)
- Desert Research Institute (US)
- Corresponding author
- Avalon, Nicole E.
- Murray, Alison E.
- Baker, Bill J.
- Venue
- Analytical Chemistry
- Publisher
- American Chemical Society (ACS)
- Published
- 2022-08-22
- Volume
- 94
- Issue
- 35
- Pages
- 11959-11966
- ISSN
- 0003-2700 (ISSN-L)
- 1520-6882
- PMC
- PMC9453739
- OpenAlex
- W4292668615
- Cited by
- 47
- References
- 76
- Citations by year
- 2026: 8 · 2025: 12 · 2024: 16 · 2023: 10 · 2022: 1
- FWCI
- 1.40
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Analytical Chemistry (publishedVersion, cc-by-nc-nd)
- PubMed Central (publishedVersion, cc-by-nc-nd)
- PubMed (publishedVersion)
- eScholarship (California Digital Library) (submittedVersion, cc-by-nc-nd)
- Funders
- National Cancer Institute (CA205932)
- Topics
- Health Sciences › Medicine › Pharmacology › Microbial Natural Products and Biosynthesis
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Microbial Metabolic Engineering and Bioproduction
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Metabolomics and Mass Spectrometry Studies
- Keywords
- microbial natural products, secondary metabolite biosynthesis, retrobiosynthesis, molecular networking, biosynthetic gene clusters
- MeSH terms
- Biological Products, Genomics, Metabolomics, Drug Discovery, Workflow
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