Abstract
Confidently, nuclear magnetic resonance (NMR) is the most informative technique in analytical chemistry and its use as an analytical platform in metabolomics is well proven. This chapter aims to present NMR as a viable tool for microbial metabolomics discussing its fundamental aspects and applications in metabolomics using some chosen examples.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
Similar content being viewed by others
References
Wishart DS (2019) NMR metabolomics: a look ahead. J Magn Reson 306:155–161
Shoulders B (2000) High-resolution NMR techniques in organic chemistry. Tetrahedron organic chemistry series volume 19 by Timothy D. W. Claridge (Dyson Perrins Laborotory, Oxford). Pergamon: Oxford. 1999. ix + 384 pp. Hardbound $134.50, ISBN 0-08-042799-5. Paperback $49.50, ISBN 0-08-042798-7. J Am Chem Soc 122(33):8104–8104
Soares V, Bezerra T, Lafetá R, Borges R, da Silva AJ (2016) Three new steroidal Glycoalkaloids from Solanum pseudoquina A. St.-Hil. (Solanaceae). J Braz Chem Soc 28:782–789
Simmler C, Napolitano JG, McAlpine JB, Chen SN, Pauli GF (2014) Universal quantitative NMR analysis of complex natural samples. Curr Opin Biotechnol 25:51–59
Westwood S, Yamazaki T, Huang T, Garrido B, Ün I, Zhang W, Martos G, Stoppacher N, Saito T, Wielgosz R (2019) Development and validation of a suite of standards for the purity assignment of organic compounds by quantitative NMR spectroscopy. Metrologia 56(6)
Emwas A-HM (2015) The strengths and weaknesses of NMR spectroscopy and mass spectrometry with particular focus on metabolomics research. In: Bjerrum JT (ed) Metabonomics: methods and protocols. Springer New York, New York, pp 161–193
Evard H, Kruve A, Leito I (2016) Tutorial on estimating the limit of detection using LC-MS analysis, part I: theoretical review. Anal Chim Acta 942:23–39
Wang M, Carver JJ, Phelan VV, Sanchez LM, Garg N, Peng Y, Nguyen DD, Watrous J, Kapono CA, Luzzatto-Knaan T, Porto C, Bouslimani A, Melnik AV, Meehan MJ, Liu WT, Crusemann M, Boudreau PD, Esquenazi E, Sandoval-Calderon M, Kersten RD, Pace LA, Quinn RA, Duncan KR, Hsu CC, Floros DJ, Gavilan RG, Kleigrewe K, Northen T, Dutton RJ, Parrot D, Carlson EE, Aigle B, Michelsen CF, Jelsbak L, Sohlenkamp C, Pevzner P, Edlund A, McLean J, Piel J, Murphy BT, Gerwick L, Liaw CC, Yang YL, Humpf HU, Maansson M, Keyzers RA, Sims AC, Johnson AR, Sidebottom AM, Sedio BE, Klitgaard A, Larson CB, Torres-Mendoza CABPD, Gonzalez DJ, Silva DB, Marques LM, Demarque DP, Pociute E, O'Neill EC, Briand E, Helfrich EJN, Granatosky EA, Glukhov E, Ryffel F, Houson H, Mohimani H, Kharbush JJ, Zeng Y, Vorholt JA, Kurita KL, Charusanti P, McPhail KL, Nielsen KF, Vuong L, Elfeki M, Traxler MF, Engene N, Koyama N, Vining OB, Baric R, Silva RR, Mascuch SJ, Tomasi S, Jenkins S, Macherla V, Hoffman T, Agarwal V, Williams PG, Dai J, Neupane R, Gurr J, Rodriguez AMC, Lamsa A, Zhang C, Dorrestein K, Duggan BM, Almaliti J, Allard PM, Phapale P, Nothias LF, Alexandrov T, Litaudon M, Wolfender JL, Kyle JE, Metz TO, Peryea T, Nguyen DT, VanLeer D, Shinn P, Jadhav A, Muller R, Waters KM, Shi W, Liu X, Zhang L, Knight R, Jensen PR, Palsson BO, Pogliano K, Linington RG, Gutierrez M, Lopes NP, Gerwick WH, Moore BS, Dorrestein PC, Bandeira N (2016) Sharing and community curation of mass spectrometry data with global natural products social molecular networking. Nat Biotechnol 34(8):828–837
Steinbeck C, Kuhn S (2004) NMRShiftDB -- compound identification and structure elucidation support through a free community-built web database. Phytochemistry 65(19):2711–2717
Bingol K, Li DW, Bruschweiler-Li L, Cabrera OA, Megraw T, Zhang F, Bruschweiler R (2015) Unified and isomer-specific NMR metabolomics database for the accurate analysis of (13)C-(1)H HSQC spectra. ACS Chem Biol 10(2):452–459
Bingol K, Li DW, Zhang B, Bruschweiler R (2016) Comprehensive metabolite identification strategy using multiple two-dimensional NMR spectra of a complex mixture implemented in the COLMARm web server. Anal Chem 88(24):12411–12418
Sorokina M, Steinbeck C (2020) Review on natural products databases: where to find data in 2020. J Cheminform 12(1):20
Borges RM, Colby SM, Das S, Edison AS, Fiehn O, Kind T, Lee J, Merrill AT, Merz KM Jr, Metz TO, Nunez JR, Tantillo DJ, Wang LP, Wang S, Renslow RS (2021) Quantum chemistry calculations for metabolomics. Chem Rev 121(10):5633–5670
Jonas E, Kuhn S (2019) Rapid prediction of NMR spectral properties with quantified uncertainty. J Cheminform 11(1):50
Luiz Paranhos Costa F, de Albuquerque ACF, Borges RM, dos Santos Junior FM, de Amorim MB (2014) High cost-effectiveness ratio: GIAO-MPW1PW91/6-31G(d)//MPW1PW91/6-31G(d) scaling factor for <SUP>13</SUP>C nuclear magnetic resonance chemical shifts calculation. J Comput Theor Nanosci 11(1):219–225
Kuhn S, Johnson SR (2019) Stereo-aware extension of HOSE codes. ACS Omega 4(4):7323–7329
Hayden HL, Rochfort SJ, Ezernieks V, Savin KW, Mele PM (2019) Metabolomics approaches for the discrimination of disease suppressive soils for Rhizoctonia solani AG8 in cereal crops using (1)H NMR and LC-MS. Sci Total Environ 651(Pt 1):1627–1638
Jousse C, Dalle C, Abila A, Traikia M, Diogon M, Lyan B, El Alaoui H, Vidau C, Delbac F (2020) A combined LC-MS and NMR approach to reveal metabolic changes in the hemolymph of honeybees infected by the gut parasite Nosema ceranae. J Invertebr Pathol 176:107478
Kuhn S, Colreavy-Donnelly S, Santana de Souza J, Borges RM (2019) An integrated approach for mixture analysis using MS and NMR techniques. Faraday Discuss 218:339–353
Leggett A, Wang C, Li DW, Somogyi A, Bruschweiler-Li L, Bruschweiler R (2019) Identification of unknown metabolomics mixture compounds by combining NMR, MS, and cheminformatics. Methods Enzymol 615:407–422
Morgan MA, Griffith CM, Dinges MM, Lyon YA, Julian RR, Larive CK (2019) Evaluating sub-lethal stress from roundup((R)) exposure in Artemia franciscana using (1)H NMR and GC-MS. Aquat Toxicol 212:77–87
Silva EL, Almeida-Lafeta RC, Borges RM, Staerk D (2018) Athenolide a, a new steroidal lactone from the leaves of Athenaea martiana (Solanaceae) determined by means of HPLC-HR-MS-SPE-NMR analysis. Chem Biodivers 15(1)
Tomita S, Nakamura T, Okada S (2018) NMR- and GC/MS-based metabolomic characterization of sunki, an unsalted fermented pickle of turnip leaves. Food Chem 258:25–34
Walker LR, Hoyt DW, Walker SM 2nd, Ward JK, Nicora CD, Bingol K (2016) Unambiguous metabolite identification in high-throughput metabolomics by hybrid 1D (1) H NMR/ESI MS(1) approach. Magn Reson Chem 54(12):998–1003
Blaise BJ, Correia G, Tin A, Young JH, Vergnaud AC, Lewis M, Pearce JT, Elliott P, Nicholson JK, Holmes E, Ebbels TM (2016) Power analysis and sample size determination in metabolic phenotyping. Anal Chem 88(10):5179–5188
Chong J, Soufan O, Li C, Caraus I, Li S, Bourque G, Wishart DS, Xia J (2018) MetaboAnalyst 4.0: towards more transparent and integrative metabolomics analysis. Nucleic Acids Res 46(W1):W486–W494
Halouska S, Zhang B, Gaupp R, Lei S, Snell E, Fenton RJ, Barletta RG, Somerville GA, Powers R (2013) Revisiting protocols for the NMR analysis of bacterial metabolomes. J Integr OMICS 3(2):120–137
Broadhurst D, Goodacre R, Reinke SN, Kuligowski J, Wilson ID, Lewis MR, Dunn WB (2018) Guidelines and considerations for the use of system suitability and quality control samples in mass spectrometry assays applied in untargeted clinical metabolomic studies. Metabolomics 14(6):72
Dunn WB, Broadhurst DI, Edison A, Guillou C, Viant MR, Bearden DW, Beger RD (2017) Quality assurance and quality control processes: summary of a metabolomics community questionnaire. Metabolomics 13(5):1–6
Garcia CJ, Yang X, Huang D, Tomas-Barberan FA (2020) Can we trust biomarkers identified using different non-targeted metabolomics platforms? Multi-platform, inter-laboratory comparative metabolomics profiling of lettuce cultivars via UPLC-QTOF-MS. Metabolomics 16(8):85
Gouveia GJ, Shaver AO, Garcia BM, Morse AM, Andersen EC, Edison AS, McIntyre LM (2021) Long-term metabolomics reference material. Anal Chem 93(26):9193–9199
Maier TS, Kuhn J, Muller C (2010) Proposal for field sampling of plants and processing in the lab for environmental metabolic fingerprinting. Plant Methods 6:6
Deborde C, Moing A, Roch L, Jacob D, Rolin D, Giraudeau P (2017) Plant metabolism as studied by NMR spectroscopy. Prog Nucl Magn Reson Spectrosc 102-103:61–97
Kim HK, Choi YH, Verpoorte R (2010) NMR-based metabolomic analysis of plants. Nat Protoc 5(3):536–549
Nagana Gowda GA, Raftery D (2017) Recent advances in NMR-based metabolomics. Anal Chem 89(1):490–510
Newton JM, Betts EL, Yiangou L, Ortega Roldan J, Tsaousis AD, Thompson GS (2021) Establishing a metabolite extraction method to study the metabolome of blastocystis using NMR. Molecules 26(11):3285
Robinette SL, Brüschweiler R, Schroeder FC, Edison AS (2012) NMR in metabolomics and natural products research: two sides of the same coin. Acc Chem Res 45(2):288–297
Schripsema J (2010) Application of NMR in plant metabolomics: techniques, problems and prospects. Phytochem Anal 21(1):14–21
Wang C, Timari I, Zhang B, Li DW, Leggett A, Amer AO, Bruschweiler-Li L, Kopec RE, Bruschweiler R (2020a) COLMAR lipids web server and ultrahigh-resolution methods for two-dimensional nuclear magnetic resonance- and mass spectrometry-based Lipidomics. J Proteome Res 19(4):1674–1683
Wang R, Li B, Lam SM, Shui G (2020b) Integration of lipidomics and metabolomics for in-depth understanding of cellular mechanism and disease progression. J Genet Genomics 47(2):69–83
Wist J (2017) Complex mixtures by NMR and complex NMR for mixtures: experimental and publication challenges. Magn Reson Chem 55(1):22–28
Zacharias HU, Altenbuchinger M, Gronwald W (2018) Statistical analysis of NMR metabolic fingerprints: established methods and recent advances. Meta 8(3)
Zabek A, Klimek-Ochab M, Jawien E, Mlynarz P (2017) Biodiversity in targeted metabolomics analysis of filamentous fungal pathogens by (1)H NMR-based studies. World J Microbiol Biotechnol 33(7):132
Palama TL, Canard I, Rautureau GJ, Mirande C, Chatellier S, Elena-Herrmann B (2016) Identification of bacterial species by untargeted NMR spectroscopy of the exo-metabolome. Analyst 141(15):4558–4561
Beltran A, Suarez M, Rodriguez MA, Vinaixa M, Samino S, Arola L, Correig X, Yanes O (2012) Assessment of compatibility between extraction methods for NMR- and LC/MS-based metabolomics. Anal Chem 84(14):5838–5844
Mielko KA, Jablonski SJ, Lukaszewicz M, Mlynarz P (2021) Comparison of bacteria disintegration methods and their influence on data analysis in metabolomics. Sci Rep 11(1):20859
Dong C, Reilly DK, Bergame C, Dolke F, Srinivasan J, von Reuss SH (2018) Comparative ascaroside profiling of Caenorhabditis exometabolomes reveals species-specific (omega) and (omega - 2)-hydroxylation downstream of peroxisomal beta-oxidation. J Org Chem 83(13):7109–7120
Lugo Charriez K, Soledade Lemos L, Carrazana Y, Rodriguez-Casariego JA, Eirin-Lopez JM, Hauser-Davis RA, Gardinali P, Quinete N (2021) Application of an improved chloroform-free lipid extraction method to staghorn coral (Acropora cervicornis) lipidomics assessments. Bull Environ Contam Toxicol 107:92–99
Shiva S, Enninful R, Roth MR, Tamura P, Jagadish K, Welti R (2018) An efficient modified method for plant leaf lipid extraction results in improved recovery of phosphatidic acid. Plant Methods 14:14
Edison AS, Colonna M, Gouveia GJ, Holderman NR, Judge MT, Shen X, Zhang S (2021) NMR: unique strengths that enhance modern metabolomics research. Anal Chem 93(1):478–499
Emwas AH, Roy R, McKay RT, Tenori L, Saccenti E, Gowda GAN, Raftery D, Alahmari F, Jaremko L, Jaremko M, Wishart DS (2019) NMR spectroscopy for metabolomics research. Meta 9(7):123
Forseth RR, Schroeder FC (2011) NMR-spectroscopic analysis of mixtures: from structure to function. Curr Opin Chem Biol 15(1):38–47
Hansen AL, Kupce ER, Li DW, Bruschweiler-Li L, Wang C, Bruschweiler R (2021) 2D NMR-based metabolomics with HSQC/TOCSY NOAH supersequences. Anal Chem 93(15):6112–6119
Malet-Martino M, Holzgrabe U (2011) NMR techniques in biomedical and pharmaceutical analysis. J Pharm Biomed Anal 55(1):1–15
Giraudeau P, Silvestre V, Akoka S (2015) Optimizing water suppression for quantitative NMR-based metabolomics: a tutorial review. Metabolomics 11(5):1041–1055
Simpson AJ, Brown SA (2005) Purge NMR: effective and easy solvent suppression. J Magn Reson 175(2):340–346
Le Guennec A, Tayyari F, Edison AS (2017) Alternatives to nuclear overhauser enhancement spectroscopy presat and Carr-Purcell-Meiboom-Gill presat for NMR-based metabolomics. Anal Chem 89(17):8582–8588
Meiboom S, Gill D (1958) Modified spin-Echo method for measuring nuclear relaxation times. Rev Sci Instrum 29(8):688–691
Aguilar JA, Nilsson M, Bodenhausen G, Morris GA (2012) Spin echo NMR spectra without J modulation. Chem Commun 48(6):811–813
Ferretti JA, Highet RJ, Pohl LR, Monks TJ, Hinson JA (1985) Two-dimensional J-resolved nuclear magnetic resonance spectral study of two bromobenzene glutathione conjugates. Environ Health Perspect 61:139–145
Huang Y, Zhang Z, Chen H, Feng J, Cai S, Chen Z (2015) A high-resolution 2D J-resolved NMR detection technique for metabolite analyses of biological samples. Sci Rep 5(1):8390
Kuhn S, Colreavy-Donnelly S, de Andrade Silva Quaresma LE, de Andrade Silva Quaresma E, Borges RM (2020) Applying NMR compound identification using NMRfilter to match predicted to experimental data. Metabolomics 16(12):123
Bakiri A, Hubert J, Reynaud R, Lanthony S, Harakat D, Renault JH, Nuzillard JM (2017) Computer-aided (13)C NMR chemical profiling of crude natural extracts without fractionation. J Nat Prod 80(5):1387–1396
Bruguiere A, Derbre S, Coste C, Le Bot M, Siegler B, Leong ST, Sulaiman SN, Awang K, Richomme P (2018) (13)C-NMR dereplication of Garcinia extracts: predicted chemical shifts as reliable databases. Fitoterapia 131:59–64
Clendinen CS, Pasquel C, Ajredini R, Edison AS (2015) (13)C NMR metabolomics: INADEQUATE network analysis. Anal Chem 87(11):5698–5706
Emwas AH, Saccenti E, Gao X, McKay RT, Dos Santos V, Roy R, Wishart DS (2018) Recommended strategies for spectral processing and post-processing of 1D (1)H-NMR data of biofluids with a particular focus on urine. Metabolomics 14(3):31
Palaric C, Pilard S, Fontaine JX, Boccard J, Mathiron D, Rigaud S, Cailleu D, Mesnard F, Gut Y, Renaud T, Petit A, Beaumal JY, Molinie R (2019) Processing of NMR and MS metabolomics data using chemometrics methods: a global tool for fungi biotransformation reactions monitoring. Metabolomics 15(8):107
Hendriks MMWB, van Eeuwijk FA, Jellema RH, Westerhuis JA, Reijmers TH, Hoefsloot HCJ, Smilde AK (2011) Data-processing strategies for metabolomics studies. TrAC Trends Anal Chem 30(10):1685–1698
van den Berg RA, Hoefsloot HC, Westerhuis JA, Smilde AK, van der Werf MJ (2006) Centering, scaling, and transformations: improving the biological information content of metabolomics data. BMC Genomics 7:142
Dieterie F, Ross A, Schlotterbeck G, Senn H (2006) Probabilistic quotient normalization as robust method to account for dilution of complex biological mixtures. Application in 1H NMR metabonomics. Anal Chem 78:4281–4290
Jackson JE (1991) Scaling of data. John Wiley & Sons, Inc
Blaise BJ, Correia GDS, Haggart GA, Surowiec I, Sands C, Lewis MR, Pearce JTM, Trygg J, Nicholson JK, Holmes E, Ebbels TMD (2021) Statistical analysis in metabolic phenotyping. Nat Protoc 16(9):4299–4326
Keun HC, Ebbels TMD, Antti H, Bollard ME, Beckonert O, Holmes E, Lindon JC, Nicholson JK (2003) Improved analysis of multivariate data by variable stability scaling: application to NMR-based metabolic profiling. Anal Chim Acta 490(1–2):265–276
Bararpour N, Gilardi F, Carmeli C, Sidibe J, Ivanisevic J, Caputo T, Augsburger M, Grabherr S, Desvergne B, Guex N, Bochud M, Thomas A (2020) Visualization and normalization of drift effect across batches in metabolome-wide association studies. BioRxiv
Kohl SM, Klein MS, Hochrein J, Oefner PJ, Spang R, Gronwald W (2012) State-of-the art data normalization methods improve NMR-based metabolomic analysis. Metabolomics 8(Suppl 1):146–160
Reinhold D, Pielke-Lombardo H, Jacobson S, Ghosh D, Kechris K (2019) Pre-analytic considerations for mass spectrometry-based untargeted metabolomics data. Methods Mol Biol 1978:323–340
Silva LP, Lorenzi PL, Purwaha P, Yong V, Hawke DH, Weinstein JN (2013) Measurement of DNA concentration as a normalization strategy for metabolomic data from adherent cell lines. Anal Chem 85(20):9536–9542
Barnes S, Benton HP, Casazza K, Cooper SJ, Cui X, Du X, Engler J, Kabarowski JH, Li S, Pathmasiri W, Prasain JK, Renfrow MB, Tiwari HK (2016a) Training in metabolomics research. I. Designing the experiment, collecting and extracting samples and generating metabolomics data. J Mass Spectrom 51(7):461–475
Barnes S, Benton HP, Casazza K, Cooper SJ, Cui X, Du X, Engler J, Kabarowski JH, Li S, Pathmasiri W, Prasain JK, Renfrow MB, Tiwari HK (2016b) Training in metabolomics research. II. Processing and statistical analysis of metabolomics data, metabolite identification, pathway analysis, applications of metabolomics and its future. J Mass Spectrom 51(8):535–548
Fay DS, Gerow K (2013) A biologist’s guide to statistical thinking and analysis. In: WormBook, pp 1–54
Gromski PS, Muhamadali H, Ellis DI, Xu Y, Correa E, Turner ML, Goodacre R (2015) A tutorial review: metabolomics and partial least squares-discriminant analysis--a marriage of convenience or a shotgun wedding. Anal Chim Acta 879:10–23
Mutihac L, Mutihac R (2008) Mining in chemometrics. Anal Chim Acta 612(1):1–18
Sumner LW, Mendes P, Dixon RA (2003) Plant metabolomics: large-scale phytochemistry in the functional genomics era. Phytochemistry 62(6):817–836
Wishart DS (2008) Quantitative metabolomics using NMR. TrAC Trends Anal Chem 27(3):228–237
Worley B, Powers R (2016) PCA as a practical indicator of OPLS-DA model reliability. Curr Metabolomics 4(2):97–103
Selegato DM, Freire RT, Tannús A, Castro-Gamboa I (2016) New Dereplication method applied to NMR-based metabolomics on different Fusarium species isolated from rhizosphere of Senna spectabilis. J Braz Chem Soc 27:1421–1431
Kumar N, Bansal A, Sarma GS, Rawal RK (2014) Chemometrics tools used in analytical chemistry: an overview. Talanta 123:186–199
Bevilacqua M, Bro R (2020) Can we trust score plots? Meta 10(7)
Westerhuis JA, Hoefsloot HCJ, Smit S, Vis DJ, Smilde AK, van Velzen EJJ, van Duijnhoven JPM, van Dorsten FA (2008) Assessment of PLSDA cross validation. Metabolomics 4(1):81–89
Ghosh T, Zhang W, Ghosh D, Kechris K (2020) Predictive modeling for metabolomics data. Methods Mol Biol 2104:313–336
Skinner SP, Fogh RH, Boucher W, Ragan TJ, Mureddu LG, Vuister GW (2016) CcpNmr AnalysisAssign: a flexible platform for integrated NMR analysis. J Biomol NMR 66(2):111–124
Maciejewski MW, Schuyler AD, Gryk MR, Moraru PR II, Romero EL, Ulrich HR, Eghbalnia M, Livny FD, Hoch JC (2017) NMRbox: a resource for biomolecular NMR computation. Biophys J 112(8):1529–1534
Worley B, Powers R (2014) MVAPACK: a complete data handling package for NMR metabolomics. ACS Chem Biol 9(5):1138–1144
Wishart DS, Tzur D, Knox C, Eisner R, Guo AC, Young N, Cheng D, Jewell K, Arndt D, Sawhney S, Fung C, Nikolai L, Lewis M, Coutouly MA, Forsythe I, Tang P, Shrivastava S, Jeroncic K, Stothard P, Amegbey G, Block D, Hau DD, Wagner J, Miniaci J, Clements M, Gebremedhin M, Guo N, Zhang Y, Duggan GE, Macinnis GD, Weljie AM, Dowlatabadi R, Bamforth F, Clive D, Greiner R, Li L, Marrie T, Sykes BD, Vogel HJ, Querengesser L (2007) HMDB: the human metabolome database. Nucleic Acids Res 35(Database issue):D521–D526
Sajed T, Marcu A, Ramirez M, Pon A, Guo AC, Knox C, Wilson M, Grant JR, Djoumbou Y, Wishart DS (2016) ECMDB 2.0: a richer resource for understanding the biochemistry of E. coli. Nucleic Acids Res 44(D1):D495–D501
Reher R, Kim HW, Zhang C, Mao HH, Wang M, Nothias LF, Caraballo-Rodriguez AM, Glukhov E, Teke B, Leao T, Alexander KL, Duggan BM, Van Everbroeck EL, Dorrestein PC, Cottrell GW, Gerwick WH (2020) A convolutional neural network-based approach for the rapid annotation of molecularly diverse natural products. J Am Chem Soc 142(9):4114–4120
Egan JM, van Santen JA, Liu DY, Linington RG (2021) Development of an NMR-based platform for the direct structural annotation of complex natural products mixtures. J Nat Prod 84(4):1044–1055
Wishart, D. S., Z. Sayeeda, Z. Budinski, A. Guo, B. L. Lee, M. Berjanskii, M. Rout, H. Peters, R. Dizon, R. Mah, C. Torres-Calzada, M. Hiebert-Giesbrecht, D. Varshavi, D. Varshavi, E. Oler, D. Allen, X. Cao, V. Gautam, A. Maras, Ella F. Poynton, P. Tavangar, V. Yang, Jeffrey A. van Santen, R. Ghosh, S. Sarma, E. Knutson, V. Sullivan, Amy M. Jystad, R. Renslow, Lloyd W. Sumner, Roger G. Linington and John R. Cort (2021). "NP-MRD: the natural products magnetic resonance database." Nucleic Acids Res
Mielko KA, Jabłoński SJ, Wojtowicz W, Milczewska J, Sands D, Łukaszewicz M, Młynarz P (2020) Possible metabolic switch between environmental and pathogenic Pseudomonas aeruginosa strains: 1H NMR based metabolomics study. J Pharm Biomed Anal 188:113369
Borchert AJ, Gouveia GJ, Edison AS, Downs DM (2020) Proton nuclear magnetic resonance metabolomics corroborates serine Hydroxymethyltransferase as the primary target of 2-Aminoacrylate in a ridA mutant of salmonella enterica. mSystems 5(2):10–1128
Marshall DD, Halouska S, Zinniel DK, Fenton RJ, Kenealy K, Chahal HK, Rathnaiah G, Barletta RG, Powers R (2017) Assessment of metabolic changes in mycobacterium smegmatis wild-type and alr mutant strains: evidence of a new pathway of d-alanine biosynthesis. J Proteome Res 16(3):1270–1279
Betancur LA, Forero AM, Vinchira-Villarraga DM, Cardenas JD, Romero-Otero A, Chagas FO, Pupo MT, Castellanos L, Ramos FA (2020) NMR-based metabolic profiling to follow the production of anti-phytopathogenic compounds in the culture of the marine strain Streptomyces sp. PNM-9. Microbiol Res 239:126507
Carvalho FV, Fonseca Santana L, Diogenes A d SV, Costa SL, Zambotti-Villelae L, Colepicolo P, Ferraz CG, Ribeiro PR (2021) Combination of a multiplatform metabolite profiling approach and chemometrics as a powerful strategy to identify bioactive metabolites in Lepidium meyenii (Peruvian maca). Food Chem 364:130453
Kellogg JJ, Cech NB (2020) Uncovering bioactive natural products via biochemometric methodologies. In: Comprehensive natural products III, pp 271–279
Ory L, Nazih EH, Daoud S, Mocquard J, Bourjot M, Margueritte L, Delsuc MA, Bard JM, Pouchus YF, Bertrand S, Roullier C (2019) Targeting bioactive compounds in natural extracts - development of a comprehensive workflow combining chemical and biological data. Anal Chim Acta 1070:29–42
Wen C, Wang D, Li X, Huang T, Huang C, Hu K (2018) Targeted isolation and identification of bioactive compounds lowering cholesterol in the crude extracts of crabapples using UPLC-DAD-MS-SPE/NMR based on pharmacology-guided PLS-DA. J Pharm Biomed Anal 150:144–151
Liu M, Grkovic T, Liu X, Han J, Zhang L, Quinn RJ (2017a) A systems approach using OSMAC, Log P and NMR fingerprinting: an approach to novelty. Synth Syst Biotechnol 2(4):276–286
Fernand MG, Roullier C, Guitton Y, Lalande J, Lacoste S, Dupont J, Ruiz N, Pouchus YF, Raheriniaina C, Ranaivoson E (2017) Fungi isolated from Madagascar shrimps - investigation of the aspergillus Niger metabolism by combined LC-MS and NMR metabolomics studies. Aquaculture 479:750–758
Chen L, Zhao X, Wu J, Liu Q, Pang X, Yang H (2020) Metabolic characterisation of eight Escherichia coli strains including “Big Six” and acidic responses of selected strains revealed by NMR spectroscopy. Food Microbiol 88:103399
Aries ML, Cloninger MJ (2020) NMR metabolomic analysis of bacterial resistance pathways using multivalent quaternary ammonium functionalized macromolecules. Metabolomics 16(8):82
Liu Q, Wu JE, Lim ZY, Aggarwal A, Yang H, Wang S (2017b) Evaluation of the metabolic response of Escherichia coli to electrolysed water by 1 H NMR spectroscopy. LWT Food Sci Technol 79:428–436
Rona GB, Almeida NP, Santos GC Jr, Fidalgo TK, Almeida FC, Eleutherio EC, Pinheiro AS (2019) (1) H NMR metabolomics reveals increased glutaminolysis upon overexpression of NSD3s or Pdp3 in Saccharomyces cerevisiae. J Cell Biochem 120(4):5377–5385
Imai A, Lankin DC, Godecke T, Chen SN, Pauli GF (2020) Differentiation of Actaea species by NMR metabolomics analysis. Fitoterapia 146:104686
Kroymann J (2011) Natural diversity and adaptation in plant secondary metabolism. Curr Opin Plant Biol 14(3):246–251
Leiss KA, Choi YH, Verpoorte R, Klinkhamer PG (2011) An overview of NMR-based metabolomics to identify secondary plant compounds involved in host plant resistance. Phytochem Rev 10(2):205–216
Nephali L, Piater LA, Dubery IA, Patterson V, Huyser J, Burgess K, Tugizimana F (2020) Biostimulants for plant growth and mitigation of abiotic stresses: a metabolomics perspective. Meta 10(12)
Schauer N, Fernie AR (2006) Plant metabolomics: towards biological function and mechanism. Trends Plant Sci 11(10):508–516
Zulak KG, Weljie AM, Vogel HJ, Facchini PJ (2008) Quantitative 1H NMR metabolomics reveals extensive metabolic reprogramming of primary and secondary metabolism in elicitor-treated opium poppy cell cultures. BMC Plant Biol 8:5
Shaver AO, Gouveia GJ, Kirby PS, Andersen EC, Edison AS (2021) Culture and assay of large-scale mixed-stage Caenorhabditis elegans populations. JoVE 171:e61453
Polozsányi Z, Kaliňák M, Babjak M, Šimkovič M, Varečka Ľ (2021) How to enter the state of dormancy? A suggestion by Trichoderma atroviride conidia. Fungal Biol 125(11):934–949
Judge MT, Wu Y, Tayyari F, Hattori A, Glushka J, Ito T, Arnold J, Edison AS (2019) Continuous in vivo metabolism by NMR. Front Mol Biosci 6:26
Koczula KM, Ludwig C, Hayden R, Cronin L, Pratt G, Parry H, Tennant D, Drayson M, Bunce CM, Khanim FL, Gunther UL (2016) Metabolic plasticity in CLL: adaptation to the hypoxic niche. Leukemia 30(1):65–73
Dalisay DS, Rogers EW, Edison AS, Molinski TF (2009) Structure elucidation at the nanomole scale. 1. Trisoxazole macrolides and thiazole-containing cyclic peptides from the nudibranch Hexabranchus sanguineus. J Nat Prod 72(4):732–738
Pintér G, Schwalbe H (2017) Unprecedented carbon signal enhancement in liquid-state NMR spectroscopy. Angew Chem Int Ed 56(29):8332–8334
Delaglio F, Walker GS, Farley KA, Sharma R, Hoch JC, Arbogast LW, Brinson RG, Marino JP (2017) Non-uniform sampling for all: more NMR spectral quality, less measurement time <non-uniform sampling for all more NMR spectral quality, less measurement time.pdf>. Am Pharm Rev 20(4):1–12
Author information
Authors and Affiliations
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2023 The Author(s), under exclusive license to Springer Nature Switzerland AG
About this chapter
Cite this chapter
Borges, R.M., Gouveia, G.J., das Chagas, F.O. (2023). Advances in Microbial NMR Metabolomics. In: Pacheco Fill, T. (eds) Microbial Natural Products Chemistry. Advances in Experimental Medicine and Biology(), vol 1439. Springer, Cham. https://doi.org/10.1007/978-3-031-41741-2_6
Download citation
DOI: https://doi.org/10.1007/978-3-031-41741-2_6
Published:
Publisher Name: Springer, Cham
Print ISBN: 978-3-031-41740-5
Online ISBN: 978-3-031-41741-2
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)