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Metabolic Footprinting and Systems Biology: the Medium Is the Message

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Metabolic Footprinting and Systems Biology: the Medium Is the Message Nature Reviews Microbiology | AOP, published online 10 June 2005; doi:10.1038/nrmicro1177 REVIEWS METABOLIC FOOTPRINTING AND SYSTEMS BIOLOGY: THE MEDIUM IS THE MESSAGE Douglas B. Kell*, Marie Brown*, Hazel M. Davey‡, Warwick B. Dunn*, Irena Spasic* and Stephen G. Oliver§ Abstract | One element of classical systems analysis treats a system as a black or grey box, the inner structure and behaviour of which can be analysed and modelled by varying an internal or external condition, probing it from outside and studying the effect of the variation on the external observables. The result is an understanding of the inner make-up and workings of the system. The equivalent of this in biology is to observe what a cell or system excretes under controlled conditions — the ‘metabolic footprint’ or exometabolome — as this is readily and accurately measurable. Here, we review the principles, experimental approaches and scientific outcomes that have been obtained with this useful and convenient strategy. The METABOLOME is defined as the quantitative comple- either the transcriptome or proteome. This is because ment of low-molecular-weight metabolites present in the activities of metabolic pathways are reflected a cell under a given set of physiological conditions1–9. more accurately in the concentrations of pools of It lends itself readily to functional genomic and other metabolites than in the concentrations of the relevant analyses, as changes in a cell’s physiology as a result of enzymes (or indeed the concentrations of the mRNAs gene deletion or overexpression are amplified through encoding them). the hierarchy of the TRANSCRIPTOME and the PROTEOME, Metabolomics is therefore considered to be, in *School of Chemistry, and are therefore more easily measurable through the many senses, more ‘useful’ (that is, ‘discriminatory’) University of Manchester, metabolome, even when changes in metabolic fluxes than transcriptomics and proteomics, for the following Faraday Building, are negligible1,10–12. In addition, the default assump- reasons. Metabolomics is ‘downstream’ — changes in the PO Box 88, Sackville Street, tion underlying transcriptome and proteome analysis metabolome are amplified relative to changes in the tran- Manchester M60 1QD, UK. ‡Institute of Biological — that an x-fold increase in a transcript or protein scriptome and proteome, and are arguably numerically 1 Sciences, University of Wales, necessarily results in an x-fold increase in the effective more tractable . There is no need for a whole genome Cledwyn Building, activity — does not normally reflect reality. At any given sequence or for large expressed-sequence-tag databases Aberystwyth SY23 3DD, UK. time, the rate of an enzymatic reaction is a function of to be available for each species. Metabolic profiling is § Faculty of Life Sciences, the available substrates, products and modifiers as well cheaper and more high-throughput than proteomics University of Manchester, 13 Michael Smith Building, as gene expression , and the formalism of metabolic and transcriptomics, making it feasible to examine Oxford Road, control analysis14–16 tells us that, although changes in large numbers of samples from organisms that have Manchester M13 9PT, UK. the expression level of individual proteins might have been ‘grown’ under a wide range of conditions. Finally, Correspondence to D.B.K. little influence on fluxes, they can and do have large the technology involved in metabolomics is generic, as e-mail: [email protected] effects on the concentrations of intermediary metabo- a given metabolite — unlike a transcript or protein — is doi:10.1038/nrmicro1177 lites. Consequently, the metabolome is expected — and the same in every organism that contains it (other than Published online 10 June 2005 found17 — to be more sensitive to perturbations than for secondary metabolites, as originally defined18). NATURE REVIEWS | MICROBIOLOGY ADVANCE ONLINE PUBLICATION | 1 © 2005 Nature Publishing Group REVIEWS 0.037 METABOLOME ab Nominally all of the small- molecular-weight metabolites in 0.03 a sample. For practical reasons, this is rarely, if ever, achieved using a single extraction 0.024 method, and subsets of metabolites (‘metabolic profiles’) Samples Table of metabolites or peaks 0.018 are more typically obtained. Footprinting analyses TRANSCRIPTOME 0.012 All the mRNA molecules Mean (% total ion current) (transcripts) in a sample. 0.006 PROTEOME Nominally all the proteins in a 0 Chemometrics or machine- sample. This measurement is 50 100 150 200 250 300 350 400 not usually achieved because of Identification learning data processing m/z poor solubilities, especially of Figure 1 | The basis of metabolic footprinting. a | The basic metabolic footprinting strategy, starting with samples and membrane proteins, and proceeding through analysis to data processing until a classification can be effected or a scientific conclusion can be drawn. sometimes protein digests are This can lead to the acquisition and analysis of further samples and subsequent loops around this cycle. b | A typical metabolic used, from which peptides footprint (H.M.D. & D.B.K., unpublished data) using direct-injection positive-ionization low-resolution (to unit mass) electrospray representing the proteome are mass spectrometry54. Shown is the average footprint from 250 single-gene yeast knockout strains. Note that there are peaks at analysed. The concept of the + + proteome should also include every m/z (mass/charge ratio) value. Glucose can be identified at m/z 181, 203 (Na adduct) and 219 (K adduct). Other metabolites tentatively identified are glycerol-NH + (m/z 110), valine (m/z 118), histidine (m/z 156) and phenylalanine-Na+ or all the post-translational 4 + modifications that might occur. methionine-K (m/z 188). CE-MS A technique in which However, measurement of a complete set of intra- As such secretory activities clearly reflect cellular metabolites are separated using cellular microbial metabolites not only requires rapid metabolic activity (and the level of transcription and capillary electrophoresis and quenching of metabolism19,20 and a time-consuming translation of relevant genes), it occurred to us that then analysed using mass spectrometry. Two different runs and often inadequate extraction and separation pro- the global measurement of secreted metabolites might 20–22 are used for cations and anions, cedure , but also the development of a method be exploited to analytical advantage. In particular, whereas neutral molecules can suitable for detecting and quantifying large numbers the rapid quenching required to profile intracellular be separated using techniques of metabolites that can be present at widely differing metabolites would be avoided, as the turnover time that give them an effective charge. concentrations. Although several diverse techniques of metabolites diluted into the greater extracellular have previously been used for this purpose, including space is decreased in proportion to the relative ratios GCMS enzymatic metabolite quantification12, nuclear mag- of extracellular and intracellular volumes. Although A high-resolution analytical netic resonance (NMR) spectroscopy12,23, capillary the characterization of metabolites in microbial cul- technique in which molecules, electrophoresis coupled to mass spectrometry CEMS24, ture broths has already been carried out using various typically derivatized to enhance 50,51 their volatility, are separated gas chromatography coupled to mass spectrometry detection methods (and in culture off-gas using 25–28 48,52,53 and then identified using mass GCMS and liquid chromatography coupled to mass an electronic ‘nose’ ), such analyses were largely spectrometry. spectrometry LCMS29–32, none of these completely ful- confined to specific metabolites and have not been fils the need for an accurate, simple and, in particular, done on a global scale. LCMS METABOLIC FOOTPRINTING54 A technique in which rapid method with a broad dynamic range. We note Consequently, we devised metabolites are separated especially the rapid timescale for the turnover of an as a novel method for the functional analysis and according to their polarity. In intracellular metabolite (the turnover time is approxi- characterization of cells using the metabolome metabolomics, reverse-phase mately equal to the concentration of the metabolite (FIG. 1). Metabolic footprinting as described relies chromatography (in which the divided by the flux through the pathway of which it is not on the measurement of intracellular metabolites column is hydrophobic and an 33 organic solvent such as methanol a member ), which can be under 1 second in microbial (a technique which is widely referred to as METABOLIC 19 55 or acetonitrile is used for systems, even for metabolites at mM concentrations . FINGERPRINTING ) but on the monitoring of metabo- elution) is most popular, lites consumed from, and secreted into, the growth although polar chromato- Metabolite secretion, excretion and footprinting medium by batch cultures of yeast using direct- graphies are also used. It has long been known that microorganisms (and injection MS, in which samples of culture media are 7,23,34,35 METABOLIC FOOTPRINTING humans ) secrete a large number of metabolites injected directly into an electrospray ionization mass A strategy for analysing the into their external environment (especially under con- spectrometer. To maximize the excretion of metabo- properties of cells or tissues by ditions of unbalanced growth). Fermented beverages lites, overflow
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