» Articles » PMID: 38916306

Metabologenomics Reveals Strain-level Genetic and Chemical Diversity of Secondary Metabolism

Overview
Journal mSystems
Specialty Microbiology
Date 2024 Jun 25
PMID 38916306
Authors
Affiliations
Soon will be listed here.
Abstract

spp. are renowned for producing the hepatotoxin microcystin in freshwater cyanobacterial harmful algal blooms around the world, threatening drinking water supplies and public and environmental health. However, genomes also harbor numerous biosynthetic gene clusters (BGCs) encoding the biosynthesis of other secondary metabolites, including many with toxic properties. Most of these BGCs are uncharacterized and currently lack links to biosynthesis products. However, recent field studies show that many of these BGCs are abundant and transcriptionally active in natural communities, suggesting potentially important yet unknown roles in bloom ecology and water quality. Here, we analyzed 21 xenic cultures isolated from western Lake Erie to investigate the diversity of the biosynthetic potential of this genus. Through metabologenomic and approaches, we show that these strains contain variable BGCs, previously observed in natural populations, and encode distinct metabolomes across cultures. Additionally, we find that the majority of metabolites and gene clusters are uncharacterized, highlighting our limited understanding of the chemical repertoire of spp. Due to the complex metabolomes observed in culture, which contain a wealth of diverse congeners as well as unknown metabolites, these results underscore the need to deeply explore and identify secondary metabolites produced by beyond microcystins to assess their impacts on human and environmental health.IMPORTANCEThe genus forms dense cyanobacterial harmful algal blooms (cyanoHABs) and can produce the toxin microcystin, which has been responsible for drinking water crises around the world. While microcystins are of great concern, also produces an abundance of other secondary metabolites that may be of interest due to their potential for toxicity, ecological importance, or pharmaceutical applications. In this study, we combine genomic and metabolomic approaches to study the genes responsible for the biosynthesis of secondary metabolites as well as the chemical diversity of produced metabolites in strains from the Western Lake Erie Culture Collection. This unique collection comprises strains that were directly isolated from western Lake Erie, which experiences substantial cyanoHAB events annually and has had negative impacts on drinking water, tourism, and industry.

References
1.
Qin B, Zhu G, Gao G, Zhang Y, Li W, Paerl H . A drinking water crisis in Lake Taihu, China: linkage to climatic variability and lake management. Environ Manage. 2009; 45(1):105-12. DOI: 10.1007/s00267-009-9393-6. View

2.
Faltermann S, Zucchi S, Kohler E, Blom J, Pernthaler J, Fent K . Molecular effects of the cyanobacterial toxin cyanopeptolin (CP1020) occurring in algal blooms: global transcriptome analysis in zebrafish embryos. Aquat Toxicol. 2014; 149:33-9. DOI: 10.1016/j.aquatox.2014.01.018. View

3.
Martins J, Vasconcelos V . Cyanobactins from Cyanobacteria: Current Genetic and Chemical State of Knowledge. Mar Drugs. 2015; 13(11):6910-46. PMC: 4663559. DOI: 10.3390/md13116910. View

4.
Otify A, Mohamed O, El-Amier Y, Saber F, Tripathi A, Younis I . Bioherbicidal Activity and Metabolic Profiling of Allelopathic Metabolites of Three Cassia species using UPLC-qTOF-MS/MS and Molecular Networking. Metabolomics. 2023; 19(3):16. DOI: 10.1007/s11306-023-01980-5. View

5.
Hjorleifsson Eldjarn G, Ramsay A, van der Hooft J, Duncan K, Soldatou S, Rousu J . Ranking microbial metabolomic and genomic links in the NPLinker framework using complementary scoring functions. PLoS Comput Biol. 2021; 17(5):e1008920. PMC: 8130963. DOI: 10.1371/journal.pcbi.1008920. View