Metabolomics Reveals Strain-Specific Cyanopeptide Profiles and Their Production Dynamics in Microcystis aeruginosa and M. flos-aquae
Abstract
:1. Introduction
2. Results and Discussion
2.1. Factor Analysis of LC-HRMS Data to Reveal Cyanopeptide Variation
2.2. Molecular Networking with GNPS to Visualize Strain-Specific Cyanopeptide Diversity
2.2.1. Cyanopeptolins
2.2.2. Microviridins
2.2.3. Microcystins
2.2.4. Microginins
2.2.5. Cyanobactins
2.2.6. Anabaenopeptins
2.2.7. Aeruginosins and Unknown Clusters
2.3. Temporal Co-Production of Cyanopeptides
3. Conclusions
4. Materials and Methods
4.1. Growth of Microcystis Strains
4.2. Cyanopeptide Extraction from Microcystis Cells
4.3. Acquisition of Non-Targeted LC-MS/MS Data
4.4. Processing of Non-Targeted LC-MS/MS Datasets
4.4.1. PCA and Factor Loading in R
4.4.2. GNPS Molecular Networking
4.4.3. Heat Map Analysis to Illustrate Temporal Cyanopeptide Co-Production
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Pick, F.R. Blooming algae: A Canadian perspective on the rise of toxic cyanobacteria. Can. J. Fish. Aquat. Sci. 2016, 73, 1149–1158. [Google Scholar] [CrossRef] [Green Version]
- Paerl, H.W.; Otten, T.G. Harmful Cyanobacterial Blooms: Causes, Consequences, and Controls. Microb. Ecol. 2013, 65, 995–1010. [Google Scholar] [CrossRef] [PubMed]
- Preece, E.P.; Hardy, F.J.; Moore, B.C.; Bryan, M. A review of microcystin detections in Estuarine and Marine waters: Environmental implications and human health risk. Harmful Algae 2017, 61, 31–45. [Google Scholar] [CrossRef] [Green Version]
- Reid, A.J.; Carlson, A.K.; Creed, I.F.; Eliason, E.J.; Gell, P.A.; Johnson, P.T.J.; Kidd, K.A.; MacCormack, T.J.; Olden, J.D.; Ormerod, S.J.; et al. Emerging threats and persistent conservation challenges for freshwater biodiversity. Biol. Rev. 2019, 94, 849–873. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Carmichael, W.W.; Boyer, G.L. Health impacts from cyanobacteria harmful algae blooms: Implications for the North American Great Lakes. Harmful Algae 2016, 54, 194–212. [Google Scholar] [CrossRef] [PubMed]
- Janssen, E.M.L. Cyanobacterial peptides beyond microcystins—A review on co-occurrence, toxicity, and challenges for risk assessment. Water Res. 2019, 151, 488–499. [Google Scholar] [CrossRef]
- Taranu, Z.E.; Gregory-Eaves, I.; Leavitt, P.R.; Bunting, L.; Buchaca, T.; Catalan, J.; Domaizon, I.; Guilizzoni, P.; Lami, A.; McGowan, S.; et al. Acceleration of cyanobacterial dominance in north temperate-subarctic lakes during the Anthropocene. Ecol. Lett. 2015, 18, 375–384. [Google Scholar] [CrossRef]
- Harke, M.J.; Steffen, M.M.; Gobler, C.J.; Otten, T.G.; Wilhelm, S.W.; Wood, S.A.; Paerl, H.W. A review of the global ecology, genomics, and biogeography of the toxic cyanobacterium, Microcystis spp. Harmful Algae 2016, 54, 4–20. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Chen, L.; Giesy, J.P.; Adamovsky, O.; Svircev, Z.; Meriluoto, J.; Codd, G.A.; Mijovic, B.; Shi, T.; Tuo, X.; Li, S.-C.; et al. Challenges of using blooms of Microcystis spp. in animal feeds: A comprehensive review of nutritional, toxicological and microbial health evaluation. Sci. Total Environ. 2021, 764, 142319. [Google Scholar] [CrossRef]
- Jones, M.R.; Pinto, E.; Torres, M.A.; Dorr, F.; Mazur-Marzec, H.; Szubert, K.; Tartaglione, L.; Dell’Aversano, C.; Miles, C.O.; Beach, D.G.; et al. CyanoMetDB, a comprehensive public database of secondary metabolites from cyanobacteria. Water Res. 2021, 196, 117017. [Google Scholar] [CrossRef]
- Huang, I.S.; Zimba, P.V. Cyanobacterial bioactive metabolites-A review of their chemistry and biology. Harmful algae 2019, 86, 139–209. [Google Scholar] [CrossRef]
- Welker, M.; von Dohren, H. Cyanobacterial peptides—Nature’s own combinatorial biosynthesis. Fems Microbiol. Rev. 2006, 30, 530–563. [Google Scholar] [CrossRef] [Green Version]
- Bouaïcha, N.; Miles, C.; Beach, D.; Labidi, Z.; Djabri, A.; Benayache, N.; Nguyen-Quang, T. Structural Diversity, Characterization and Toxicology of Microcystins. Toxins 2019, 11, 714. [Google Scholar] [CrossRef] [Green Version]
- Shih, P.M.; Wu, D.; Latifi, A.; Axen, S.D.; Fewer, D.P.; Talla, E.; Calteau, A.; Cai, F.; de Marsac, N.T.; Rippka, R.; et al. Improving the coverage of the cyanobacterial phylum using diversity-driven genome sequencing. Proc. Natl. Acad. Sci. USA 2013, 110, 1053–1058. [Google Scholar] [CrossRef] [Green Version]
- Pearson, L.A.; Crosbie, N.D.; Neilan, B.A. Distribution and conservation of known secondary metabolite biosynthesis gene clusters in the genomes of geographically diverse Microcystis aeruginosa strains. Mar. Freshw. Res. 2020, 71, 701–716. [Google Scholar] [CrossRef]
- Chen, M.; Xu, C.; Wang, X.; Wu, Y.; Li, L. Nonribosomal peptide synthetases and nonribosomal cyanopeptides synthesis in Microcystis: A comparative genomics study. Algal Res.-Biomass Biofuels Bioprod. 2021, 59, 102432. [Google Scholar] [CrossRef]
- Baunach, M.; Chowdhury, S.; Stallforth, P.; Dittmann, E. The Landscape of Recombination Events That Create Nonribosomal Peptide Diversity. Mol. Biol. Evol. 2021, 38, 2116–2130. [Google Scholar] [CrossRef] [PubMed]
- Wang, M.; Carver, J.J.; Phelan, V.V.; Sanchez, L.M.; Garg, N.; Peng, Y.; Don Duy, N.; Watrous, J.; Kapono, C.A.; Luzzatto-Knaan, T.; et al. Sharing and community curation of mass spectrometry data with Global Natural Products Social Molecular Networking. Nat. Biotechnol. 2016, 34, 828–837. [Google Scholar] [CrossRef] [Green Version]
- Walsh, J.P.; Renaud, J.B.; Hoogstra, S.; McMullin, D.R.; Ibrahim, A.; Visagie, C.M.; Tanney, J.B.; Yeung, K.K.C.; Sumarah, M.W. Diagnostic fragmentation filtering for the discovery of new chaetoglobosins and cytochalasins. Rapid Commun. Mass Spectrom. 2019, 33, 133–139. [Google Scholar] [CrossRef] [PubMed]
- Taha, H.M.; Aalizadeh, R.; Alygizakis, N.; Antignac, J.-P.; Arp, H.P.H.; Bade, R.; Baker, N.; Belova, L.; Bijlsma, L.; Bolton, E.E.; et al. The NORMAN Suspect List Exchange (NORMAN-SLE): Facilitating European and worldwide collaboration on suspect screening in high resolution mass spectrometry. Environ. Sci. Eur. 2022, 34, 104. [Google Scholar] [CrossRef] [PubMed]
- van Der Hooft, J.J.J.; Mohimani, H.; Bauermeister, A.; Dorrestein, P.C.; Duncan, K.R.; Medema, M.H. Linking genomics and metabolomics to chart specialized metabolic diversity. Chem. Soc. Rev. 2020, 49, 3297–3314. [Google Scholar] [CrossRef] [PubMed]
- Teta, R.; Della Sala, G.; Glukhov, E.; Gerwick, L.; Gerwick, W.H.; Mangoni, A.; Costantino, V. Combined LC-MS/MS and Molecular Networking Approach Reveals New Cyanotoxins from the 2014 Cyanobacterial Bloom in Green Lake, Seattle. Environ. Sci. Technol. 2015, 49, 14301–14310. [Google Scholar] [CrossRef]
- Tiam, S.K.; Gugger, M.; Demay, J.; Le Manach, S.; Duval, C.; Bernard, C.; Marie, B. Insights into the Diversity of Secondary Metabolites of Planktothrix Using a Biphasic Approach Combining Global Genomics and Metabolomics. Toxins 2019, 11, 498. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Kust, A.; Rehakova, M.; Vrba, J.; Maicher, V.; Mares, J.; Hrouzek, P.; Chiriac, M.-C.; Benedova, Z.; Tesarova, B.; Saurav, K. Insight into Unprecedented Diversity of Cyanopeptides in Eutrophic Ponds Using an MS/MS Networking Approach. Toxins 2020, 12, 561. [Google Scholar] [CrossRef] [PubMed]
- Welker, M.; Marsalek, B.; Sejnohova, L.; von Dohren, H. Detection and identification of oligopeptides in Microcystis (cyanobacteria) colonies: Toward an understanding of metabolic diversity. Peptides 2006, 27, 2090–2103. [Google Scholar] [CrossRef] [PubMed]
- Fisch, K.M. Biosynthesis of natural products by microbial iterative hybrid PKS-NRPS. Rsc Adv. 2013, 3, 18228–18247. [Google Scholar] [CrossRef] [Green Version]
- Renaud, J.B.; Kelman, M.J.; McMullin, D.R.; Yeung, K.K.C.; Sumarah, M.W. Application of C8 liquid chromatography-tandem mass spectrometry for the analysis of enniatins and bassianolides. J. Chromatogr. A 2017, 1508, 65–72. [Google Scholar] [CrossRef]
- McDonald, K.; Renaud, J.B.; Pick, F.R.; Miller, J.D.; Sumarah, M.W.; McMullin, D.R. Diagnostic Fragmentation Filtering for Cyanopeptolin Detection. Environ. Toxicol. Chem. 2021, 40, 1087–1097. [Google Scholar] [CrossRef]
- McMullin, D.R.; Hoogstra, S.; McDonald, K.P.; Sumarah, M.W.; Renaud, J.B. Natural Product Discovery with LC-MS/MS Diagnostic Fragmentation Filtering: Application for Microcystin Analysis. Jove-J. Vis. Exp. 2019, 147, e59712. [Google Scholar] [CrossRef] [Green Version]
- Martin, C.; Oberer, L.; Ino, T.; Konig, W.A.; Busch, M.; Weckesser, J. Cyanopeptolins, new depsipeptides from the cyanobacterium Microcystis sp. PCC 7806. J. Antibiot. 1993, 46, 1550–1556. [Google Scholar] [CrossRef] [Green Version]
- Faltermann, S.; Zucchi, S.; Kohler, E.; Blom, J.F.; Pernthaler, J.; Fent, K. Molecular effects of the cyanobacterial toxin cyanopeptolin (CPI 020) occurring in algal blooms: Global transcriptome analysis in zebrafish embryos. Aquat. Toxicol. 2014, 149, 33–39. [Google Scholar] [CrossRef]
- Lenz, K.A.; Miller, T.R.; Ma, H. Anabaenopeptins and cyanopeptolins induce systemic toxicity effects in a model organism the nematode Caenorhabditis elegans. Chemosphere 2019, 214, 60–69. [Google Scholar] [CrossRef] [PubMed]
- Bojadzija Savic, G.; Bormans, M.; Edwards, C.; Lawton, L.; Briand, E.; Wiegand, C. Cross talk: Two way allelopathic interactions between toxic Microcystis and Daphnia. Harmful Algae 2020, 94, 101803. [Google Scholar] [CrossRef] [PubMed]
- Bister, B.; Keller, S.; Baumann, H.I.; Nicholson, G.; Weist, S.; Jung, G.; Sussmuth, R.D.; Juttner, F. Cyanopeptolin 963A, a chymotrypsin inhibitor of Microcystis PCC 7806. J. Nat. Prod. 2004, 67, 1755–1757. [Google Scholar] [CrossRef] [PubMed]
- Portmann, C.; Blom, J.F.; Kaiser, M.; Brun, R.; Juettner, F.; Gademann, K. Isolation of Aerucyclamides C and D and Structure Revision of Microcyclamide 7806A: Heterocyclic Ribosomal Peptides from Microcystis aeruginosa PCC 7806 and Their Antiparasite Evaluation. J. Nat. Prod. 2008, 71, 1891–1896. [Google Scholar] [CrossRef]
- Beversdorf, L.J.; Rude, K.; Weirich, C.A.; Bartlett, S.L.; Seaman, M.; Kozik, C.; Biese, P.; Gosz, T.; Suha, M.; Stempa, C.; et al. Analysis of cyanobacterial metabolites in surface and raw drinking waters reveals more than microcystin. Water Res. 2018, 140, 280–290. [Google Scholar] [CrossRef] [PubMed]
- Miller, T.R.; Bartlett, S.L.; Weirich, C.A.; Hernandez, J. Automated Subdaily Sampling of Cyanobacterial Toxins on a Buoy Reveals New Temporal Patterns in Toxin Dynamics. Environ. Sci. Technol. 2019, 53, 5661–5670. [Google Scholar] [CrossRef]
- Ziemert, N.; Ishida, K.; Weiz, A.; Hertweck, C.; Dittmann, E. Exploiting the Natural Diversity of Microviridin Gene Clusters for Discovery of Novel Tricyclic Depsipeptides. Appl. Environ. Microbiol. 2010, 76, 3568–3574. [Google Scholar] [CrossRef] [Green Version]
- do Amaral, S.C.; Monteiro, P.R.; Pinto Neto, J.d.S.; Serra, G.M.; Goncalves, E.C.; Xavier, L.P.; Santos, A.V. Current Knowledge on Microviridin from Cyanobacteria. Marine Drugs 2021, 19, 17. [Google Scholar] [CrossRef]
- Arnison, P.G.; Bibb, M.J.; Bierbaum, G.; Bowers, A.A.; Bugni, T.S.; Bulaj, G.; Camarero, J.A.; Campopiano, D.J.; Challis, G.L.; Clardy, J.; et al. Ribosomally synthesized and post-translationally modified peptide natural products: Overview and recommendations for a universal nomenclature. Nat. Prod. Rep. 2013, 30, 108–160. [Google Scholar] [CrossRef]
- Rohrlack, T.; Christoffersen, K.; Hansen, P.E.; Zhang, W.; Czarnecki, O.; Henning, M.; Fastner, J.; Erhard, M.; Neilan, B.A.; Kaebernick, M. Isolation, characterization, and quantitative analysis of microviridin J, a new Microcystis metabolite toxic to Daphnia. J. Chem. Ecol. 2003, 29, 1757–1770. [Google Scholar] [CrossRef]
- WHO. Toxic Cyanobacteria in Water, 2nd ed.; CRC Press: Boca Raton, FL, USA, 2021. [Google Scholar] [CrossRef]
- Hollingdale, C.; Thomas, K.; Lewis, N.; Bekri, K.; McCarron, P.; Quilliam, M.A. Feasibility study on production of a matrix reference material for cyanobacterial toxins. Anal. Bioanal. Chem. 2015, 407, 5353–5363. [Google Scholar] [CrossRef]
- Racine, M.; Saleem, A.; Pick, F.R. Metabolome Variation between Strains of Microcystis aeruginosa by Untargeted Mass Spectrometry. Toxins 2019, 11, 723. [Google Scholar] [CrossRef] [Green Version]
- Neumann, U.; Forchert, A.; Flury, T.; Weckesser, J. Microginin FR1, a linear peptide from a water bloom of Microcystis species. Fems Microbiol. Lett. 1997, 153, 475–478. [Google Scholar] [CrossRef]
- Strangman, W.K.; Wright, J.L.C. Microginins 680, 646, and 612-new chlorinated Ahoa-containing peptides from a strain of cultured Microcystis aeruginosa. Tetrahedron Lett. 2016, 57, 1801–1803. [Google Scholar] [CrossRef]
- Zervou, S.-K.; Gkelis, S.; Kaloudis, T.; Hiskia, A.; Mazur-Marzec, H. New microginins from cyanobacteria of Greek freshwaters. Chemosphere 2020, 248, 125961. [Google Scholar] [CrossRef]
- Kraft, M.; Schleberger, C.; Weckesser, J.; Schulz, G.E. Binding structure of the leucine aminopeptidase inhibitor microginin FR1. Febs Lett. 2006, 580, 6943–6947. [Google Scholar] [CrossRef] [Green Version]
- Leikoski, N.; Liu, L.; Jokela, J.; Wahlsten, M.; Gugger, M.; Calteau, A.; Permi, P.; Kerfeld, C.A.; Sivonen, K.; Fewer, D.P. Genome Mining Expands the Chemical Diversity of the Cyanobactin Family to Include Highly Modified Linear Peptides. Chem. Biol. 2013, 20, 1033–1043. [Google Scholar] [CrossRef] [PubMed]
- Sivonen, K.; Leikoski, N.; Fewer, D.P.; Jokela, J. Cyanobactins-ribosomal cyclic peptides produced by cyanobacteria. Appl. Microbiol. Biotechnol. 2010, 86, 1213–1225. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Ziemert, N.; Ishida, K.; Quillardet, P.; Bouchier, C.; Hertweck, C.; de Marsac, N.T.; Dittmann, E. Microcyclamide biosynthesis in two strains of Microcystis aeruginosa: From structure to genes and vice versa. Appl. Environ. Microbiol. 2008, 74, 1791–1797. [Google Scholar] [CrossRef] [Green Version]
- Ishida, K.; Nakagawa, H.; Murakami, M. Microcyclamide, a cytotoxic cyclic hexapeptide from the cyanobacterium Microcystis aeruginosa. J. Nat. Prod. 2000, 63, 1315–1317. [Google Scholar] [CrossRef] [PubMed]
- Portmann, C.; Blom, J.F.; Gademann, K.; Juttner, F. Aerucyclamides A and B: Isolation and synthesis of toxic ribosomal heterocyclic peptides from the cyanobacterium Microcystis aeruginosa PCC 7806. J. Nat. Prod. 2008, 71, 1193–1196. [Google Scholar] [CrossRef] [PubMed]
- Monteiro, P.R.; do Amaral, S.C.; Siqueira, A.S.; Xavier, L.P.; Santos, A.V. Anabaenopeptins: What We Know So Far. Toxins 2021, 13, 522. [Google Scholar] [CrossRef] [PubMed]
- Harada, K.; Fujii, K.; Shimada, T.; Suzuki, M.; Sano, H.; Adachi, K.; Carmichael, W.W. 2 Cyclic-Peptides, anabaenopeptins, A 3rd group of bioactive compounds from the cyanobacterium Anabaena-flos-aquae NRC-525-17. Tetrahedron Letters 1995, 36, 1511–1514. [Google Scholar] [CrossRef]
- Williams, D.E.; Craig, M.; Holmes, C.F.B.; Andersen, R.J. Ferintoic acids A and B, new cyclic hexapeptides from the freshwater cyanobacterium Microcystis aeruginosa. J. Nat. Prod. 1996, 59, 570–575. [Google Scholar] [CrossRef]
- Spoof, L.; Blaszczyk, A.; Meriluoto, J.; Ceglowska, M.; Mazur-Marzec, H. Structures and Activity of New Anabaenopeptins Produced by Baltic Sea Cyanobacteria. Mar. Drugs 2016, 14, 8. [Google Scholar] [CrossRef] [Green Version]
- Pawlik-Skowronska, B.; Bownik, A. Synergistic toxicity of some cyanobacterial oligopeptides to physiological activities of Daphnia magna (Crustacea). Toxicon 2022, 206, 74–84. [Google Scholar] [CrossRef]
- Beversdorf, L.J.; Weirich, C.A.; Bartlett, S.L.; Miller, T.R. Variable Cyanobacterial Toxin and Metabolite Profiles across Six Eutrophic Lakes of Differing Physiochemical Characteristics. Toxins 2017, 9, 62. [Google Scholar] [CrossRef] [Green Version]
- Ersmark, K.; Del Valle, J.R.; Hanessian, S. Chemistry and biology of the aeruginosin family of serine protease inhibitors. Angew. Chem.-Int. Ed. 2008, 47, 1202–1223. [Google Scholar] [CrossRef]
- Ishida, K.; Okita, Y.; Matsuda, H.; Okino, T.; Murakami, M. Aeruginosins, protease inhibitors from the cyanobacterium Microcystis aeruginosa. Tetrahedron 1999, 55, 10971–10988. [Google Scholar] [CrossRef]
- Natumi, R.; Janssen, E.M.L. Cyanopeptide Co-Production Dynamics beyond Mirocystins and Effects of Growth Stages and Nutrient Availability. Environ. Sci. Technol. 2020, 54, 6063–6072. [Google Scholar] [CrossRef]
- Andersen, R. (Ed.) Algal Culturing Techniques, 1st ed.; Elsevier: Amsterdam, The Netherlands, 2005. [Google Scholar]
- Watanabe, M.F.; Harada, K.I.; Matsuura, K.; Watanabe, M.; Suzuki, M. Heptapeptide toxin production during the batch culture of two Microcystis species (Cyanobacteria). J. Appl. Phycol. 1989, 1, 161–165. [Google Scholar] [CrossRef]
- Watanabe, M.F.; Oishi, S. Effects of environmental-factors on toxicity of A cyanobacterium (Microcystis, Aeruginosa) under culture conditions. Appl. Environ. Microbiol. 1985, 49, 1342–1344. [Google Scholar] [CrossRef] [Green Version]
- Carneiro, R.L.; Dorr, F.A.; Dorr, F.; Bortoli, S.; Delherbe, N.; Vasquez, M.; Pinto, E. Co-occurrence of microcystin and microginin congeners in Brazilian strains of Microcystis sp. FEMS Microbiol. Ecol. 2012, 82, 692–702. [Google Scholar] [CrossRef] [Green Version]
- Moustaka-Gouni, M.; Sommer, U. Effects of Harmful Blooms of Large-Sized and Colonial Cyanobacteria on Aquatic Food Webs. Water 2020, 12, 1587. [Google Scholar] [CrossRef]
- Chambers, M.C.; Maclean, B.; Burke, R.; Amodei, D.; Ruderman, D.L.; Neumann, S.; Gatto, L.; Fischer, B.; Pratt, B.; Egertson, J.; et al. A cross-platform toolkit for mass spectrometry and proteomics. Nat. Biotechnol. 2012, 30, 918–920. [Google Scholar] [CrossRef] [PubMed]
- McMillan, A.; Rulisa, S.; Sumarah, M.; Macklaim, J.M.; Renaud, J.; Bisanz, J.E.; Gloor, G.B.; Reid, G. A multi-platform metabolomics approach identifies highly specific biomarkers of bacterial diversity in the vagina of pregnant and non-pregnant women. Sci. Rep. 2015, 5, 14174. [Google Scholar] [CrossRef] [Green Version]
- Scrucca, L.; Fop, M.; Murphy, T.B.; Raftery, A.E. mclust 5: Clustering, Classification and Density Estimation Using Gaussian Finite Mixture Models. R J. 2016, 8, 289–317. [Google Scholar] [CrossRef] [Green Version]
- Nyamundanda, G.; Brennan, L.; Gormley, I.C. Probabilistic principal component analysis for metabolomic data. BMC Bioinform. 2010, 11, 571. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Benjamini, Y.; Hochberg, Y. Controlling the false discovery rate—A practical and powerful approach to multiple testing. J. R. Stat. Soc. Ser. B-Stat. Methodol. 1995, 57, 289–300. [Google Scholar] [CrossRef]
- von Elert, E.; Oberer, L.; Merkel, P.; Huhn, T.; Blom, J.F. Cyanopeptolin 954, a Chlo-rine-Containing Chymotrypsin Inhibitor of Microcystis aeruginosa NIVA Cya 43. J. Nat. Prod. 2005, 68, 1324–1327. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Murakami, M.; Sun, Q.; Ishida, K.; Matsuda, H.; Okino, T.; Yamaguchi, K. Microviridins, elastase inhibitors from the cyanobacte-rium Nostoc minutum (NIES-26). Phytochemistry 1997, 45, 1197–1202. [Google Scholar] [CrossRef]
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McDonald, K.; DesRochers, N.; Renaud, J.B.; Sumarah, M.W.; McMullin, D.R. Metabolomics Reveals Strain-Specific Cyanopeptide Profiles and Their Production Dynamics in Microcystis aeruginosa and M. flos-aquae. Toxins 2023, 15, 254. https://doi.org/10.3390/toxins15040254
McDonald K, DesRochers N, Renaud JB, Sumarah MW, McMullin DR. Metabolomics Reveals Strain-Specific Cyanopeptide Profiles and Their Production Dynamics in Microcystis aeruginosa and M. flos-aquae. Toxins. 2023; 15(4):254. https://doi.org/10.3390/toxins15040254
Chicago/Turabian StyleMcDonald, Kimberlynn, Natasha DesRochers, Justin B. Renaud, Mark W. Sumarah, and David R. McMullin. 2023. "Metabolomics Reveals Strain-Specific Cyanopeptide Profiles and Their Production Dynamics in Microcystis aeruginosa and M. flos-aquae" Toxins 15, no. 4: 254. https://doi.org/10.3390/toxins15040254