Advanced solid-state NMR spectroscopy of natural organic matter
Graphical abstract
Introduction
Abundant nonliving natural organic compounds exist in soil, water, and sediment [1], [2], [3], [4], [5], [6]. The generic term for these organic molecules is natural organic matter (NOM). NOM can be involved in agricultural, environmental, geochemical, and energy issues by playing important roles in fundamental processes. For example, in agriculture it controls many physical, chemical and biological processes in soils, such as enhancing soil fertility and improving soil structure [1]. In the environment, it regulates the fate and transport of inorganic and organic pollutants, and thus influences their toxicity [7]. In addition NOM functions as both a sink and source in the global carbon and nitrogen cycles [8]. Fossil fuels such as coal and oil shale still provide a significant proportion of the energy consumed worldwide [9], [10]. Furthermore, there is intense research interest in converting biomass to biorenewable energy products [11].
The first step towards understanding NOM reactivity, properties and functions is to identify its composition and functional groups, which is extremely challenging though, due to the structural complexity and heterogeneity of NOM. Decades of research have shown that NOM is a heterogeneous mixture of various functional units present in charged macromolecules of polydisperse size [4], [12]. These functional units include nonpolar alkyl, carbohydrate-like, protein-like, lignin-like, heterocyclic, and polycyclic aromatic moieties. One new paradigm considers soil NOM as a heterogeneous mixture of physical states with a hierarchy of preferred sites [13]. Although several more hypotheses on NOM structures have been proposed, none of them has been confirmed at the molecular level. Various methods have been used to investigate NOM structure, including chemical degradation, thermal degradation and spectroscopic methods [6], [14], [15]. Although chemical and thermal degradation methods could yield structural information on subunits, the structures of these subunits might be unrepresentative, or even from artifacts, and difficult to relate directly back to the original structures of NOM. Many spectroscopic methods such as infrared (IR), electron paramagnetic resonance, Raman, fluorescence and nuclear magnetic resonance (NMR) spectroscopies have been applied to NOM [1], and it has been established that non-destructive spectroscopic analyses such as NMR spectroscopy are better choices than destructive approaches [16]. Compared to other spectroscopic methods such as IR or Raman spectroscopy, solid-state NMR allows for comprehensive and quantitative structural information to be obtained from NOM, and is therefore arguably one of the most powerful techniques for the comprehensive characterization of NOM.
Both solid- and liquid-state NMR spectroscopy have been extensively used to investigate NOM structure, and have been the topic of several recent excellent reviews [17], [18], [19], [20], [21], [22]. Solution NMR is very useful for studying soluble components in NOM, especially those with low molecular weight. However, compared with solid-state NMR, solution NMR has some disadvantages when applied to NOM: (1) Some NOM samples, or some fractions of NOM, are not soluble; (2) solid-state NMR facilitates a much higher sample concentration than solution NMR, enhancing signals and saving instrument time; making the NOM concentration high enough to achieve a strong signal in the solution state may lead to aggregation, resulting in lower sensitivity, lower resolution, and loss of structural information; (3) solid-state NMR generally requires less sample handling, and is free from solvent effects that may introduce artifact peaks; (4) solid-state NMR is conservative, i.e., it does not consume sample. Solution NMR is not conservative; changes that occur during sample preparation and analysis by solution NMR would void further analyses by other methods; (5) it is much easier and more straightforward to detect nonprotonated carbons using solid-state NMR techniques, while most advanced modern solution NMR techniques employ 1H detection, greatly overemphasizing, in NOM, the signals of protonated carbon sites; (6) in solution NMR, the fast tumbling of molecules averages anisotropic interactions, while in solid-state NMR these anisotropic interactions can be manipulated with specially developed pulse sequences to extract structural information not available from solution NMR; (7) solid-state techniques can identify domains and heterogeneities within NOM structures, while solution NMR cannot; and (8) the macro-molecular structures, aggregates and colloids of NOM slow the tumbling of these molecules, leading to T2 values that are too short to allow many of the pulse sequences of solution NMR to be successfully used. Based on experience with pure organic compounds, one probably has an intuitive notion that solution NMR spectra of complex NOM are of higher resolution than the corresponding solid-state NMR spectra, and that high magnetic fields provide better resolution than lower magnetic fields in solution NMR. However, this does not hold true for NOM samples with inhomogeneous line broadening. Given the aforementioned limitations associated with solution NMR when applied to NOM, solution NMR spectra of NOM should be interpreted with caution; for instance, one should not attempt a complete NOM picture based on partial structures mostly of low-molecular weight and protonated species derived from solution NMR.
Solid-state NMR has been widely employed to study NOM structure, with most studies relying on the routine, at best semi-quantitative 13C cross polarization/magic angle spinning (CP/MAS) technique. This technique has some known limitations, such as non-quantitative peak intensities [23]. The literature indicates additional problems, such as spinning sidebands, baseline distortion, and ambiguous assignments. Recently a number of multi-dimensional techniques and advanced spectral-editing approaches have been applied with great promise for systematically characterizing complex NOM in plants, soils, water, sediments, as well as in the Murchison meteorite [24], and have provided substantial additional information over basic CP/MAS studies alone. Routine 13C solid-state NMR spectra consist of broad and heavily overlapped bands in which functional groups cannot be clearly distinguished. This limitation can generally be overcome by using some spectral-editing techniques that selectively retain certain peaks and eliminate others, clearly revealing specific functional groups. Two-dimensional 1H-13C heteronuclear correlation NMR can be used to identify spatial proximity of different specific functional groups. In addition, 1H spin diffusion can be adopted to detect domains or heterogeneities on a 1- to 50-nm scale, as a basis for realistic structural models of different forms of NOM in the environment. Furthermore, solid-state NMR techniques enable detailed investigations of dynamics over a wide range of motional rates [25], [26]. Application of these advanced NMR techniques has enabled the identification of aliphatic domains, char domains, lignin-derived regions, peptide–sugar components, as well as indications of linked aromatic and sugar rings in NOM. Finally, quantitative structural information can be obtained using direct polarization/magic angle spinning (DP/MAS) and DP/MAS with recoupled dipolar dephasing or multiple cross polarization/MAS (multiCP/MAS) and multiCP with dipolar dephasing [27].
This review is intended to highlight advanced solid-state NMR techniques and their applications to the study of NOM. Section 2 discusses some basics of how to acquire high-quality, quantitative solid-state 13C NMR spectra, and lists some common technical mistakes that lead to unreliable spectra of NOM. Section 3 details the identification of specific functional groups in NOM, primarily based on spectral-editing techniques. In Section 4, the applications of solid-state NMR to investigate nitrogen in NOM are described. Connectivities and proximities are dealt with in Section 5. Section 6 discusses heterogeneity and domains within NOM, as investigated by solid-state NMR techniques such as Goldman-Shen spin diffusion. Segmental dynamics within NOM, which are important for addressing the sorption of organic contaminants, are described in Section 7. In Section 8, we review reported applications of advanced solid-state NMR techniques to study NOM from various sources. Section 9 introduces structural models that are based on NMR-derived structural information. The concluding Section 10 presents a summary as well as an outlook for future research in studies of NOM using NMR spectroscopy.
Section snippets
Basic considerations for acquiring high-quality, quantitative solid-state 13C NMR spectra of natural organic matter (NOM)
Solid-state NMR has been applied to the study of NOM for several decades (see for example, [11], [15], [18], [19], [22], [28], [29], [30], [31], [32], [33], [34], [35]). Nevertheless, the acquisition of high-quality, quantitative 13C spectra of NOM is still not routine for this field, due to technical and access limitations. The most common problems are spinning sidebands and baseline distortion resulting from spectrometer dead-time after single-pulse excitation. These issues have become more
Introduction to spectral-editing techniques
Spectral-editing techniques greatly assist peak assignment and simplify complex spectra [71], [72], [73], [74], [75]. In solution 13C NMR, various spectral-editing techniques such as distortionless enhancement by polarization transfer (DEPT) and the attached-proton test (APT) are used to distinguish CH3, CH2, and CH groups. In the solid state, these J-coupling based spectral-editing techniques are only applicable to crystalline materials with long transverse relaxation times [76], [77], [78].
Solid-state NMR techniques to investigate organic nitrogen in NOM
The nitrogen (N) cycle involves multiple biogeochemical transformations of nitrogen and nitrogen-containing compounds in nature. Nitrogen is essential for many biological processes and is crucial for life on earth. For example, N-containing amino acids are the building blocks of proteins, and N is a key element of the bases in DNA and RNA that make up the genetic code of all life. Therefore, the N cycle is one of the most important topics in biogeochemistry. The major form of nitrogen in soils
Connectivities and proximities
NMR can provide structural information that goes beyond the individual chemical segments discussed so far, because 1H13C dipolar couplings can provide information about internuclear distances on a 6-Å scale. 2D 1H13C HETCOR NMR is a valuable tool for characterizing the environments of carbon sites [160], [161], [162], [163], [164].
Close proximity of different functional groups can be observed using 2D HETCOR and 2D HETCOR with dipolar dephasing. In this way, junctions between different groups
Introduction to heterogeneities and domains
The nanometer-scale chemical heterogeneity of NOM is an important structural aspect of complex organic systems. In particular, it can provide insights into the mechanism for NOM formation: partial survival of biomacromolecules (lignin, polysaccharides, proteins, protective coatings, etc.) would result in heterogeneities on a >1-nm scale, while depolymerization-repolymerization could lead to a more intimate mixing of components. Domain information is also important for the sorption of organic
Importance of information on segmental dynamics
The properties of NOM are affected both by its chemical and physical structures and by segmental dynamics. For example, it has been proposed that both rubbery and glassy components exist in NOM [109], [179], [180]. Rubbery regions in NOM with a glass transition temperature far below ambient temperature can play important roles as excellent sorption environments for organic contaminants [109], [179], [180]. Solid-state NMR provides powerful techniques for characterizing NOM dynamics in detail
Soil organic matter
The chemical nature of soil organic matter (SOM) has attracted considerable attention from chemists and soil scientists for many decades. Its chemical structure has not yet been fully identified, mainly due to the convergence of two intractable issues: the complex (and perhaps nonreproducible) chemical nature of SOM, and the inability to fully separate inorganic soil materials (which interfere with NMR and other analyses) from SOM without potentially altering the intrinsic chemical structure
Structural models based on NMR-derived structural information
In order to advance our understanding of NOM structure, NMR should provide a comprehensive analysis of the chemical composition of the material under investigation. The traditional integration table of functional group composition, in terms of fairly generic structural units, is based on often ambiguous assignments of overlapping peaks and may leave out possibly important components, such as nonprotonated carbons. In addition, many published tables of functional group abundances are derived
Summary and outlook
Advanced solid-state NMR techniques have great potential to elucidate NOM structure at the molecular level, whose significance for NOM cycling in biogeochemical environments can then be assessed. Such a systematic approach enables generation of reliable and quantitative structural information, identification of specific functional groups using spectral-editing techniques, examination of proximities using 2D HETCOR, and investigations of domains and heterogeneities via spin diffusion techniques.
Acknowledgments
Financial support by the NSF (EAR-1226323, EAR-0843996 and CBET-0853950), Petroleum Research Fund Type G Grant (46373-G2), and the Thomas F. Jeffress and Kate Miller Jeffress Memorial Trust is gratefully acknowledged.
Glossary of abbreviations
- APT
- attached-proton test
- CODEX
- centerband-only detection of exchange
- CP/MAS
- cross polarization/magic angle spinning
- CRAMPS
- combined rotation and multiple-pulse spectroscopy
- CSA
- chemical shift anisotropy
- CW
- continuous-wave
- DEPT
- distortionless enhancement by polarization transfer
- DOM
- dissolved organic matter
- DP/MAS
- direct polarization/magic angle spinning
- FID
- free induction decay
- FSLG
- frequency-switched Lee–Goldburg
- HA
- humic acid
- HARDSHIP
- heteronuclear recoupling with dephasing by strong homonuclear interactions of
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