Profiling planktonic biomass using element-specific, multicomponent nuclear magnetic resonance spectroscopy

Environmental Science and Technology

Volumn 49, Issue 11, 2015, Pages 7056-7062

  Komatsu, Takanori ^a,b   Kobayashi, Toshiya ^b   Hatanaka, Minoru ^c   Kikuchi, Jun ^a,b,d  

^a Elements Chemistry Laboratory   (Japan)

^b YOKOHAMA CITY UNIVERSITY   (Japan)

^c Bruker Corporation   (United States)

^d NAGOYA UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACIDS; ARGININE; BIOGEOCHEMISTRY; DEGRADATION; MAGNETIC RESONANCE SPECTROSCOPY; METABOLISM; MOBILE SECURITY; NUCLEAR MAGNETIC RESONANCE; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PHOTODEGRADATION; QUANTUM THEORY; RESONANCE;

BIOGEOCHEMICAL CYCLE; CHEMICAL SPECIATION TECHNIQUES; CORRELATION SPECTROSCOPY; DIPOLAR ASSISTED ROTATIONAL RESONANCE; ENVIRONMENTAL CHEMICALS; ENVIRONMENTAL RESEARCHES; HETERONUCLEAR SINGLE QUANTUM CORRELATIONS; SOLID-STATE NUCLEAR MAGNETIC RESONANCE;

CHEMICAL SPECIATION;

AMMONIA; ARGININE; ARGININE DEIMINASE; CARBON 13; ELEMENT; ENVIRONMENTAL CHEMICAL; NITROGEN; NITROGEN 15; PHOSPHORUS 31; AMMONIUM DERIVATIVE; CARBON; CULTURE MEDIUM;

AMINO ACID; AMMONIUM; BIOMASS; CARBOHYDRATE; CARBON ISOTOPE; HYDROGEN ISOTOPE; NITROGEN ISOTOPE; NUCLEAR MAGNETIC RESONANCE; PLANKTON; PROTIST; SPECIATION (CHEMISTRY);

AMINATION; ANALYTIC METHOD; ARTICLE; BIOGEOCHEMICAL CYCLE; BIOMASS; CARBON NUCLEAR MAGNETIC RESONANCE; CATABOLISM; CELL METABOLISM; CHEMICAL ANALYSIS; CHEMICAL STRUCTURE; CONTROLLED STUDY; DEGRADATION KINETICS; EUGLENA GRACILIS; HETERONUCLEAR SINGLE QUANTUM COHERENCE; METABOLOMICS; NITROGEN NUCLEAR MAGNETIC RESONANCE; NONHUMAN; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PHOSPHORUS NUCLEAR MAGNETIC RESONANCE; PLANKTON; POLARIZATION; PROTON NUCLEAR MAGNETIC RESONANCE; QUANTITATIVE ANALYSIS; SOLID STATE; STOICHIOMETRY; THREE DIMENSIONAL IMAGING; CULTURE MEDIUM; DRUG EFFECTS; METABOLISM; PHARMACOLOGY; PROCEDURES; SIGNAL PROCESSING;

EUGLENA GRACILIS; PROTISTA;

AMMONIUM COMPOUNDS; BIOMASS; CARBON ISOTOPES; CULTURE MEDIA; ELEMENTS; MAGNETIC RESONANCE SPECTROSCOPY; NITROGEN; PLANKTON; SIGNAL PROCESSING, COMPUTER-ASSISTED;

EID: 84930615736     PISSN: 0013936X     EISSN: 15205851     Source Type: Journal    
DOI: 10.1021/acs.est.5b00837     Document Type: Article

References (64)

1. Sterner, R. W.; Andersen, T.; Elser, J. J.; Hessen, D. O.; Hood, J. M.; McCauley, E.; Urabe, J. Scale-dependent carbon: Nitrogen: Phosphorus seston stoichiometry in marine and freshwaters Limnol. Oceanogr. 2008, 53 (3) 1169-1180
2. Quan, T. M.; Falkowski, P. G. Redox control of N:P ratios in aquatic ecosystems Geobiology 2009, 7 (2) 124-139
3. Hopkinson, C. S.; Vallino, J. J. Efficient export of carbon to the deep ocean through dissolved organic matter Nature 2005, 433 (7022) 142-145
4. Wei, F.; Ito, K.; Sakata, K.; Date, Y.; Kikuchi, J. Pretreatment and integrated analysis of spectral data reveal seaweed similarities based on chemical diversity Anal. Chem. 2015, 87 (5) 2819-2826
5. Ogawa, D. M.; Moriya, S.; Tsuboi, Y.; Date, Y.; Prieto-da-Silva, A. R.; Radis-Baptista, G.; Yamane, T.; Kikuchi, J. Biogeochemical typing of paddy field by a data-driven approach revealing sub-systems within a complex environment-A pipeline to filtrate, organize and frame massive dataset from multi-omics analyses PLoS One 2014, 9 (10) e110723
6. Yoshida, S.; Date, Y.; Akama, M.; Kikuchi, J. Comparative metabolomic and ionomic approach for abundant fishes in estuarine environments of Japan. Sci. Rep. 2014, 4; DOI: 10.1038/srep07005.
7. Asakura, T.; Date, Y.; Kikuchi, J. Comparative analysis of chemical and microbial profiles in estuarine sediments sampled from Kanto and Tohoku regions in Japan Anal. Chem. 2014, 86 (11) 5425-5432
8. Ito, K.; Sakata, K.; Date, Y.; Kikuchi, J. Integrated analysis of seaweed components during seasonal fluctuation by data mining across heterogeneous chemical measurements with network visualization Anal. Chem. 2014, 86 (2) 1098-1105
9. Ogura, T.; Date, Y.; Kikuchi, J. Differences in cellulosic supramolecular structure of compositionally similar rice straw affect biomass metabolism by paddy soil microbiota PLoS One 2013, 8 (6) e66919
10. Everroad, R. C.; Yoshida, S.; Tsuboi, Y.; Date, Y.; Kikuchi, J.; Moriya, S. Concentration of metabolites from low-density planktonic communities for environmental metabolomics using nuclear magnetic resonance spectroscopy J. Visualized Exp. 2012, 62) e3163
11. Simpson, A. J.; Simpson, M. J.; Soong, R. Nuclear magnetic resonance spectroscopy and its key role in environmental research Environ. Sci. Technol. 2012, 46 (21) 11488-11496
12. Ogata, Y.; Chikayama, E.; Morioka, Y.; Everroad, R. C.; Shino, A.; Matsushima, A.; Haruna, H.; Moriya, S.; Toyoda, T.; Kikuchi, J. Ecomics: A web-based toolkit for investigating the biomolecular web in ecosystems using a trans-omics approach PLoS One 2012, 7 (2) e30263
13. Lam, B.; Baer, A.; Alaee, M.; Lefebvre, B.; Moser, A.; Williams, A.; Simpson, A. J. Major structural components in freshwater dissolved organic matter Environ. Sci. Technol. 2007, 41 (24) 8240-8247
14. Mao, J.; Cory, R. M.; McKnight, D. M.; Schmidt-Rohr, K. Characterization of a nitrogen-rich fulvic acid and its precursor algae from solid state NMR Org. Geochem. 2007, 38 (8) 1277-1292
15. Fan, T. W. M.; Lane, A. N. NMR-based stable isotope resolved metabolomics in systems biochemistry J. Biomol. NMR 2011, 49 (3-4) 267-280
16. 13C-labelled bacteria, plants, and animals Anal. Chem. 2011, 83 (3) 719-726
17. 13C-cellulose degradation in an anaerobic microbial ecosystem Molecules 2013, 18 (8) 9021-9033
18. Sekiyama, Y.; Chikayama, E.; Kikuchi, J. Profiling polar and semipolar plant metabolites throughout extraction processes using a combined solution-state and high-resolution magic angle spinning NMR approach Anal. Chem. 2010, 82 (5) 1643-1652
19. Farooq, H.; Courtier-Murias, D.; Soong, R.; Bermel, W.; Kingery, W. M.; Simpson, A. J. HR-MAS NMR spectroscopy: A practical guide for natural samples Curr. Org. Chem. 2013, 17 (24) 3013-3031
20. Beckonert, O.; Coen, M.; Keun, H. C.; Wang, Y. L.; Ebbels, T. M. D.; Holmes, E.; Lindon, J. C.; Nicholson, J. K. High-resolution magic-angle-spinning NMR spectroscopy for metabolic profiling of intact tissues Nat. Protoc. 2010, 5 (6) 1019-1032
21. Renault, M.; Tommassen-van Boxtel, R.; Bos, M. P.; Post, J. A.; Tommassen, J.; Baldus, M. Cellular solid-state nuclear magnetic resonance spectroscopy Proc. Natl. Acad. Sci. U. S. A. 2012, 109 (13) 4863-4868
22. Kikuchi, J.; Williamson, M. P.; Shimada, K.; Asakura, T. Structure and dynamics of photosynthetic membrane-bound proteins in rhodobacter sphaeroides, studied with solid-state NMR spectroscopy Photosynth. Res. 2000, 63 (3) 259-267
23. Courtier-Murias, D.; Farooq, H.; Masoom, H.; Botana, A.; Soong, R.; Longstaffe, J. G.; Simpson, M. J.; Maas, W. E.; Fey, M.; Andrew, B.; Struppe, J.; Hutchins, H.; Krishnamurthy, S.; Kumar, R.; Monette, M.; Stronks, H. J.; Hume, A.; Simpson, A. J. Comprehensive multiphase NMR spectroscopy: Basic experimental approaches to differentiate phases in heterogeneous samples J. Magn. Reson. 2012, 217, 61-76
24. Mao, J.; Palazzo, A. J.; Olk, D. C.; Clapp, C. E.; Senesi, N.; Bashore, T. L.; Cao, X. Chemical structure of soil organic matter in slickspots as investigated by advanced solid-state NMR Soil Sci. 2010, 175 (7) 329-338
25. 13C nuclear magnetic resonance (NMR) spectroscopy Energy Fuels 2011, 25, 388-397
26. Mao, J.; Kong, X.; Schmidt-Rohr, K.; Pignatello, J. J.; Perdue, E. M. Advanced solid-state NMR characterization of marine dissolved organic matter isolated using the coupled reverse osmosis/electrodialysis method Environ. Sci. Technol. 2012, 46 (11) 5806-5814
27. Komatsu, T.; Kikuchi, J. Selective signal detection in solid-state NMR using rotor-synchronized dipolar dephasing for the analysis of hemicellulose in lignocellulosic biomass J. Phys. Chem. Lett. 2013, 4 (14) 2279-2283
28. Okushita, K.; Komatsu, T.; Chikayama, E.; Kikuchi, J. Statistical approach for solid-state NMR spectra of cellulose derived from a series of variable parameters Polym. J. 2012, 44 (8) 895-900
29. Gowda, G. A. N.; Tayyari, F.; Ye, T.; Suryani, Y.; Wei, S.; Shanaiah, N.; Raftery, D. Quantitative analysis of blood plasma metabolites using isotope enhanced NMR methods Anal. Chem. 2010, 82 (21) 8983-8990
30. 15N labeled solid proteins by two- and three-dimensional magic-angle-spinning NMR J. Biomol. NMR 1999, 15 (1) 1-14
31. 13C chemical shift comparison with solid-state NMR Anal. Chem. 2013, 85 (18) 8857-8865
32. Foston, M.; Samuel, R.; Ragauskas, A. J. 13C cell wall enrichment and ionic liquid NMR analysis: Progress towards a high-throughput detailed chemical analysis of the whole plant cell wall Analyst 2012, 137 (17) 3904-3909
33. 13C-labelled cellulose digestion in a lower termite: Insights into gut symbiont function Proc. Biol. Sci. 2014, 281 (1789) 20140990
34. 13C-stable-iotopologue monitoring in initial growth metabolism of Jatropha curcas L Metabolites 2014, 4 (4) 1018-1033
35. Yamazawa, A.; Iikura, T.; Morioka, Y.; Shino, A.; Ogata, Y.; Date, Y.; Kikuchi, J. Cellulose digestion and metabolism induced biocatalytic transitions in anaerobic microbial ecosystems Metabolites 2013, 4 (1) 36-52
36. 14N 2D solid-state NMR: Sub-micro-liter sample data collection in a few minutes J. Magn. Reson. 2011, 208 (1) 44-48
37. Deschamps, M. Ultrafast magic angle spinning nuclear magnetic resonance. In Annual Reports on NMR Spectroscopy; Webb, G. A., Ed., 2014; Vol. 81, pp 109-144.
38. Fung, B. M.; Khitrin, A. K.; Ermolaev, K. An improved broadband decoupling sequence for liquid crystals and solids J. Magn. Reson. 2000, 142 (1) 97-101
39. 15N chemical shift referencing in solid state NMR Solid State Nucl. Magn. Reson. 2014, 61-62, 15-18
40. Lesage, A.; Bardet, M.; Emsley, L. Through-bond carbon-carbon connectivities in disordered solids by NMR J. Am. Chem. Soc. 1999, 121 (47) 10987-10993
41. Hu, B.; Trébosc, J.; Lafon, O.; Chen, Q.; Masuda, Y.; Takegoshi, K.; Amoureux, J.-P. Very-long-distance correlations in proteins revealed by solid-state NMR spectroscopy ChemPhysChem 2012, 13 (16) 3585-3588
42. Mao, K.; Wiench, J. W.; Lin, V. S. Y.; Pruski, M. Indirectly detected through-bond chemical shift correlation NMR spectroscopy in solids under fast MAS: Studies of organic-inorganic hybrid materials J. Magn. Reson. 2009, 196 (1) 92-95
43. Zhou, D. H.; Shah, G.; Cormos, M.; Mullen, C.; Sandoz, D.; Rienstra, C. M. Proton-detected solid-state NMR spectroscopy of fully protonated proteins at 40 kHz magic-angle spinning J. Am. Chem. Soc. 2007, 129 (38) 11791-11801
44. Holland, G. P.; Cherry, B. R.; Jenkins, J. E.; Yarger, J. L. Proton-detected heteronuclear single quantum correlation NMR spectroscopy in rigid solids with ultra-fast MAS J. Magn. Reson. 2010, 202 (1) 64-71
45. 13C correlation NMR for de novo distance determination of solid proteins and application to a human alpha-defensin J. Magn. Reson. 2010, 202 (2) 203-210
46. Bodenhausen, G.; Ruben, D. J. Natural abundance nitrogen-15 NMR by enhanced heteronuclear spectroscopy Chem. Phys. Lett. 1980, 69 (1) 185-189
47. Lerner, L.; Bax, A. Sensitivity-enhanced two-dimensional heteronuclear relayed coherence transfer NMR spectroscopy J. Magn. Reson. 1986, 69 (2) 375-380
48. 13C NMR with signal enhancement by multiple cross polarization J. Magn. Reson. 2014, 239, 44-49
49. Monfils, A. K.; Triemer, R. E.; Bellairs, E. F. Characterization of paramylon morphological diversity in photosynthetic euglenoids (euglenales, euglenophyta) Phycologia 2011, 50 (2) 156-169
50. Kobayashi, K.; Kimura, S.; Togawa, E.; Wada, M.; Kuga, S. Crystal transition of paramylon with dehydration and hydration Carbohydr. Polym. 2010, 80 (2) 491-497
51. 13C NMR-spectroscopy Macromolecules 1989, 22 (10) 3892-3898
52. 1H solid-state NMR Solid State Nucl. Magn. Reson. 2012, 41 (0) 1-27
53. Lesage, A.; Sakellariou, D.; Steuernagel, S.; Emsley, L. Carbon-proton chemical shift correlation in solid-state NMR by through-bond multiple-quantum spectroscopy J. Am. Chem. Soc. 1998, 120 (50) 13194-13201
54. Lesage, A.; Emsley, L. Through-bond heteronuclear single-quantum correlation spectroscopy in solid-state NMR, and comparison to other through-bond and through-space experiments J. Magn. Reson. 2001, 148 (2) 449-454
55. Mao, K. M.; Pruski, M. Directly and indirectly detected through-bond heteronuclear correlation solid-state NMR spectroscopy under fast MAS J. Magn. Reson. 2009, 201 (2) 165-174
56. Sumida, S.; Ehara, T.; Osafune, T.; Hase, E. Ammonia-induced and light-induced degradation of paramylum in Euglena gracilis Plant Cell Physiol. 1987, 28 (8) 1587-1592
57. Park, B. S.; Hirotani, A.; Nakano, Y.; Kitaoka, S. The physiological-role and catabolism of arginine in Euglena gracilis Agric. Biol. Chem. 1983, 47 (11) 2561-2567
58. 14N} NMR investigation of the major nitrogen-containing segment in an aquatic fulvic acid: Evidence for a hydantoin derivative Magn. Reson. Chem. 2011, 49 (12) 775-780
59. Miyatake, K.; Kitaoka, S. NADH-dependent glutamate synthase in Euglena-gracilis Z Agric. Biol. Chem. 1981, 45 (7) 1727-1729
60. Fayyazchaudhary, M.; Javed, Q.; Merrett, M. J. Effect of growth-conditions on NADPH-specific glutamate-dehydrogenase activity of Euglena gracilis New Phytol. 1985, 101 (3) 367-376
61. Cade-Menun, B. J. Characterizing phosphorus in environmental and agricultural samples by 31p nuclear magnetic resonance spectroscopy Talanta 2005, 66 (2) 359-371
62. Mahapatra, D. M.; Chanakya, H. N.; Ramachandra, T. V. Euglena sp as a suitable source of lipids for potential use as biofuel and sustainable wastewater treatment J. Appl. Phycol 2013, 25 (3) 855-865
63. Takeda, K.; Ichijo, N.; Noda, Y.; Takegoshi, K. Elemental analysis by NMR J. Magn. Reson. 2012, 224, 48-52
64. Ichijo, N.; Takeda, K.; Takegoshi, K. Paramagnetic shimming for wide-range variable-field NMR J. Magn. Reson. 2014, 246, 57-61