In-situ 13CO2 labeling to trace carbon fluxes in plant-soil-microorganism systems: Review and methodological guideline

Achouak, 2019, Stable isotope probing of microbiota structure and function in the plant rhizosphere, Stable Isotope Probing, 233, 10.1007/978-1-4939-9721-3_18 Albers, 2006, Incorporation of plant carbon into the soil animal food web of an arable system, Ecology, 87, 235, 10.1890/04-1728 Amelung, 2001, Fate of microbial residues during litter decomposition as affected by minerals, Soil Sci., 166, 598, 10.1097/00010694-200109000-00003 Amelung, 2008, Combining biomarker with stable isotope analyses for assessing the transformation and turnover of soil organic matter, Adv. Agron., 155, 10.1016/S0065-2113(08)00606-8 Anderson, 2003, Microbial eco-physiological indicators to asses soil quality, Agric. Ecosyst. Environ., 98, 285, 10.1016/S0167-8809(03)00088-4 Anderson, 2010, Soil microbial biomass: the eco-physiological approach, Soil Biol. Biochem., 42, 2039, 10.1016/j.soilbio.2010.06.026 Apostel, 2015, Biochemistry of hexose and pentose transformations in soil analyzed by position-specific labeling and 13C-PLFA, Soil Biol. Biochem., 80, 199, 10.1016/j.soilbio.2014.09.005 Appuhn, 2004, The automated determination of glucosamine, galactosamine, muramic acid, and mannosamine in soil and root hydrolysates by HPLC, J. Plant Nutr. Soil Sci., 167, 17, 10.1002/jpln.200321302 Bååth, 2003, Comparison of soil fungal/bacterial ratios in a pH gradient using physiological and PLFA-based techniques, Soil Biol. Biochem., 35, 955, 10.1016/S0038-0717(03)00154-8 Balasooriya, 2014, Translocation and turnover of rhizodeposit carbon within soil microbial communities of an extensive grassland ecosystem, Plant Soil, 376, 61, 10.1007/s11104-012-1343-z Bardgett, 1996, Changes in soil fungal: bacterial biomass ratios following reductions in the intensity of management of an upland grassland, Biol. Fertil. Soils, 22, 261, 10.1007/BF00382522 Batjes, 1996, Total carbon and nitrogen in the soils of the world, Eur. J. Soil Sci., 47, 151, 10.1111/j.1365-2389.1996.tb01386.x Biasi, 2012, An isotope approach based on 13C pulse-chase labelling vs. the root trenching method to separate heterotrophic and autotrophic respiration in cultivated Peatlands, Boreal Environ. Res., 17, 184 Black, 1965 Blagodatskaya, 2013, Active microorganisms in soil: critical review of estimation criteria and approaches, Soil Biol. Biochem., 67, 192, 10.1016/j.soilbio.2013.08.024 Blagodatskaya, 2011, Three-source-partitioning of microbial biomass and of CO2 efflux from soil to evaluate mechanisms of priming effects, Soil Biol. Biochem., 43, 778, 10.1016/j.soilbio.2010.12.011 Boschker, 2002, Stable isotopes and biomarkers in microbial ecology, FEMS (Fed. Eur. Microbiol. Soc.) Microbiol. Ecol., 40, 85, 10.1111/j.1574-6941.2002.tb00940.x Buchholz, 2009 Bunn, 1989, Stable isotope analysis of carbon flow in a tundra river system, Can. J. Fish. Aquat. Sci., 46, 1769, 10.1139/f89-224 Butler, 2004, Distribution and turnover of recently fixed photosynthate in ryegrass rhizospheres, Soil Biol. Biochem., 36, 371, 10.1016/j.soilbio.2003.10.011 Chaudhary, 2016, Identification of metabolically active rhizosphere microorganisms by stable isotopic probing of PLFA in switchgrass, Commun. Soil Sci. Plant Anal., 47, 2433, 10.1080/00103624.2016.1243704 Chaudhary, 2014, Fate of carbon in water-stable aggregates during decomposition of 13C-labeled corn straw, Commun. Soil Sci. Plant Anal., 45, 1906, 10.1080/00103624.2014.909834 Chen, 2010, When metagenomics meets stable-isotope probing: progress and perspectives, Trends Microbiol., 18, 157, 10.1016/j.tim.2010.02.002 Chen, 2019, Microbial C : N : P stoichiometry and turnover depend on nutrients availability in soil: a 14C, 15N and 33P triple labelling study, Soil Biol. Biochem., 206, 10.1016/j.soilbio.2019.01.017 Cheng, 1994, Investigating short-term carbon flows in the rhizospheres of different plant species, using isotopic trapping, Agron. J., 86, 782, 10.2134/agronj1994.00021962008600050007x Cheshire, 1990, Labelled and native sugars in particle-size fractions from soils incubated with 14C straw for 6 to 18 years, J. Soil Sci., 41, 29, 10.1111/j.1365-2389.1990.tb00042.x Decock, 2009, Critical assessment of the applicability of gas chromatography-combustion-isotope ratio mass spectrometry to determine amino sugar dynamics in soil, Rapid Commun. Mass Spectrom., 23, 1201, 10.1002/rcm.3990 Derrien, 2017, Lipid biomarkers and spectroscopic indices for identifying organic matter sources in aquatic environments: a review, Water Res., 112, 58, 10.1016/j.watres.2017.01.023 De Schepper, 2013, 11C-PET imaging reveals transport dynamics and sectorial plasticity of oak phloem after girdling, Front. Plant Sci., 4, 200, 10.3389/fpls.2013.00200 Dippold, 2014, Improved δ13C analysis of amino sugars in soil by ion chromatography–oxidation–isotope ratio mass spectrometry, Rapid Commun. Mass Spectrom., 28, 569, 10.1002/rcm.6814 Dirks, 2012, Carbon partitioning in soybean (Glycine max) leaves by combined 11C and 13C labeling, New Phytol., 196, 1109, 10.1111/j.1469-8137.2012.04333.x Domanski, 2001, Carbon flows in the rhizosphere of ryegrass (Lolium perenne), J. Plant Nutr. Soil Sci., 164, 381, 10.1002/1522-2624(200108)164:4<381::AID-JPLN381>3.0.CO;2-5 Dumont, 2011, DNA-, rRNA- and mRNA-based stable isotope probing of aerobic methanotrophs in lake sediment, Environ. Microbiol., 13, 1153, 10.1111/j.1462-2920.2010.02415.x Eder, 2010, Analysis of hydrolysable neutral sugars in mineral soils: improvement of alditol acetylation for gas chromatographic separation and measurement, Org. Geochem., 41, 580, 10.1016/j.orggeochem.2010.02.009 Engelking, 2007, Shifts in amino sugar and ergosterol contents after addition of sucrose and cellulose to soil, Soil Biol. Biochem., 39, 2111, 10.1016/j.soilbio.2007.03.020 Fairbanks, 2005, Radiocarbon calibration curve spanning 0 to 50,000 years BP based on paired 230Th/234U/238U and 14C dates on pristine corals, Quat. Sci. Rev., 24, 1781, 10.1016/j.quascirev.2005.04.007 Fan, 2014, Probing potential microbial coupling of carbon and nitrogen cycling during decomposition of maize residue by 13C-DNA-SIP, Soil Biol. Biochem., 70, 12, 10.1016/j.soilbio.2013.12.002 Feng, 2018, Effect of climate warming and nitrogen deposition on net photosynthetic rate of alpine plants on Qinghai-Tibet Plateau, Pratacult. Sci., 35, 781 Frostegård, 1991, Microbial biomass measured as total lipid phosphate in soils of different organic content, J. Microbiol. Methods, 14, 151, 10.1016/0167-7012(91)90018-L Frostegård, 1993, Shifts in the structure of soil microbial communities in limed forests as revealed by phospholipid fatty acid analysis, Soil Biol. Biochem., 25, 723, 10.1016/0038-0717(93)90113-P Gavrichkova, 2010, Respiration costs associated with nitrate reduction as estimated by 14CO2 pulse labeling of corn at various growth stages, Plant Soil, 329, 433, 10.1007/s11104-009-0169-9 Ge, 2015, Tracking the photosynthesized carbon input into soil organic carbon pools in a rice soil fertilized with nitrogen, Plant Soil, 392, 17, 10.1007/s11104-014-2265-8 Ge, 2012, Biological carbon assimilation and dynamics in a flooded rice–soil system, Soil Biol. Biochem., 48, 39, 10.1016/j.soilbio.2012.01.009 Glaser, 2004, Amino sugars and muramic acid - biomarkers for soil microbial community structure analysis, Soil Biol. Biochem., 36, 399, 10.1016/j.soilbio.2003.10.013 Glaser, 2005, Compound-specific stable-isotope (δ13C) analysis in soil science, J. Plant Nutr. Soil Sci., 168, 633, 10.1002/jpln.200521794 Glaser, 2005, Compound‐specific δ13C analysis of individual amino sugars - a tool to quantify timing and amount of soil microbial residue stabilization, Rapid Commun. Mass Spectrom., 19, 1409, 10.1002/rcm.1913 Guo, 2020, Compound-specific carbon and nitrogen isotope analysis of amino sugars and their applications, Chin. J. Appl. Ecol., 31, 1753 Griffiths, 2004, 13CO2 pulse labelling of plants in tandem with stable isotope probing: methodological considerations for examining microbial function in the rhizosphere, J. Microbiol. Methods, 58, 119, 10.1016/j.mimet.2004.03.011 Guckert, 1985, Phospholipid, ester-linked fatty acid profiles as reproducible assays for changes in prokaryotic community structure of estuarine sediments, FEMS (Fed. Eur. Microbiol. Soc.) Microbiol. Ecol., 1, 147, 10.1111/j.1574-6968.1985.tb01143.x Gunina, 2014, Pathways of litter C by formation of aggregates and SOM density fractions: implications from 13C natural abundance, Soil Biol. Biochem., 71, 95, 10.1016/j.soilbio.2014.01.011 Gunina, 2017, Turnover of microbial groups and cell components in soil: C analysis of cellular biomarkers, Biogeosciences, 14, 271, 10.5194/bg-14-271-2017 Gunina, 2015, Sugars in soil and sweets for microorganisms: review of origin, content, composition and fate, Soil Biol. Biochem., 90, 87, 10.1016/j.soilbio.2015.07.021 Gülay, 2019, DNA- and RNA-SIP reveal nitrospira spp. as key drivers of nitrification in groundwater-fed biofilters, Appl. Environ. Sci., 10 Hafner, 2012, Effect of grazing on carbon stocks and assimilate partitioning in a Tibetan montane pasture revealed by 13CO2 pulse labeling, Global Change Biol., 18, 528, 10.1111/j.1365-2486.2011.02557.x Haines, 1979, Food sources of estuarine invertebrates analyzed using 13C/12C ratios, Ecology, 60, 48, 10.2307/1936467 Hanson, 2000, Separating root and soil microbial contributions to soil respiration: a review of methods and observations, Biogeochemistry, 48, 115, 10.1023/A:1006244819642 Hatté, 2009, Climate reconstruction from pollen and δ 13C records using inverse vegetation modeling–Implication for past and future climates, Clim. Past, 5, 147, 10.5194/cp-5-147-2009 Harris, 2001, Acid fumigation of soils to remove carbonates prior to total organic carbon or carbon-13 isotopic analysis, Soil Sci. Soc. Am. J., 65, 1853, 10.2136/sssaj2001.1853 Hood-Nowotny, 2007, Stable isotope methods in biological and ecological studies of arthropods, Entomol. Exp. Appl., 124, 3, 10.1111/j.1570-7458.2007.00572.x Hütsch, 2002, Plant rhizodeposition-an important source for carbon turnover in soils, J. Plant Nutr. Soil Sci., 165, 397, 10.1002/1522-2624(200208)165:4<397::AID-JPLN397>3.0.CO;2-C Ida, 2014, Heating effect by perianth retention on developing achenes and implications for seed production in the alpine herb Ranunculus glacialis, Alpine Bot., 124, 37, 10.1007/s00035-014-0129-8 Irmler, 2000, Changes in the fauna and its contribution to mass loss and N release during leaf litter decomposition in two deciduous forests, Pedobiologia, 44, 105, 10.1078/S0031-4056(04)70032-3 Janzen, 2015, Beyond carbon sequestration: soil as conduit of solar energy, Eur. J. Soil Sci., 66, 19, 10.1111/ejss.12194 Joergensen, 2018, Amino sugars as specific indices for fungal and bacterial residues in soil, Biol. Fertil. Soils, 54, 559, 10.1007/s00374-018-1288-3 Kagawa, 2006, 13CO2 pulse-labelling of photoassimilates reveals carbon allocation within and between tree rings, Plant Cell Environ., 29, 1571, 10.1111/j.1365-3040.2006.01533.x Kelly, 2012, Fatty acids as dietary tracers in benthic food webs, Mar. Ecol. Prog. Ser., 446, 1, 10.3354/meps09559 Kawachi, 2011, Real-time whole-plant imaging of 11C translocation using positron-emitting tracer imaging system, nuclear Inst. Method. Phy. Res.: Accelarators Spectrom. Detector Associated Equip., 648, S317, 10.1016/j.nima.2010.10.152 Keutgen, 1995, Use of transfer function and compartmental analysis to quantify 11C-labelled photoassimilate export from wheat leaves, J. Exp. Bot., 46, 489, 10.1093/jxb/46.5.489 Khan, 2002, Quantifying below-ground nitrogen of legumes. 2. a comparison of 15n and non isotopic methods, Plant Soil, 239, 277, 10.1023/A:1015066323050 Kouchi, 1984, Dynamics of carbon photosynthetically assimilated in nodulated soya bean plants under steady-state conditions 2. The incorporation of 13C into carbohydrates, organic acids, amino acids and some storage compounds, Ann. Bot., 53, 883, 10.1093/oxfordjournals.aob.a086758 Kucera, 1971, Soil respiration studies in tallgrass prairie in Missouri, Ecology, 52, 912, 10.2307/1936043 Kuzyakov, 2000, Carbon input by plants into the soil. review, J. Plant Nutr. Soil Sci., 163, 421, 10.1002/1522-2624(200008)163:4<421::AID-JPLN421>3.0.CO;2-R Kuzyakov, 2000, Review of mechanisms and quantification of priming effects, Soil Biol. Biochem., 32, 1485, 10.1016/S0038-0717(00)00084-5 Kuzyakov, 2006, Sources of CO2 efflux from soil and review of partitioning methods, Soil Biol. Biochem., 38, 425, 10.1016/j.soilbio.2005.08.020 Kuzyakov, 2002, Carbon partitioning in plant and soil, carbon dioxide fluxes and enzyme activities as affected by cutting ryegrass, Biol. Fertil. Soils, 35, 348, 10.1007/s00374-002-0480-6 Kuzyakov, 2004, Photosynthesis controls of CO2 efflux from maize rhizosphere, Plant Soil, 263, 85, 10.1023/B:PLSO.0000047728.61591.fd Kuzyakov, 2010, Priming effects: interactions between living and dead organic matter, Soil Biol. Biochem., 42, 1363, 10.1016/j.soilbio.2010.04.003 Le Tacon, 2013, Carbon transfer from the host to Tuber melanosporum mycorrhizas and ascocarps followed using a 13C pulse-labeling technique, PLoS One, 8, 10.1371/journal.pone.0064626 Lederer, 1967, Table of isotopes, Phys. Today, 20, 97, 10.1063/1.3034044 Lehmann, 2015, The contentious nature of soil organic matter, Nature, 528, 60, 10.1038/nature16069 Lekberg, 2012, Seasonal carbon allocation to arbuscular mycorrhizal fungi assessed by microscopic examination, stable isotope probing and fatty acid analysis, Plant Soil, 368, 547 Le Quéré, 2016, Global carbon budget 2016, Earth Syst. Sci. Data, 8, 605, 10.5194/essd-8-605-2016 Lesuffleur, 2013, Use of a 15N2 labelling technique to estimate exudation by white clover and transfer to companion ryegrass of symbiotically fixed N, Plant Soil, 369, 187, 10.1007/s11104-012-1562-3 Lin, 2012, Application of stable isotope probing on in-situ identification of soil functional microorganism, J. Agro. Environ. Sci., 109 Lu, 2002, Contribution of plant-derived carbon to soil microbial biomass dynamics in a paddy rice microcosm, Biol. Fertil. Soils, 36, 136, 10.1007/s00374-002-0504-2 Lu, 2005, Detecting active methanogenic populations on rice roots using stable isotope probing, Environ. Microbiol., 7, 326, 10.1111/j.1462-2920.2005.00697.x Lu, 2007, Spatial variation of active microbiota in the rice rhizosphere revealed by in situ stable isotope probing of phospholipid fatty acids, Environ. Microbiol., 9, 474, 10.1111/j.1462-2920.2006.01164.x Lueders, 2003, Enhanced sensitivity of DNA- and rRNA-based stable isotope probing by fractionation and quantitative analysis of isopycnic centrifugation gradients, Environ. Microbiol., 6, 73, 10.1046/j.1462-2920.2003.00536.x Lueders, 2016, RNA-stable isotope probing: from carbon flow within key microbiota to targeted transcriptomes, Curr. Opin. Biotechnol., 41, 83, 10.1016/j.copbio.2016.05.001 MacFadyen, 1962, Soil arthropod sampling, Adv. Ecol. Res., 1–34, 10.1016/S0065-2504(08)60299-8 Manefield, 2007, Insights into the fate of a 13C labelled phenol pulse for stable isotope probing (SIP) experiments, J. Microbiol. Methods, 69, 340, 10.1016/j.mimet.2007.01.019 Manefield, 2002, RNA stable isotope probing, a novel means of linking microbial community function to phylogeny, Appl. Environ. Microbiol., 68, 5367, 10.1128/AEM.68.11.5367-5373.2002 Makarov, 2015, Effect of K2SO4 concentration on extractability and isotope signature (δ13C and δ15N) of soil C and N fractions, Eur. J. Soil Sci., 66, 417, 10.1111/ejss.12243 Merbach, 1999, Release of carbon and nitrogen compounds by plant roots and their possible ecological importance+, J. Plant Nutr. Soil Sci., 162, 373, 10.1002/(SICI)1522-2624(199908)162:4<373::AID-JPLN373>3.0.CO;2-# Minchin, 2003, Using the short-lived isotope 11C in mechanistic studies of photosynthate transport, Funct. Plant Biol., 30, 831, 10.1071/FP03008 Morrison, 2010, Strong anion-exchange liquid chromatography coupled with isotope ratio mass spectrometry using a Liquiface interface, Rapid Commun. Mass Spectrom., 24, 1755, 10.1002/rcm.4572 Morrissey, 2017, Bacterial carbon use plasticity, phylogenetic diversity and the priming of soil organic matter, ISME J., 11, 1890, 10.1038/ismej.2017.43 Neufeld, 2006, Methodological considerations for the use of stable isotope probing in microbial ecology, Microb. Ecol., 53, 435, 10.1007/s00248-006-9125-x Neufeld, 2007, DNA stable-isotope probing, Nat. Protoc., 2, 860, 10.1038/nprot.2007.109 Nimmo, 2002, [SSSA book series] methods of soil analysis: Part 4 Oades, 1962 Oades, 1984, Soil organic matter and structural stability: mechanisms and implications for management, Plant Soil, 76, 319, 10.1007/BF02205590 Ondrasek, 2019, Biogeochemistry of soil organic matter in agroecosystems & environmental implications, Sci. Total Environ., 658, 1559, 10.1016/j.scitotenv.2018.12.243 Ostle, 2003, Active microbial RNA turnover in a grassland soil estimated using a 13CO2 spike, Soil Biol. Biochem., 35, 877, 10.1016/S0038-0717(03)00117-2 Pang, 2018, Effects of clipping and shading on 15NO3− and 15NH4+ recovery by plants in grazed and ungrazed temperate grasslands, Plant Soil, 433, 339, 10.1007/s11104-018-3844-x Pang, 2019, Differential response to warming of the uptake of nitrogen by plant species in non-degraded and degraded alpine grasslands, J. Soils Sediments, 19, 2212, 10.1007/s11368-019-02255-0 Parsons, 1981, Chemistry and distribution of amino sugars in soils and soil organisms, ume 5, 197 Pausch, 2017, Carbon input by roots into the soil: quantification of rhizodeposition from root to ecosystem scale, Global Change Biol., 24, 1, 10.1111/gcb.13850 Pausch, 2013, Estimation of rhizodeposition at field scale: upscaling of a 14C labeling study, Plant Soil, 364, 273, 10.1007/s11104-012-1363-8 Peixoto, 2020, Decreased rhizodeposition, but increased microbial carbon stabilization with soil depth down to 3.6 m, Soil Biol. Biochem., 150, 10.1016/j.soilbio.2020.108008 Petersen, 2002, Dynamics of a soil microbial community under spring wheat, Soil Sci. Soc. Am. J., 66, 826, 10.2136/sssaj2002.8260 Pollierer, 2012, Carbon flux through fungi and bacteria into the forest soil animal food web as indicated by compound-specific 13C fatty acid analysis, Funct. Ecol., 26, 978, 10.1111/j.1365-2435.2012.02005.x Potthoff, 2003, The determination of δ13C in soil microbial biomass using fumigation-extraction, Soil Biol. Biochem., 35, 947, 10.1016/S0038-0717(03)00151-2 Radajewski, 2000, Stable-isotope probing as a tool in microbial ecology, Nature, 403, 646, 10.1038/35001054 Ramnarine, 2011, Carbonate removal by acid fumigation for measuring the δ13C of soil organic carbon, Can. J. Soil Sci., 91, 247, 10.4141/cjss10066 Rasmussen, 2007, In situ carbon and nitrogen dynamics in ryegrass–clover mixtures: transfers, deposition and leaching, Soil Biol. Biochem., 39, 804, 10.1016/j.soilbio.2006.10.004 Rasmussen, 2019, Temporal fate of 15N and 14C leaf-fed to red and white clover in pure stand or mixture with grass – implications for estimation of legume derived N in soil and companion species, Soil Biol. Biochem., 133, 60, 10.1016/j.soilbio.2019.02.011 Robinson, 1969, 33P: a superior radiotracer for phosphorus?, Int. J. Appl. Radiat. Isot., 20, 531, 10.1016/0020-708X(69)90007-6 Sangster, 2010, Repeat-pulse 13CO2 labeling of canola and field pea: implications for soil organic matter studies, Rapid Commun. Mass Spectrom., 24, 2791, 10.1002/rcm.4699 Scheu, 1994, Changes in bacterial and fungal biomass C, bacterial and fungal biovolume and ergosterol content after drying, remoistening and incubation of different layers of cool temperate forest soils, Soil Biol. Biochem., 26, 1515, 10.1016/0038-0717(94)90093-0 Schmidt, 2011, Persistence of soil organic matter as an ecosystem property, Nature, 478, 49, 10.1038/nature10386 Shahbaz, 2018, Priming effects induced by glucose and decaying plant residues on SOM decomposition: a three-source 13C/14C partitioning study, Soil Biol. Biochem., 121, 138, 10.1016/j.soilbio.2018.03.004 Simard, 1997, Carbon allocation and carbon transfer between Betula papyrifera and Pseudotsuga menziesii seedlings using a 13C pulse-labeling method, Plant Soil, 191, 41, 10.1023/A:1004205727882 Sommer, 2016, Allocation and dynamics of C and N within plant-soil system of ash and beech, J. Plant Nutr. Soil Sci., 179, 376, 10.1002/jpln.201500384 Sommer, 2017, The tree species matters: belowground carbon input and utilization in the myco-rhizosphere, Eur. J. Soil Biol., 81, 100, 10.1016/j.ejsobi.2017.07.001 Spalding, 2005, Retrospective birth dating of cells in humans, Cell, 122, 133, 10.1016/j.cell.2005.04.028 Stenström, 2010, Local variations in 14C–How is bomb-pulse dating of human tissues and cells affected?, Nucl. Instrum. Methods Phys. Res. Sect. B Beam Interact. Mater. Atoms, 268, 1299, 10.1016/j.nimb.2009.10.157 Stevenel, 2019, Using a tri-isotope (13C, 15N, 33P) labelling method to quantify rhizodeposition, Rhizosphere Biol., 169, 10.1007/978-981-13-5767-1_10 Stockmann, 2013, The knowns, known unknowns and unknowns of sequestration of soil organic carbon. Agriculture, Ecosyst. Environ., 164, 80, 10.1016/j.agee.2012.10.001 Studer, 2014, Carbon transfer, partitioning and residence time in the plant-soil system: a comparison of two 1³CO₂ labelling techniques, Biogeosciences, 11, 1637, 10.5194/bg-11-1637-2014 Sun, 2014, Mechanism of rhizosphere priming effects and their ecological significance, Chinese J. Plant Ecol., 38, 62, 10.3724/SP.J.1258.2014.00007 Thorpe, 2010, Rapid cooling triggers forisome dispersion just before phloem transport stops, Plant Cell Environ., 33, 259, 10.1111/j.1365-3040.2009.02079.x Uhlik, 2013, Stable isotope probing in the metagenomics era: a bridge towards improved bioremediation, Biotechnol. Adv., 31, 154, 10.1016/j.biotechadv.2012.09.003 Vogt, 2016, Stable isotope probing approaches to study anaerobic hydrocarbon degradation and degraders, J. Mol. Microbiol. Biotechnol., 26, 195, 10.1159/000440806 Volkman, 2008, Organic matter sources in an enclosed coastal inlet assessed using lipid biomarkers and stable isotopes, Org. Geochem., 39, 689, 10.1016/j.orggeochem.2008.02.014 Vollmer, 2008, Peptidoglycan structure and architecture, FEMS Microbiol. Rev., 149, 10.1111/j.1574-6976.2007.00094.x Wang, 2008, Paleovegetation reconstruction using δ13C of soil organic matter, Biogeosciences, 5, 1325, 10.5194/bg-5-1325-2008 Wang, 2016, Vertical distribution and indications of lipids biomarkers in the sediment core from east China sea, Continent. Shelf Res., 122, 43, 10.1016/j.csr.2016.03.027 Wang, 2007, Dynamics and allocation of recently photo-assimilated carbon in an Inner Mongolia temperate steppe, Environ. Exp. Bot., 59, 1, 10.1016/j.envexpbot.2005.09.011 Warembourg, 1982, The simultaneous use of 14CO2 and 15N2 labelling techniques to study the carbon and nitrogen economy of legumes grown under natural conditions, Physiol. Plantarum, 56, 46, 10.1111/j.1399-3054.1982.tb04898.x Warembourg, 1991, vols. 11–37 Werth, 2006, Assimilate partitioning affects 13C fractionation of recently assimilated carbon in maize, Plant Soil, 284, 319, 10.1007/s11104-006-0054-8 Werth, 2008, Root-derived carbon in soil respiration and microbial biomass determined by 14C and 13C, Soil Biol. Biochem., 40, 625, 10.1016/j.soilbio.2007.09.022 Wichern, 2007, Rhizodeposition of C and N in peas and oats after 13C–15N double labelling under field conditions, Soil Biol. Biochem., 39, 2527, 10.1016/j.soilbio.2007.04.022 Wichern, 2011, Stem labeling results in different patterns of 14C rhizorespiration and 15N distribution in plants compared to natural assimilation pathways, J. Plant Nutr. Soil Sci., 174, 732, 10.1002/jpln.201000206 Wiesenberg, 2010, Fast incorporation of root-derived lipids and fatty acids into soil-Evidence from a short term multiple 14CO2 pulse labelling experiment, Org. Geochem., 41, 1049, 10.1016/j.orggeochem.2009.12.007 Whiteley, 2007, RNA stable-isotope probing, Nat. Protoc., 2, 838, 10.1038/nprot.2007.115 Wilhelm, 2014, Sensitive, efficient quantitation of 13C-enriched nucleic acids via ultrahigh-performance liquid chromatography–tandem mass spectrometry for applications in stable isotope probing, Appl. Environ. Microbiol., 80, 7206, 10.1128/AEM.02223-14 Williams, 2006, Carbon flow from 13C-labeled straw and root residues into the phospholipid fatty acids of a soil microbial community under field conditions, Soil Biol. Biochem., 38, 759, 10.1016/j.soilbio.2005.07.001 Wolters, 2001, Biodiversity of soil animals and its function, Eur. J. Soil Biol., 37, 221, 10.1016/S1164-5563(01)01088-3 Wu, 2010, Partitioning pattern of carbon flux in a Kobresia grassland on the Qinghai-Tibetan Plateau revealed by field 13C pulse-labeling, Global Change Biol., 16, 2322, 10.1111/j.1365-2486.2009.02069.x Yao, 2014, 13C PLFAs: a key to open the soil microbial black box?, Plant Soil, 392, 3 Yin, 2020, Visualising spatio-temporal distributions of assimilated carbon translocation and release in root systems of leguminous plants, Sci. Rep., 10, 10.1038/s41598-020-65668-9 Zamanian, 2016, Pedogenic carbonates: forms and formation processes, Earth Sci. Rev., 157, 1, 10.1016/j.earscirev.2016.03.003 Zhang, 1996, Gas chromatographic determination of muramic acid, glucosamine, mannosamine, and galactosamine in soils, Soil Biol. Biochem., 28, 1201, 10.1016/0038-0717(96)00117-4 Zhang, 2019, Three Tibetan grassland plant species tend to partition niches with limited plasticity in nitrogen use, Plant Soil, 441, 601, 10.1007/s11104-019-04148-0 Zhang, 2016, Fate of organic and inorganic nitrogen in crusted and non-crusted Kobresia grasslands, Land Degrad. Dev., 28, 166, 10.1002/ldr.2582 Zhao, 2021 Zou, 2014, Field 13CO2 pulse labeling reveals differential partitioning patterns of photoassimilated carbon in response to livestock exclosure in a Kobresia meadow, Biogeosciences, 11, 4381, 10.5194/bg-11-4381-2014