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Journal articles on the topic 'Protein-Based Stable Isotope Probing'

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Published: 1 July 2021

Last updated: 6 February 2022

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1

Jehmlich, Nico, Frank Schmidt, Martin Taubert, Jana Seifert, Felipe Bastida, Martin von Bergen, Hans-Hermann Richnow, and Carsten Vogt. "Protein-based stable isotope probing." Nature Protocols 5, no. 12 (November 18, 2010): 1957–66. http://dx.doi.org/10.1038/nprot.2010.166.

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Seifert, Jana, Martin Taubert, Nico Jehmlich, Frank Schmidt, Uwe Völker, Carsten Vogt, Hans-Hermann Richnow, and Martin von Bergen. "Protein-based stable isotope probing (protein-SIP) in functional metaproteomics." Mass Spectrometry Reviews 31, no. 6 (March 15, 2012): 683–97. http://dx.doi.org/10.1002/mas.21346.

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Hungate, Bruce A., Rebecca L. Mau, Egbert Schwartz, J. Gregory Caporaso, Paul Dijkstra, Natasja van Gestel, Benjamin J. Koch, et al. "Quantitative Microbial Ecology through Stable Isotope Probing." Applied and Environmental Microbiology 81, no. 21 (August 21, 2015): 7570–81. http://dx.doi.org/10.1128/aem.02280-15.

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ABSTRACTBacteria grow and transform elements at different rates, and as yet, quantifying this variation in the environment is difficult. Determining isotope enrichment with fine taxonomic resolution after exposure to isotope tracers could help, but there are few suitable techniques. We propose a modification tostableisotopeprobing (SIP) that enables the isotopic composition of DNA from individual bacterial taxa after exposure to isotope tracers to be determined. In our modification, after isopycnic centrifugation, DNA is collected in multiple density fractions, and each fraction is sequenced separately. Taxon-specific density curves are produced for labeled and nonlabeled treatments, from which the shift in density for each individual taxon in response to isotope labeling is calculated. Expressing each taxon's density shift relative to that taxon's density measured without isotope enrichment accounts for the influence of nucleic acid composition on density and isolates the influence of isotope tracer assimilation. The shift in density translates quantitatively to isotopic enrichment. Because this revision to SIP allows quantitative measurements of isotope enrichment, we propose to call it quantitative stable isotope probing (qSIP). We demonstrated qSIP using soil incubations, in which soil bacteria exhibited strong taxonomic variations in18O and13C composition after exposure to [18O]water or [13C]glucose. The addition of glucose increased the assimilation of18O into DNA from [18O]water. However, the increase in18O assimilation was greater than expected based on utilization of glucose-derived carbon alone, because the addition of glucose indirectly stimulated bacteria to utilize other substrates for growth. This example illustrates the benefit of a quantitative approach to stable isotope probing.

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Jehmlich, Nico, Frank Schmidt, Martin von Bergen, Hans-Hermann Richnow, and Carsten Vogt. "Protein-based stable isotope probing (Protein-SIP) reveals active species within anoxic mixed cultures." ISME Journal 2, no. 11 (June 19, 2008): 1122–33. http://dx.doi.org/10.1038/ismej.2008.64.

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Taubert, Martin, Martin von Bergen, and Jana Seifert. "Limitations in detection of 15N incorporation by mass spectrometry in protein-based stable isotope probing (protein-SIP)." Analytical and Bioanalytical Chemistry 405, no. 12 (March 17, 2013): 3989–96. http://dx.doi.org/10.1007/s00216-013-6828-y.

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6

Jehmlich, Nico, Frank Schmidt, Mathias Hartwich, Martin von Bergen, Hans-Hermann Richnow, and Carsten Vogt. "Incorporation of carbon and nitrogen atoms into proteins measured by protein-based stable isotope probing (Protein-SIP)." Rapid Communications in Mass Spectrometry 22, no. 18 (September 30, 2008): 2889–97. http://dx.doi.org/10.1002/rcm.3684.

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7

von Bergen, Martin, Nico Jehmlich, Martin Taubert, Carsten Vogt, Felipe Bastida, Florian-Alexander Herbst, Frank Schmidt, Hans-Hermann Richnow, and Jana Seifert. "Insights from quantitative metaproteomics and protein-stable isotope probing into microbial ecology." ISME Journal 7, no. 10 (May 16, 2013): 1877–85. http://dx.doi.org/10.1038/ismej.2013.78.

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8

Bozinovski, Dragana, Steffi Herrmann, Hans-Hermann Richnow, Martin Bergen, Jana Seifert, and Carsten Vogt. "Functional analysis of an anaerobic m-xylene-degrading enrichment culture using protein-based stable isotope probing." FEMS Microbiology Ecology 81, no. 1 (March 12, 2012): 134–44. http://dx.doi.org/10.1111/j.1574-6941.2012.01334.x.

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9

Wang, Juan, Xian Zhang, and Huaiying Yao. "Optimizing ultracentrifugation conditions for DNA-based stable isotope probing (DNA-SIP)." Journal of Microbiological Methods 173 (June 2020): 105938. http://dx.doi.org/10.1016/j.mimet.2020.105938.

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10

Papp, Katerina, Bruce A. Hungate, and Egbert Schwartz. "Microbial rRNA Synthesis and Growth Compared through Quantitative Stable Isotope Probing with H218O." Applied and Environmental Microbiology 84, no. 8 (February 9, 2018): e02441-17. http://dx.doi.org/10.1128/aem.02441-17.

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ABSTRACTGrowing bacteria have a high concentration of ribosomes to ensure sufficient protein synthesis, which is necessary for genome replication and cellular division. To elucidate whether metabolic activity of soil microorganisms is coupled with growth, we investigated the relationship between rRNA and DNA synthesis in a soil bacterial community using quantitative stable isotope probing (qSIP) with H218O. Most soil bacterial taxa were metabolically active and grew, and there was no significant difference between the isotopic composition of DNA and RNA extracted from soil incubated with H218O. The positive correlation between18O content of DNA and rRNA of taxa, with a slope statistically indistinguishable from 1 (slope = 0.96; 95% confidence interval [CI], 0.90 to 1.02), indicated that few taxa made new rRNA without synthesizing new DNA. There was no correlation between rRNA-to-DNA ratios obtained from sequencing libraries and the atom percent excess (APE)18O values of DNA or rRNA, suggesting that the ratio of rRNA to DNA is a poor indicator of microbial growth or rRNA synthesis. Our results support the notion that metabolic activity is strongly coupled to cellular division and suggest that nondividing taxa do not dominate soil metabolic activity.IMPORTANCEUsing quantitative stable isotope probing of microbial RNA and DNA with H218O, we show that most soil taxa are metabolically active and grow because their nucleic acids are significantly labeled with18O. A majority of the populations that make new rRNA also grow, which argues against the common paradigm that most soil taxa are dormant. Additionally, our results indicate that relative sequence abundance-based RNA-to-DNA ratios, which are frequently used for identifying active microbial populations in the environment, underestimate the number of metabolically active taxa within soil microbial communities.

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Taubert, Martin, Nico Jehmlich, Carsten Vogt, Hans H. Richnow, Frank Schmidt, Martin von Bergen, and Jana Seifert. "Time resolved protein-based stable isotope probing (Protein-SIP) analysis allows quantification of induced proteins in substrate shift experiments." PROTEOMICS 11, no. 11 (May 20, 2011): 2265–74. http://dx.doi.org/10.1002/pmic.201000788.

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12

Uhlík, Ondrej, Katerina Jecná, Mary Beth Leigh, Martina Macková, and Tomas Macek. "DNA-based stable isotope probing: a link between community structure and function." Science of The Total Environment 407, no. 12 (June 2009): 3611–19. http://dx.doi.org/10.1016/j.scitotenv.2008.05.012.

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13

Whiteley, Andrew S., Mike Manefield, and Tillmann Lueders. "Unlocking the ‘microbial black box’ using RNA-based stable isotope probing technologies." Current Opinion in Biotechnology 17, no. 1 (February 2006): 67–71. http://dx.doi.org/10.1016/j.copbio.2005.11.002.

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14

Volkmann, T. H. M., and M. Weiler. "Continual in-situ monitoring of pore water stable isotopes in the subsurface." Hydrology and Earth System Sciences Discussions 10, no. 11 (November 5, 2013): 13293–331. http://dx.doi.org/10.5194/hessd-10-13293-2013.

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Abstract. The stable isotope signature of pore water provides an integral fingerprint of water origin, flow path, transport processes, and residence times and can thus serve as a powerful tracer of hydrological processes in the unsaturated and saturated zone. However, the full potential of stable isotopes to quantitatively characterize subsurface water dynamics is yet unfolded due to the difficulty in obtaining extensive detailed and continual measurements of spatiotemporally variable pore water signatures. With the development of field-deployable laser-based isotope analyzers, such measurements are now becoming feasible. This study presents the development and application of a functional, automatable, and cost-efficient system for non-destructive continual in-situ monitoring of pore water stable isotope signatures with high resolution. The monitoring system uses automatic-controllable valve arrays to continuously extract diluted soil air water vapor via a branching network of multiple small microporous probes into a commercial isotope analyzer. Soil temperature observations are used to convert obtained vapor phase into liquid phase water isotope signatures, but these can also be obtained based on vapor concentration measurements. In-situ sampling was conducted at six depths for each of three plots planted with varying vegetation on an experimental site in SW Germany. Two different methods based on advective and diffusive soil water vapor probing were employed suitable under unsaturated and all (including saturated) moisture conditions, respectively. The advective sampling method was applied using multiple permanently installed probes (continual mode) and using a single probe subsequently inserted to sample the various locations (push-in mode), while the diffusive sampling method was applied in push-in mode only. Using a specific identical treatment onsite calibration approach along with basic corrections for instrument bias and temperature dependent free water-vapor isotopic equilibrium fractionation, the monitoring system facilitated inference of normalized liquid pore water isotopic composition with sufficiently high accuracy and precision at sampling intervals of less than four minutes and resolved the isotopic variability along natural depth profiles. Comparison indicated that the presented in-situ approaches may be used interchangeably with each other and with concurrent laboratory-based direct equilibration measurements of destructively collected samples, such that the choice of method will depend upon the task and anticipated conditions of sampling. The introduced sampling techniques provide powerful tools towards a detailed quantitative understanding of dynamic and heterogeneous shallow subsurface and vadose zone processes.

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Vogt, Carsten, Tillmann Lueders, Hans H. Richnow, Martin Krüger, Martin von Bergen, and Jana Seifert. "Stable Isotope Probing Approaches to Study Anaerobic Hydrocarbon Degradation and Degraders." Journal of Molecular Microbiology and Biotechnology 26, no. 1-3 (2016): 195–210. http://dx.doi.org/10.1159/000440806.

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Stable isotope probing (SIP) techniques have become state-of-the-art in microbial ecology over the last 10 years, allowing for the targeted detection and identification of organisms, metabolic pathways and elemental fluxes active in specific processes within complex microbial communities. For studying anaerobic hydrocarbon-degrading microbial communities, four stable isotope techniques have been used so far: DNA/RNA-SIP, PLFA (phospholipid-derived fatty acids)-SIP, protein-SIP, and single-cell-SIP by nanoSIMS (nanoscale secondary ion mass spectrometry) or confocal Raman microscopy. DNA/RNA-SIP techniques are most frequently applied due to their most meaningful phylogenetic resolution. Especially using <sup>13</sup>C-labeled benzene and toluene as model substrates, many new hydrocarbon degraders have been identified by SIP under various electron acceptor conditions. This has extended the current perspective of the true diversity of anaerobic hydrocarbon degraders relevant in the environment. Syntrophic hydrocarbon degradation was found to be a common mechanism for various electron acceptors. Fundamental concepts and recent advances in SIP are reflected here. A discussion is presented concerning how these techniques generate direct insights into intrinsic hydrocarbon degrader populations in environmental systems and how useful they are for more integrated approaches in the monitoring of contaminated sites and for bioremediation.

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Hatamoto, Masashi, Hiroyuki Imachi, Yuto Yashiro, Akiyoshi Ohashi, and Hideki Harada. "Detection of Active Butyrate-Degrading Microorganisms in Methanogenic Sludges by RNA-Based Stable Isotope Probing." Applied and Environmental Microbiology 74, no. 11 (April 11, 2008): 3610–14. http://dx.doi.org/10.1128/aem.00045-08.

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ABSTRACT Butyrate-degrading bacteria in four methanogenic sludges were studied by RNA-based stable isotope probing. Bacterial populations in the 13C-labeled rRNA fractions were distinct from unlabeled fractions, and Syntrophaceae species, Tepidanaerobacter sp., and Clostridium spp. dominated. These results suggest that diverse microbes were active in butyrate degradation under methanogenic conditions.

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17

Mosbæk, Freya, Henrik Kjeldal, Daniel G. Mulat, Mads Albertsen, Alastair J. Ward, Anders Feilberg, and Jeppe L. Nielsen. "Identification of syntrophic acetate-oxidizing bacteria in anaerobic digesters by combined protein-based stable isotope probing and metagenomics." ISME Journal 10, no. 10 (April 29, 2016): 2405–18. http://dx.doi.org/10.1038/ismej.2016.39.

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18

Taubert, Martin, Sven Baumann, Martin von Bergen, and Jana Seifert. "Exploring the limits of robust detection of incorporation of 13C by mass spectrometry in protein-based stable isotope probing (protein-SIP)." Analytical and Bioanalytical Chemistry 401, no. 6 (August 7, 2011): 1975–82. http://dx.doi.org/10.1007/s00216-011-5289-4.

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19

Xu, Jiangbing, Zhongjun Jia, Xiangui Lin, and Youzhi Feng. "DNA-based stable isotope probing identifies formate-metabolizing methanogenic archaea in paddy soil." Microbiological Research 202 (September 2017): 36–42. http://dx.doi.org/10.1016/j.micres.2017.05.004.

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20

Egert, Markus, Severin Weis, and Sylvia Schnell. "RNA-based stable isotope probing (RNA-SIP) to unravel intestinal host-microbe interactions." Methods 149 (October 2018): 25–30. http://dx.doi.org/10.1016/j.ymeth.2018.05.022.

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21

Azemtsop Matanfack, Georgette, Aikaterini Pistiki, Petra Rösch, and Jürgen Popp. "Raman Stable Isotope Probing of Bacteria in Visible and Deep UV-Ranges." Life 11, no. 10 (September 24, 2021): 1003. http://dx.doi.org/10.3390/life11101003.

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Raman stable isotope probing (Raman-SIP) is an excellent technique that can be used to access the overall metabolism of microorganisms. Recent studies have mainly used an excitation wavelength in the visible range to characterize isotopically labeled bacteria. In this work, we used UV resonance Raman spectroscopy (UVRR) to evaluate the spectral red-shifts caused by the uptake of isotopes (13C, 15N, 2H(D) and 18O) in E. coli cells. Moreover, we present a new approach based on the extraction of labeled DNA in combination with UVRR to identify metabolically active cells. The proof-of-principle study on E. coli revealed heterogeneities in the Raman features of both the bacterial cells and the extracted DNA after labeling with 13C, 15N, and D. The wavelength of choice for studying 18O- and deuterium-labeled cells is 532 nm is, while 13C-labeled cells can be investigated with visible and deep UV wavelengths. However, 15N-labeled cells are best studied at the excitation wavelength of 244 nm since nucleic acids are in resonance at this wavelength. These results highlight the potential of the presented approach to identify active bacterial cells. This work can serve as a basis for the development of new techniques for the rapid and efficient detection of active bacteria cells without the need for a cultivation step.

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22

Herrmann, Elena, Patrick Koch, Christian U. Riedel, Wayne Young, and Markus Egert. "Effect of rotor type on the separation of isotope-labeled and unlabeled Escherichia coli RNA by isopycnic density ultracentrifugation." Canadian Journal of Microbiology 63, no. 1 (January 2017): 83–87. http://dx.doi.org/10.1139/cjm-2016-0483.

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Separation of differentially isotope-labeled bacterial RNA by isopycnic density gradient centrifugation is a critical step in RNA-based stable isotope probing analyses, which help to link the structure and function of complex microbial communities. Using isotope-labeled Escherichia coli RNA, we showed that an 8 mL near-vertical rotor performed better than a 2 mL fixed-angle rotor, thereby corroborating current recommendations. Neither increased concentrations of formamide nor urea in the medium improved the separation results using the fixed-angle rotor.

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23

Feng, Youzhi, Xiangui Lin, Zhongjun Jia, and Jianguo Zhu. "Identification of Formate‐Metabolizing Bacteria in Paddy Soil by DNA‐Based Stable Isotope Probing." Soil Science Society of America Journal 76, no. 1 (January 2012): 121–29. http://dx.doi.org/10.2136/sssaj2011.0216.

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24

Rasche, Frank, Tillmann Lueders, Michael Schloter, Sabine Schaefer, Franz Buegger, Andreas Gattinger, Rebecca C. Hood-Nowotny, and Angela Sessitsch. "DNA-based stable isotope probing enables the identification of active bacterial endophytes in potatoes." New Phytologist 181, no. 4 (December 24, 2008): 802–7. http://dx.doi.org/10.1111/j.1469-8137.2008.02744.x.

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Dumont, Marc G., Bianca Pommerenke, Peter Casper, and Ralf Conrad. "DNA-, rRNA- and mRNA-based stable isotope probing of aerobic methanotrophs in lake sediment." Environmental Microbiology 13, no. 5 (January 24, 2011): 1153–67. http://dx.doi.org/10.1111/j.1462-2920.2010.02415.x.

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Jia, Jing-Xin, Jing-Feng Gao, Hui-Hui Dai, Wen-Zhi Zhang, Da Zhang, and Zhi-Qi Wang. "DNA-based stable isotope probing identifies triclosan degraders in nitrification systems under different surfactants." Bioresource Technology 302 (April 2020): 122815. http://dx.doi.org/10.1016/j.biortech.2020.122815.

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27

Jehmlich, Nico, Frank Schmidt, Martin Taubert, Jana Seifert, Martin von Bergen, Hans-Hermann Richnow, and Carsten Vogt. "Comparison of methods for simultaneous identification of bacterial species and determination of metabolic activity by protein-based stable isotope probing (Protein-SIP) experiments." Rapid Communications in Mass Spectrometry 23, no. 12 (May 15, 2009): 1871–78. http://dx.doi.org/10.1002/rcm.4084.

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28

Xu, Jiabao, Tong Yu, Christos E. Zois, Ji-Xin Cheng, Yuguo Tang, Adrian L. Harris, and Wei E. Huang. "Unveiling Cancer Metabolism through Spontaneous and Coherent Raman Spectroscopy and Stable Isotope Probing." Cancers 13, no. 7 (April 5, 2021): 1718. http://dx.doi.org/10.3390/cancers13071718.

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Metabolic reprogramming is a common hallmark in cancer. The high complexity and heterogeneity in cancer render it challenging for scientists to study cancer metabolism. Despite the recent advances in single-cell metabolomics based on mass spectrometry, the analysis of metabolites is still a destructive process, thus limiting in vivo investigations. Being label-free and nonperturbative, Raman spectroscopy offers intrinsic information for elucidating active biochemical processes at subcellular level. This review summarizes recent applications of Raman-based techniques, including spontaneous Raman spectroscopy and imaging, coherent Raman imaging, and Raman-stable isotope probing, in contribution to the molecular understanding of the complex biological processes in the disease. In addition, this review discusses possible future directions of Raman-based technologies in cancer research.

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29

Schwartz, Egbert. "Characterization of Growing Microorganisms in Soil by Stable Isotope Probing with H218O." Applied and Environmental Microbiology 73, no. 8 (February 23, 2007): 2541–46. http://dx.doi.org/10.1128/aem.02021-06.

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ABSTRACT A new approach to characterize growing microorganisms in environmental samples based on labeling microbial DNA with H2 18O is described. To test if sufficient amounts of 18O could be incorporated into DNA to use water as a labeling substrate for stable isotope probing, Escherichia coli DNA was labeled by cultivating bacteria in Luria broth with H2 18O and labeled DNA was separated from [16O]DNA on a cesium chloride gradient. Soil samples were incubated with H2 18O for 6, 14, or 21 days, and isopycnic centrifugation of the soil DNA showed the formation of two bands after 6 days and three bands after 14 or 21 days, indicating that 18O can be used in the stable isotope probing of soil samples. DNA extracted from soil incubated for 21 days with H2 18O was fractionated after isopycnic centrifugation and DNA from 17 subsamples was used in terminal restriction fragment length polymorphism (TRFLP) analysis of bacterial 16S rRNA genes. The TRFLP patterns clustered into three groups that corresponded to the three DNA bands. The fraction of total fluorescence contributed by individual terminal restriction fragments (TRF) to a TRFLP pattern varied across the 17 subsamples so that a TRF was more prominent in only one of the three bands. Labeling soil DNA with H2 18O allows the identification of newly grown cells. In addition, cells that survive but do not divide during an incubation period can also be characterized with this new technique because their DNA remains without the label.

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Liu, Pengfei, Qiongfen Qiu, and Yahai Lu. "Syntrophomonadaceae-Affiliated Species as Active Butyrate-Utilizing Syntrophs in Paddy Field Soil." Applied and Environmental Microbiology 77, no. 11 (April 1, 2011): 3884–87. http://dx.doi.org/10.1128/aem.00190-11.

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ABSTRACTDNA-based stable-isotope probing was applied to identify the active microorganisms involved in syntrophic butyrate oxidation in paddy field soil. After 14 and 21 days of incubation with [U-13C]butyrate, the bacterialSyntrophomonadaceaeand the archaealMethanosarcinaceaeandMethanocellalesincorporated substantial amounts of13C label into their nucleic acids. Unexpectedly, members of thePlanctomycetesandChloroflexiwere also labeled with13C by yet-unclear mechanisms.

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Akob, Denise M., Lee Kerkhof, Kirsten Küsel, David B. Watson, Anthony V. Palumbo, and Joel E. Kostka. "Linking Specific Heterotrophic Bacterial Populations to Bioreduction of Uranium and Nitrate in Contaminated Subsurface Sediments by Using Stable Isotope Probing." Applied and Environmental Microbiology 77, no. 22 (September 23, 2011): 8197–200. http://dx.doi.org/10.1128/aem.05247-11.

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ABSTRACTShifts in terminal electron-accepting processes during biostimulation of uranium-contaminated sediments were linked to the composition of stimulated microbial populations using DNA-based stable isotope probing. Nitrate reduction preceded U(VI) and Fe(III) reduction in [13C]ethanol-amended microcosms. The predominant, active denitrifying microbial groups were identified as members of theBetaproteobacteria, whereasActinobacteriadominated under metal-reducing conditions.

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32

Meyer, Rikke Louise, Aaron Marc Saunders, and Linda Louise Blackall. "Putative glycogen-accumulating organisms belonging to the Alphaproteobacteria identified through rRNA-based stable isotope probing." Microbiology 152, no. 2 (February 1, 2006): 419–29. http://dx.doi.org/10.1099/mic.0.28445-0.

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Deterioration of enhanced biological phosphorus removal (EBPR) has been linked to the proliferation of glycogen-accumulating organisms (GAOs), but few organisms possessing the GAO metabolic phenotype have been identified. An unidentified GAO was highly enriched in a laboratory-scale bioreactor and attempts to identify this organism using conventional 16S rRNA gene cloning had failed. Therefore, rRNA-based stable isotope probing followed by full-cycle rRNA analysis was used to specifically identify the putative GAOs based on their characteristic metabolic phenotype. The study obtained sequences from a group of Alphaproteobacteria not previously shown to possess the GAO phenotype, but 90 % identical by 16S rRNA gene analysis to a phylogenetic clade containing cloned sequences from putative GAOs and the isolate Defluvicoccus vanus. Fluorescence in situ hybridization (FISH) probes (DF988 and DF1020) were designed to target the new group and post-FISH chemical staining demonstrated anaerobic–aerobic cycling of polyhydroxyalkanoates, as per the GAO phenotype. The successful use of probes DF988 and DF1020 required the use of unlabelled helper probes which increased probe signal intensity up to 6·6-fold, thus highlighting the utility of helper probes in FISH. The new group constituted 33 % of all Bacteria in the lab-scale bioreactor from which they were identified and were also abundant (51 and 55 % of Bacteria) in two other similar bioreactors in which phosphorus removal had deteriorated. Unlike the previously identified Defluvicoccus-related organisms, the group identified in this study were also found in two full-scale treatment plants performing EBPR, suggesting that this group may be industrially relevant.

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Miyatake, Tetsuro, Barbara J. MacGregor, and Henricus T. S. Boschker. "Linking Microbial Community Function to Phylogeny of Sulfate-Reducing Deltaproteobacteria in Marine Sediments by Combining Stable Isotope Probing with Magnetic-Bead Capture Hybridization of 16S rRNA." Applied and Environmental Microbiology 75, no. 15 (June 5, 2009): 4927–35. http://dx.doi.org/10.1128/aem.00652-09.

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ABSTRACT We further developed the stable isotope probing, magnetic-bead capture method to make it applicable for linking microbial community function to phylogeny at the class and family levels. The main improvements were a substantial decrease in the protocol blank and an approximately 10-fold increase in the detection limit by using a micro-elemental analyzer coupled to isotope ratio mass spectrometry to determine 13C labeling of isolated 16S rRNA. We demonstrated the method by studying substrate utilization by Desulfobacteraceae, a dominant group of complete oxidizing sulfate-reducing Deltaproteobacteria in marine sediments. Stable-isotope-labeled [13C]glucose, [13C]propionate, or [13C]acetate was fed into an anoxic intertidal sediment. We applied a nested set of three biotin-labeled oligonucleotide probes to capture Bacteria, Deltaproteobacteria, and finally Desulfobacteraceae rRNA by using hydrophobic streptavidin-coated paramagnetic beads. The target specificities of the probes were examined with pure cultures of target and nontarget species and by determining the phylogenetic composition of the captured sediment rRNA. The specificity of the final protocol was generally very good, as more than 90% of the captured 16S rRNA belonged to the target range of the probes. Our results indicated that Desulfobacteraceae were important consumers of propionate but not of glucose. However, the results for acetate utilization were less conclusive due to lower and more variable labeling levels in captured rRNA. The main advantage of the method in this study over other nucleic acid-based stable isotope probing methods is that 13C labeling can be much lower, to the extent that δ13C ratios can be studied even at their natural abundances.

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Ouyang, Wei-Ying, Jian-Qiang Su, Hans H. Richnow, and Lorenz Adrian. "Identification of dominant sulfamethoxazole-degraders in pig farm-impacted soil by DNA and protein stable isotope probing." Environment International 126 (May 2019): 118–26. http://dx.doi.org/10.1016/j.envint.2019.02.001.

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35

Mooshammer, Maria, Katharina Kitzinger, Arno Schintlmeister, Soeren Ahmerkamp, Jeppe Lund Nielsen, Per Halkjær Nielsen, and Michael Wagner. "Flow-through stable isotope probing (Flow-SIP) minimizes cross-feeding in complex microbial communities." ISME Journal 15, no. 1 (September 2, 2020): 348–53. http://dx.doi.org/10.1038/s41396-020-00761-5.

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AbstractStable isotope probing (SIP) is a key tool for identifying the microorganisms catalyzing the turnover of specific substrates in the environment and to quantify their relative contributions to biogeochemical processes. However, SIP-based studies are subject to the uncertainties posed by cross-feeding, where microorganisms release isotopically labeled products, which are then used by other microorganisms, instead of incorporating the added tracer directly. Here, we introduce a SIP approach that has the potential to strongly reduce cross-feeding in complex microbial communities. In this approach, the microbial cells are exposed on a membrane filter to a continuous flow of medium containing isotopically labeled substrate. Thereby, metabolites and degradation products are constantly removed, preventing consumption of these secondary substrates. A nanoSIMS-based proof-of-concept experiment using nitrifiers in activated sludge and 13C-bicarbonate as an activity tracer showed that Flow-SIP significantly reduces cross-feeding and thus allows distinguishing primary consumers from other members of microbial food webs.

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36

Sun, Weimin, and Alison M. Cupples. "Diversity of Five Anaerobic Toluene-Degrading Microbial Communities Investigated Using Stable Isotope Probing." Applied and Environmental Microbiology 78, no. 4 (December 9, 2011): 972–80. http://dx.doi.org/10.1128/aem.06770-11.

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ABSTRACTTime-series DNA-stable isotope probing (SIP) was used to identify the microbes assimilating carbon from [13C]toluene under nitrate- or sulfate-amended conditions in a range of inoculum sources, including uncontaminated and contaminated soil and wastewater treatment samples. In all, five different phylotypes were found to be responsible for toluene degradation, and these included previously identified toluene degraders as well as novel toluene-degrading microorganisms. In microcosms constructed from granular sludge and amended with nitrate, the putative toluene degraders were classified in the genusThauera, whereas in nitrate-amended microcosms constructed from a different source (agricultural soil), microorganisms in the familyComamonadaceae(genus unclassified) were the key putative degraders. In one set of sulfate-amended microcosms (agricultural soil), the putative toluene degraders were identified as belonging to the classClostridia(genusDesulfosporosinus), while in other sulfate-amended microcosms, the putative degraders were in the classDeltaproteobacteria, within the familySyntrophobacteraceae(digester sludge) orDesulfobulbaceae(contaminated soil) (genus unclassified for both). Partial benzylsuccinate synthase gene (bssA, the functional gene for anaerobic toluene degradation) sequences were obtained for some samples, and quantitative PCR targeting this gene, along with SIP, was further used to confirm anaerobic toluene degradation by the identified species. The study illustrates the diversity of toluene degraders across different environments and highlights the utility of ribosomal and functional gene-based SIP for linking function with identity in microbial communities.

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Weis, Severin, Sylvia Schnell, and Markus Egert. "Towards safer stable isotope probing — effect of formamide on the separation of isotope-labeled and unlabeled Escherichia coli RNA by isopycnic density ultracentrifugation." Canadian Journal of Microbiology 66, no. 8 (August 2020): 491–94. http://dx.doi.org/10.1139/cjm-2019-0612.

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RNA-based stable isotope probing (RNA-SIP) is used in molecular microbial ecology to link the identity of microorganisms in a complex community with the assimilation of a distinct substrate. The technique is highly dependent on a reliable separation of isotopic-labeled RNA from unlabeled RNA by isopycnic density gradient ultracentrifugation. Here we show that 13C-labeled and unlabeled Escherichia coli RNA can be sufficiently separated by isopycnic ultracentrifugation even in the absence of formamide. However, a slightly lower starting density is needed to obtain a distribution pattern similar to that obtained when formamide was used. Hence, the commonly used addition of formamide to the centrifugation solution might not be needed to separate 13C-labeled RNA from unlabeled RNA, but this must be verified for more complex environmental mixtures of RNA. Clearly, an omission of formamide would increase the safety of RNA-SIP analyses.

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Kasai, Yuki, Yoh Takahata, Mike Manefield, and Kazuya Watanabe. "RNA-Based Stable Isotope Probing and Isolation of Anaerobic Benzene-Degrading Bacteria from Gasoline-Contaminated Groundwater." Applied and Environmental Microbiology 72, no. 5 (May 2006): 3586–92. http://dx.doi.org/10.1128/aem.72.5.3586-3592.2006.

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ABSTRACT Stable isotope probing (SIP) of benzene-degrading bacteria in gasoline-contaminated groundwater was coupled to denaturing gradient gel electrophoresis (DGGE) of DNA fragments amplified by reverse transcription-PCR from community 16S rRNA molecules. Supplementation of the groundwater with [13C6]benzene together with an electron acceptor (nitrate, sulfate, or oxygen) showed that a phylotype affiliated with the genus Azoarcus specifically appeared in the 13C-RNA fraction only when nitrate was supplemented. This phylotype was also observed as the major band in DGGE analysis of bacterial 16S rRNA gene fragments amplified by PCR from the gasoline-contaminated groundwater. In order to isolate the Azoarcus strains, the groundwater sample was streaked on agar plates containing nonselective diluted CGY medium, and the DGGE analysis was used to screen colonies formed on the plates. This procedure identified five bacterial isolates (from 60 colonies) that corresponded to the SIP-identified Azoarcus phylotype, among which two strains (designated DN11 and AN9) degraded benzene under denitrifying conditions. Incubation of these strains with [14C]benzene showed that the labeled carbon was mostly incorporated into 14CO2 within 14 days. These results indicate that the Azoarcus population was involved in benzene degradation in the gasoline-contaminated groundwater under denitrifying conditions. We suggest that RNA-based SIP identification coupled to phylogenetic screening of nonselective isolates facilitates the isolation of enrichment/isolation-resistant microorganisms with a specific function.

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Wilhelm, Roland, András Szeitz, Tara L. Klassen, and William W. Mohn. "Sensitive, Efficient Quantitation of13C-Enriched Nucleic Acids via Ultrahigh-Performance Liquid Chromatography–Tandem Mass Spectrometry for Applications in Stable Isotope Probing." Applied and Environmental Microbiology 80, no. 23 (September 12, 2014): 7206–11. http://dx.doi.org/10.1128/aem.02223-14.

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ABSTRACTStable isotope probing (SIP) of nucleic acids is a powerful tool for studying the functional traits of microbial populations within complex communities, but SIP involves a number of technical challenges. Many of the difficulties in DNA-SIP and RNA-SIP experiments can be effectively overcome with an efficient, sensitive method for quantitating the isotopic enrichment of nucleic acids. Here, we present a sensitive method for quantitating13C enrichment of nucleic acids, requiring a few nanograms of sample, and we demonstrate its utility in typical DNA-SIP and RNA-SIP experiments. All five nucleobases (adenine, guanine, cytosine, thymine, and uracil) were separated and detected by using ultrahigh-performance liquid chromatography–tandem mass spectrometry. We detected all isotopic species in samples with as low as 1.5 atom%13C above natural abundance, using 1-ng loadings. Quantitation was used to characterize the isotopic enrichment kinetics of cellulose- and lignin-based microcosm experiments and to optimize the recovery of enriched nucleic acids. Application of our method will minimize the quantity of expensive isotopically labeled substrates required and reduce the risk of failed experiments due to insufficient recovery of labeled nucleic acids for sequencing library preparation.

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Lerch, Thomas Z., Marie-France Dignac, Naoise Nunan, Gérard Bardoux, Enrique Barriuso, and André Mariotti. "Dynamics of soil microbial populations involved in 2,4-D biodegradation revealed by FAME-based Stable Isotope Probing." Soil Biology and Biochemistry 41, no. 1 (January 2009): 77–85. http://dx.doi.org/10.1016/j.soilbio.2008.09.020.

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Kumar B. N., Vinay, Shuxia Guo, Thomas Bocklitz, Petra Rösch, and Jürgen Popp. "Demonstration of Carbon Catabolite Repression in Naphthalene Degrading Soil Bacteria via Raman Spectroscopy Based Stable Isotope Probing." Analytical Chemistry 88, no. 15 (July 18, 2016): 7574–82. http://dx.doi.org/10.1021/acs.analchem.6b01046.

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Song, Mengke, Chunling Luo, Longfei Jiang, Dayi Zhang, Yujie Wang, and Gan Zhang. "Identification of Benzo[a]pyrene-Metabolizing Bacteria in Forest Soils by Using DNA-Based Stable-Isotope Probing." Applied and Environmental Microbiology 81, no. 21 (August 7, 2015): 7368–76. http://dx.doi.org/10.1128/aem.01983-15.

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ABSTRACTDNA-based stable-isotope probing (DNA-SIP) was used in this study to investigate the uncultivated bacteria with benzo[a]pyrene (BaP) metabolism capacities in two Chinese forest soils (Mt. Maoer in Heilongjiang Province and Mt. Baicaowa in Hubei Province). We characterized three different phylotypes with responsibility for BaP degradation, none of which were previously reported as BaP-degrading microorganisms by SIP. In Mt. Maoer soil microcosms, the putative BaP degraders were classified as belonging to the genusTerrimonas(familyChitinophagaceae, orderSphingobacteriales), whereasBurkholderiaspp. were the key BaP degraders in Mt. Baicaowa soils. The addition of metabolic salicylate significantly increased BaP degradation efficiency in Mt. Maoer soils, and the BaP-metabolizing bacteria shifted to the microorganisms in the familyOxalobacteraceae(genus unclassified). Meanwhile, salicylate addition did not change either BaP degradation or putative BaP degraders in Mt. Baicaowa. Polycyclic aromatic hydrocarbon ring-hydroxylating dioxygenase (PAH-RHD) genes were amplified, sequenced, and quantified in the DNA-SIP13C heavy fraction to further confirm the BaP metabolism. By illuminating the microbial diversity and salicylate additive effects on BaP degradation across different soils, the results increased our understanding of BaP natural attenuation and provided a possible approach to enhance the bioremediation of BaP-contaminated soils.

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Herrmann, Elena, Wayne Young, Douglas Rosendale, Verena Reichert-Grimm, Christian U. Riedel, Ralf Conrad, and Markus Egert. "RNA-Based Stable Isotope Probing SuggestsAllobaculumspp. as Particularly Active Glucose Assimilators in a Complex Murine Microbiota Cultured In Vitro." BioMed Research International 2017 (2017): 1–13. http://dx.doi.org/10.1155/2017/1829685.

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RNA-based stable isotope probing (RNA-SIP) and metabolic profiling were used to detect actively glucose-consuming bacteria in a complex microbial community obtained from a murine model system. A faeces-derived microbiota was incubated under anaerobic conditions for 0, 2, and 4 h with 40 mM [U13C]glucose. Isopycnic density gradient ultracentrifugation and fractionation of isolated RNA into labeled and unlabeled fractions followed by 16S rRNA sequencing showed a quick adaptation of the bacterial community in response to the added sugar, which was dominated by unclassified Lachnospiraceae species. Inspection of distinct fractions of isotope-labeled RNA revealedAllobaculumspp. as particularly active glucose utilizers in the system, as the corresponding RNA showed significantly higher proportions among the labeled RNA. With time, the labeled sugar was used by a wider spectrum of faecal bacteria. Metabolic profiling indicated rapid fermentation of [U13C]glucose, with lactate, acetate, and propionate being the principal13C-labeled fermentation products, and suggested that “cross-feeding” occurred in the system. RNA-SIP combined with metabolic profiling of13C-labeled products allowed insights into the microbial assimilation of a general model substrate, demonstrating the appropriateness of this technology to study assimilation processes of nutritionally more relevant substrates, for example, prebiotic carbohydrates, in the gut microbiota of mice as a model system.

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Sul, Woo Jun, Joonhong Park, John F. Quensen, Jorge L. M. Rodrigues, Laurie Seliger, Tamara V. Tsoi, Gerben J. Zylstra, and James M. Tiedje. "DNA-Stable Isotope Probing Integrated with Metagenomics for Retrieval of Biphenyl Dioxygenase Genes from Polychlorinated Biphenyl-Contaminated River Sediment." Applied and Environmental Microbiology 75, no. 17 (July 31, 2009): 5501–6. http://dx.doi.org/10.1128/aem.00121-09.

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ABSTRACT Stable isotope probing with [13C]biphenyl was used to explore the genetic properties of indigenous bacteria able to grow on biphenyl in PCB-contaminated River Raisin sediment. A bacterial 16S rRNA gene clone library generated from [13C]DNA after a 14-day incubation with [13C]biphenyl revealed the dominant organisms to be members of the genera Achromobacter and Pseudomonas. A library built from PCR amplification of genes for aromatic-ring-hydroxylating dioxygenases from the [13C]DNA fraction revealed two sequence groups similar to bphA (encoding biphenyl dioxygenase) of Comamonas testosteroni strain B-356 and of Rhodococcus sp. RHA1. A library of 1,568 cosmid clones was produced from the [13C]DNA fraction. A 31.8-kb cosmid clone, detected by aromatic dioxygenase primers, contained genes of biphenyl dioxygenase subunits bphAE, while the rest of the clone's sequence was similar to that of an unknown member of the Gammaproteobacteria. A discrepancy in G+C content near the bphAE genes implies their recent acquisition, possibly by horizontal transfer. The biphenyl dioxygenase from the cosmid clone oxidized biphenyl and unsubstituted and para-only-substituted rings of polychlorinated biphenyl (PCB) congeners. A DNA-stable isotope probing-based cosmid library enabled the retrieval of functional genes from an uncultivated organism capable of PCB metabolism and suggest dispersed dioxygenase gene organization in nature.

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Lerch, Thomas Z., Marie-France Dignac, Enrique Barriuso, and André Mariotti. "Effect of Glucose on the Fatty Acid Composition of Cupriavidus necator JMP134 during 2,4-Dichlorophenoxyacetic Acid Degradation: Implications for Lipid-Based Stable Isotope Probing Methods." Applied and Environmental Microbiology 77, no. 20 (August 19, 2011): 7296–306. http://dx.doi.org/10.1128/aem.06438-11.

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ABSTRACTCombining lipid biomarker profiling with stable isotope probing (SIP) is a powerful technique for studying specific microbial populations responsible for the degradation of organic pollutants in various natural environments. However, the presence of other easily degradable substrates may induce significant physiological changes by altering both the rate of incorporation of the target compound into the biomass and the microbial lipid profiles. In order to test this hypothesis,Cupriavidus necatorJMP134, a 2,4-dichlorophenoxyacetic acid (2,4-D)-degrading bacterium, was incubated with [13C]2,4-D, [13C]glucose, or mixtures of both substrates alternatively labeled with13C.C. necatorJMP134 exhibited a preferential use of 2,4-D over glucose. The isotopic analysis showed that glucose had only a small effect on the incorporation of the acetic chain of 2,4-D into the biomass (at days 2 and 3) and no effect on that of the benzenic ring. The addition of glucose did change the fatty acid methyl ester (FAME) composition. However, the overall FAME isotopic signature reflected that of the entire biomass. Compound-specific individual isotopic analyses of FAME composition showed that the13C-enriched FAME profiles were slightly or not affected when tracing the 2,4-D acetic chain or 2,4-D benzenic ring, respectively. This batch study is a necessary step for validating the use of lipid-based SIP methods in complex environments.

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Charteris, A. F., T. D. J. Knowles, K. Michaelides, and R. P. Evershed. "Compound-specific <sup>15</sup>N stable isotope probing of N assimilation by the soil microbial biomass: a new methodological paradigm in soil N cycling." SOIL Discussions 2, no. 2 (October 30, 2015): 1135–60. http://dx.doi.org/10.5194/soild-2-1135-2015.

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Abstract. A compound-specific nitrogen-15 stable isotope probing (15N-SIP) technique is described which allows investigation of the fate of inorganic- or organic-N amendments to soils. The technique uses gas chromatography-combustion-isotope ratio mass spectrometry (GC-C-IRMS) to determine the δ15N values of individual amino acids (AAs; determined as N-acetyl, O-isopropyl derivatives) as proxies of biomass protein production. The δ15N values are used together with AA concentrations to quantify N assimilation of 15N-labelled substrates by the soil microbial biomass. The utility of the approach is demonstrated through incubation experiments using inorganic 15N-labelled substrates ammonium (15NH4+) and nitrate (15NO3-) and an organic 15N-labelled substrate, glutamic acid (15N-Glu). Assimilation of all the applied substrates was undetectable based on bulk soil properties, i.e. % total N (% TN), bulk soil N isotope composition and AA concentrations, all of which remained relatively constant throughout the incubation experiments. In contrast, compound-specific AA δ15N values were highly sensitive to N assimilation, providing qualitative and quantitative insights into the cycling and fate of the applied 15N-labelled substrates. The utility of this 15N-AA-SIP technique is considered in relation to other currently available methods for investigating the microbially-mediated assimilation of nitrogenous substrates into the soil organic N pool. This approach will be generally applicable to the study of N cycling in any soil, or indeed, in any complex ecosystem.

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Sun, Weimin, Xiaoxu Sun, and Alison M. Cupples. "Anaerobic Methyltert-Butyl Ether-Degrading Microorganisms Identified in Wastewater Treatment Plant Samples by Stable Isotope Probing." Applied and Environmental Microbiology 78, no. 8 (February 10, 2012): 2973–80. http://dx.doi.org/10.1128/aem.07253-11.

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ABSTRACTAnaerobic methyltert-butyl ether (MTBE) degradation potential was investigated in samples from a range of sources. From these 22 experimental variations, only one source (from wastewater treatment plant samples) exhibited MTBE degradation. These microcosms were methanogenic and were subjected to DNA-based stable isotope probing (SIP) targeted to both bacteria and archaea to identify the putative MTBE degraders. For this purpose, DNA was extracted at two time points, subjected to ultracentrifugation, fractioning, and terminal restriction fragment length polymorphism (TRFLP). In addition, bacterial and archaeal 16S rRNA gene clone libraries were constructed. The SIP experiments indicated bacteria in the phylaFirmicutes(familyRuminococcaceae) andAlphaproteobacteria(genusSphingopyxis) were the dominant MTBE degraders. Previous studies have suggested a role forFirmicutesin anaerobic MTBE degradation; however, the putative MTBE-degrading microorganism in the current study is a novel MTBE-degrading phylotype within this phylum. Two archaeal phylotypes (generaMethanosarcinaandMethanocorpusculum) were also enriched in the heavy fractions, and these organisms may be responsible for minor amounts of MTBE degradation or for the uptake of metabolites released from the primary MTBE degraders. Currently, limited information exists on the microorganisms able to degrade MTBE under anaerobic conditions. This work represents the first application of DNA-based SIP to identify anaerobic MTBE-degrading microorganisms in laboratory microcosms and therefore provides a valuable set of data to definitively link identity with anaerobic MTBE degradation.

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CHU Min, 楚敏, 王芸 WANG Yun, 曾军 ZENG Jun, 张志东 ZHANG Zhidong, and 娄恺 LOU Kai. "The glucose-utilizing bacterial diversity in the cold spring sediment of Shawan, Xinjiang, based on stable isotope probing." Acta Ecologica Sinica 32, no. 14 (2012): 4413–20. http://dx.doi.org/10.5846/stxb201107051003.

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Young, Wayne, Markus Egert, Shalome Bassett, and Rodrigo Bibiloni. "Detection of Sialic Acid-Utilising Bacteria in a Caecal Community Batch Culture Using RNA-Based Stable Isotope Probing." Nutrients 7, no. 4 (March 25, 2015): 2109–24. http://dx.doi.org/10.3390/nu7042109.

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Manefield, Mike, Andrew S. Whiteley, Nick Ostle, Philip Ineson, and Mark J. Bailey. "Technical considerations for RNA-based stable isotope probing: an approach to associating microbial diversity with microbial community function." Rapid Communications in Mass Spectrometry 16, no. 23 (2002): 2179–83. http://dx.doi.org/10.1002/rcm.782.

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