Skip to main content
SpringerLink
Log in

Microbial Catabolic Activity: Methods, Pertinence, and Potential Interest for Improving Microbial Inoculant Efficiency

  • Review
  • Published:
Microbial Ecology Aims and scope Submit manuscript

Abstract

Microbial catabolic activity (MCA) defined as the degrading activity of microorganisms toward various organic compounds for their growth and energy is commonly used to assess soil microbial function potential. For its measure, several methods are available including multi-substrate-induced respiration (MSIR) measurement which allow to estimate functional diversity using selected carbon substrates targeting specific biochemical pathways. In this review, the techniques used to measure soil MCA are described and compared with respect to their accuracy and practical use. Particularly the efficiency of MSIR-based approaches as soil microbial function indicators was discussed by (i) showing their sensitivity to different agricultural practices including tillage, amendments, and cropping systems and (ii) by investigating their relationship with soil enzyme activities and some soil chemical properties (pH, soil organic carbon, cation exchange capacity). We highlighted the potential of these MSIR-based MCA measurements to improve microbial inoculant composition and to determine their potential effects on soil microbial functions. Finally, we have proposed ideas for improving MCA measurement notably through the use of molecular tools and stable isotope probing which can be combined with classic MSIR methods.

Graphical Abstract

Graphical abstract describing the interrelation between the different parts and the concepts developed in the review

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  1. Harris J (2009) Soil microbial communities and restoration ecology: facilitators or followers? Science 325:573–574. https://doi.org/10.1126/science.1172975

    Article  CAS  PubMed  Google Scholar 

  2. Ritz K, Black HIJ, Campbell CD et al (2009) Selecting biological indicators for monitoring soils: a framework for balancing scientific and technical opinion to assist policy development. Ecol Indic 9:1212–1221. https://doi.org/10.1016/j.ecolind.2009.02.009

    Article  CAS  Google Scholar 

  3. Song D, Dai X, Guo T et al (2022) Organic amendment regulates soil microbial biomass and activity in wheat-maize and wheat-soybean rotation systems. Agric Ecosyst Environ 333:107974. https://doi.org/10.1016/j.agee.2022.107974

    Article  CAS  Google Scholar 

  4. ISO (2002) ISO16072:2002 soil quality—laboratory methods for determination of microbial soil respiration. ISO. https://www.iso.org/standard/32096.html

  5. Anderson JPE, Domsch KH (1978) A physiological method for the quantitative measurement of microbial biomass in soils. Soil Biol Biochem 10:215–221. https://doi.org/10.1016/0038-0717(78)90099-8

    Article  CAS  Google Scholar 

  6. Herrmann AM, Coucheney E, Nunan N (2014) Isothermal microcalorimetry provides new insight into terrestrial carbon cycling. Environ Sci Technol 48:4344–4352. https://doi.org/10.1021/es403941h

    Article  CAS  PubMed  Google Scholar 

  7. Chakrawal A, Herrmann AM, Manzoni S (2021) Leveraging energy flows to quantify microbial traits in soils. Soil Biol Biochem 155:108169. https://doi.org/10.1016/j.soilbio.2021.108169

    Article  CAS  Google Scholar 

  8. Shi A, Chakrawal A, Manzoni S et al (2021) Substrate spatial heterogeneity reduces soil microbial activity. Soil Biol Biochem 152:108068. https://doi.org/10.1016/j.soilbio.2020.108068

    Article  CAS  Google Scholar 

  9. Sparling GP (1981) Microcalorimetry and other methods to assess biomass and activity in soil. Soil Biol Biochem 13:93–98. https://doi.org/10.1016/0038-0717(81)90002-X

    Article  CAS  Google Scholar 

  10. Sparling GP (1983) Estimation of microbial biomass and activity in soil using microcalorimetry. J Soil Sci 34:381–390. https://doi.org/10.1111/j.1365-2389.1983.tb01043.x

    Article  CAS  Google Scholar 

  11. Raubuch M, Beese F (1999) Comparison of microbial properties measured by O2 consumption and microcalorimetry as bioindicators in forest soils. Soil Biol Biochem 31:949–956. https://doi.org/10.1016/S0038-0717(99)00003-6

    Article  CAS  Google Scholar 

  12. Pamatmat MM, Bhagwat AM (1973) Anaerobic metabolism in Lake Washington sediments1. Limnol Oceanogr 18:611–627. https://doi.org/10.4319/lo.1973.18.4.0611

    Article  CAS  Google Scholar 

  13. Nannipieri P, Trasar-Cepeda C, Dick RP (2018) Soil enzyme activity: a brief history and biochemistry as a basis for appropriate interpretations and meta-analysis. Biol Fertil Soils 54:11–19. https://doi.org/10.1007/s00374-017-1245-6

    Article  CAS  Google Scholar 

  14. Campbell CD, Chapman SJ, Cameron CM et al (2003) A rapid microtiter plate method to measure carbon dioxide evolved from carbon substrate amendments so as to determine the physiological profiles of soil microbial communities by using whole soil. Appl Environ Microbiol 69:3593–3599. https://doi.org/10.1128/AEM.69.6.3593-3599.2003

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Degens BP, Harris JA (1997) Development of a physiological approach to measuring the catabolic diversity of soil microbial communities. Soil Biol Biochem 29:1309–1320. https://doi.org/10.1016/S0038-0717(97)00076-X

    Article  CAS  Google Scholar 

  16. Garland JL, Roberts MS, Levine LH, Mills AL (2003) Community-level physiological profiling performed with an oxygen-sensitive fluorophore in a microtiter plate. Appl Environ Microbiol 69:2994–2998. https://doi.org/10.1128/AEM.69.5.2994-2998.2003

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Garland JL, Mills AL (1991) Classification and characterization of heterotrophic microbial communities on the basis of patterns of community-level sole-carbon-source utilization. Appl Environ Microbiol 57:2351–2359

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Kandeler F, Kampichler C, Horak O (1996) Influence of heavy metals on the functional diversity of soil microbial communities. Biol Fertil Soils 23:299–306. https://doi.org/10.1007/BF00335958

    Article  CAS  Google Scholar 

  19. Pawlett M, Deeks LK, Sakrabani R (2015) Nutrient potential of biosolids and urea derived organo-mineral fertilisers in a field scale experiment using ryegrass (Lolium perenne L.). Field Crops Res 175:56–63. https://doi.org/10.1016/j.fcr.2015.02.006

    Article  Google Scholar 

  20. Martínez-García LB, Korthals G, Brussaard L et al (2018) Organic management and cover crop species steer soil microbial community structure and functionality along with soil organic matter properties. Agric Ecosyst Environ 263:7–17. https://doi.org/10.1016/j.agee.2018.04.018

    Article  Google Scholar 

  21. Govaerts B, Mezzalama M, Unno Y et al (2007) Influence of tillage, residue management, and crop rotation on soil microbial biomass and catabolic diversity. Appl Soil Ecol 37:18–30. https://doi.org/10.1016/j.apsoil.2007.03.006

    Article  Google Scholar 

  22. Bongiorno G, Bünemann EK, Brussaard L et al (2020) Soil management intensity shifts microbial catabolic profiles across a range of European long-term field experiments. Appl Soil Ecol 154:103596. https://doi.org/10.1016/j.apsoil.2020.103596

    Article  Google Scholar 

  23. Bargaz A, Lyamlouli K, Chtouki M, et al (2018) Soil microbial resources for improving fertilizers efficiency in an integrated plant nutrient management system. Front Microbiol 9:. https://doi.org/10.3389/fmicb.2018.01606

  24. Bargaz A, Elhaissoufi W, Khourchi S et al (2021) Benefits of phosphate solubilizing bacteria on belowground crop performance for improved crop acquisition of phosphorus. Microbiol Res 252:126842. https://doi.org/10.1016/j.micres.2021.126842

    Article  CAS  PubMed  Google Scholar 

  25. Daraz U, Li Y, Sun Q et al (2021) Inoculation of Bacillus spp. modulate the soil bacterial communities and available nutrients in the rhizosphere of vetiver plant irrigated with acid mine drainage. Chemosphere 263:128345. https://doi.org/10.1016/j.chemosphere.2020.128345

    Article  CAS  PubMed  Google Scholar 

  26. Li H, Qiu Y, Yao T et al (2020) Effects of PGPR microbial inoculants on the growth and soil properties of Avena sativa, Medicago sativa, and Cucumis sativus seedlings. Soil Tillage Res 199:104577. https://doi.org/10.1016/j.still.2020.104577

    Article  Google Scholar 

  27. Pathak DV, Kumar M (2016) Microbial inoculants as biofertilizers and biopesticides. In: Singh DP, Singh HB, Prabha R (eds) Microbial inoculants in sustainable agricultural productivity, vol 1. research perspectives. Springer India, New Delhi, pp 197–209

    Chapter  Google Scholar 

  28. Smith SE, Read DJ (2008) Mycorrhizal symbiosis. Elsevier, New York, USA

    Google Scholar 

  29. Soumare A, Diedhiou AG, Thuita M et al (2020) Exploiting biological nitrogen fixation: a route towards a sustainable agriculture. Plants 9:1011. https://doi.org/10.3390/plants9081011

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Vessey JK (2003) Plant growth promoting rhizobacteria as biofertilizers. Plant Soil 255:571–586. https://doi.org/10.1023/A:1026037216893

    Article  CAS  Google Scholar 

  31. Dong L, Li Y, Xu J et al (2019) Biofertilizers regulate the soil microbial community and enhance Panax ginseng yields. Chin Med 14:20. https://doi.org/10.1186/s13020-019-0241-1

    Article  PubMed  PubMed Central  Google Scholar 

  32. Naseby DC, Pascual JA, Lynch JM (2000) Effect of biocontrol strains of Trichoderma on plant growth, Pythium ultimum populations, soil microbial communities and soil enzyme activities. J Appl Microbiol 88:161–169. https://doi.org/10.1046/j.1365-2672.2000.00939.x

    Article  CAS  PubMed  Google Scholar 

  33. Trabelsi D, Mhamdi R (2013) Microbial inoculants and their impact on soil microbial communities: a review. BioMed Res Int 2013:e863240. https://doi.org/10.1155/2013/863240

    Article  Google Scholar 

  34. Yang T, Lupwayi N, Marc S-A et al (2021) Anthropogenic drivers of soil microbial communities and impacts on soil biological functions in agroecosystems. Glob Ecol Conserv 27:e01521. https://doi.org/10.1016/j.gecco.2021.e01521

    Article  Google Scholar 

  35. Zhang F, Huo Y, Cobb AB, et al (2018) Trichoderma biofertilizer links to altered soil chemistry, altered microbial communities, and improved grassland biomass. Front Microbiol 9. https://doi.org/10.3389/fmicb.2018.00848

  36. Siczek A, Lipiec J (2016) Impact of faba bean-seed rhizobial inoculation on microbial activity in the rhizosphere soil during growing season. Int J Mol Sci 17:784. https://doi.org/10.3390/ijms17050784

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Minasny B, Malone BP, McBratney AB et al (2017) Soil carbon 4 per mille. Geoderma 292:59–86. https://doi.org/10.1016/j.geoderma.2017.01.002

    Article  Google Scholar 

  38. Blagodatskaya E, Kuzyakov Y (2013) Active microorganisms in soil: critical review of estimation criteria and approaches. Soil Biol Biochem 67:192–211. https://doi.org/10.1016/j.soilbio.2013.08.024

    Article  CAS  Google Scholar 

  39. Chapman SJ, Campbell CD, Artz RRE (2007) Assessing CLPPs using MicroResp™. J Soils Sediments 7:406–410. https://doi.org/10.1065/jss2007.10.259

    Article  Google Scholar 

  40. Insam H (1997) A new set of substrates proposed for community characterization in environmental samples. In: Insam H, Rangger A (eds) Microbial communities. Springer, Berlin, Heidelberg, pp 259–260

    Chapter  Google Scholar 

  41. Oren A, Steinberger Y (2008) Catabolic profiles of soil fungal communities along a geographic climatic gradient in Israel. Soil Biol Biochem 40:2578–2587. https://doi.org/10.1016/j.soilbio.2008.05.024

    Article  CAS  Google Scholar 

  42. Sassi MB, Dollinger J, Renault P et al (2012) The FungiResp method: an application of the MicroResp™ method to assess fungi in microbial communities as soil biological indicators. Ecol Indic 23:482–490. https://doi.org/10.1016/j.ecolind.2012.05.002

    Article  Google Scholar 

  43. Pignataro A, Moscatelli MC, Mocali S et al (2012) Assessment of soil microbial functional diversity in a coppiced forest system. Appl Soil Ecol 62:115–123. https://doi.org/10.1016/j.apsoil.2012.07.007

    Article  Google Scholar 

  44. Asadishad B, Chahal S, Akbari A et al (2018) Amendment of agricultural soil with metal nanoparticles: effects on soil enzyme activity and microbial community composition. Environ Sci Technol 52:1908–1918. https://doi.org/10.1021/acs.est.7b05389

    Article  CAS  PubMed  Google Scholar 

  45. Epelde L, Becerril JM, Hernández-Allica J et al (2008) Functional diversity as indicator of the recovery of soil health derived from Thlaspi caerulescens growth and metal phytoextraction. Appl Soil Ecol 39:299–310. https://doi.org/10.1016/j.apsoil.2008.01.005

    Article  Google Scholar 

  46. Moscatelli MC, Secondi L, Marabottini R et al (2018) Assessment of soil microbial functional diversity: land use and soil properties affect CLPP-MicroResp and enzymes responses. Pedobiologia 66:36–42. https://doi.org/10.1016/j.pedobi.2018.01.001

    Article  Google Scholar 

  47. Hoang SA, Lamb D, Sarkar B et al (2022) Phosphorus application enhances alkane hydroxylase gene abundance in the rhizosphere of wild plants grown in petroleum-hydrocarbon-contaminated soil. Environ Res 204:111924. https://doi.org/10.1016/j.envres.2021.111924

    Article  CAS  PubMed  Google Scholar 

  48. Chen X, Jiang N, Chen Z et al (2017) Response of soil phoD phosphatase gene to long-term combined applications of chemical fertilizers and organic materials. Appl Soil Ecol 119:197–204. https://doi.org/10.1016/j.apsoil.2017.06.019

    Article  Google Scholar 

  49. Fraser TD, Lynch DH, Gaiero J et al (2017) Quantification of bacterial non-specific acid (phoC) and alkaline (phoD) phosphatase genes in bulk and rhizosphere soil from organically managed soybean fields. Appl Soil Ecol 111:48–56. https://doi.org/10.1016/j.apsoil.2016.11.013

    Article  Google Scholar 

  50. Luo G, Sun B, Li L et al (2019) Understanding how long-term organic amendments increase soil phosphatase activities: insight into phoD- and phoC-harboring functional microbial populations. Soil Biol Biochem 139:107632. https://doi.org/10.1016/j.soilbio.2019.107632

    Article  CAS  Google Scholar 

  51. de Oliveira Santos T, CuryFracetto FJ, de Severino Souza Júnior V et al (2022) Carbon and nitrogen stocks and microbial indicators in tropical semiarid degraded Luvisols. CATENA 210:105885. https://doi.org/10.1016/j.catena.2021.105885

    Article  CAS  Google Scholar 

  52. Zheng B, Zhu Y, Sardans J et al (2018) QMEC: a tool for high-throughput quantitative assessment of microbial functional potential in C, N, P, and S biogeochemical cycling. Sci China Life Sci 61:1451–1462. https://doi.org/10.1007/s11427-018-9364-7

    Article  CAS  PubMed  Google Scholar 

  53. Rosado-Porto D, Ratering S, Wohlfahrt Y et al (2023) Elevated atmospheric CO2 concentrations caused a shift of the metabolically active microbiome in vineyard soil. BMC Microbiol 23:46. https://doi.org/10.1186/s12866-023-02781-5

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  54. Khan S, Afzal M, Iqbal S et al (2013) Inoculum pretreatment affects bacterial survival, activity and catabolic gene expression during phytoremediation of diesel contaminated soil. Chemosphere 91:663–668. https://doi.org/10.1016/j.chemosphere.2013.01.025

    Article  CAS  PubMed  Google Scholar 

  55. Yergeau E, Kang S, He Z et al (2007) Functional microarray analysis of nitrogen and carbon cycling genes across an Antarctic latitudinal transect. ISME J 1:163–179. https://doi.org/10.1038/ismej.2007.24

    Article  CAS  PubMed  Google Scholar 

  56. Xue K, Xie J, Zhou A, et al (2016) Warming alters expressions of microbial functional genes important to ecosystem functioning. Front Microbiol 7:

  57. Wu F, You Y, Werner D et al (2020) Carbon nanomaterials affect carbon cycle-related functions of the soil microbial community and the coupling of nutrient cycles. J Hazard Mater 390:122144. https://doi.org/10.1016/j.jhazmat.2020.122144

    Article  CAS  PubMed  Google Scholar 

  58. Cheng J, Yang Y, Yuan MM et al (2021) Winter warming rapidly increases carbon degradation capacities of fungal communities in tundra soil: potential consequences on carbon stability. Mol Ecol 30:926–937. https://doi.org/10.1111/mec.15773

    Article  CAS  PubMed  Google Scholar 

  59. Urich T, Lanzén A, Qi J et al (2008) Simultaneous assessment of soil microbial community structure and function through analysis of the meta-transcriptome. Plos One 3:e2527. https://doi.org/10.1371/journal.pone.0002527

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  60. Geisen S, Briones MJI, Gan H et al (2019) A methodological framework to embrace soil biodiversity. Soil Biol Biochem 136:107536. https://doi.org/10.1016/j.soilbio.2019.107536

    Article  CAS  Google Scholar 

  61. Enebe MC, Babalola OO (2021) Soil fertilization affects the abundance and distribution of carbon and nitrogen cycling genes in the maize rhizosphere. AMB Express 11:24. https://doi.org/10.1186/s13568-021-01182-z

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  62. Kelly CN, Schwaner GW, Cumming JR, Driscoll TP (2021) Metagenomic reconstruction of nitrogen and carbon cycling pathways in forest soil: influence of different hardwood tree species. Soil Biol Biochem 156:108226. https://doi.org/10.1016/j.soilbio.2021.108226

    Article  CAS  Google Scholar 

  63. Martens R (1987) Estimation of microbial biomass in soil by the respiration method: importance of soil pH and flushing methods for the measurement of respired CO2. Soil Biol Biochem 19:77–81. https://doi.org/10.1016/0038-0717(87)90128-3

    Article  CAS  Google Scholar 

  64. Sparling GP, West AW (1990) A comparison of gas chromatography and differential respirometer methods to measure soil respiration and to estimate the soil microbial biomass. Pedobiologia 34:103–112

    CAS  Google Scholar 

  65. Oren A, Steinberger Y (2008) Coping with artifacts induced by CaCO3–CO2–H2O equilibria in substrate utilization profiling of calcareous soils. Soil Biol Biochem 40:2569–2577. https://doi.org/10.1016/j.soilbio.2008.06.020

    Article  CAS  Google Scholar 

  66. Jones DL, Edwards AC (1998) Influence of sorption on the biological utilization of two simple carbon substrates. Soil Biol Biochem 30:1895–1902. https://doi.org/10.1016/S0038-0717(98)00060-1

    Article  CAS  Google Scholar 

  67. Nguyen C (2003) Rhizodeposition of organic C by plants: mechanisms and controls. Agron Sustain Dev 23:22. https://doi.org/10.1051/agro:2003011

    Article  CAS  Google Scholar 

  68. Sasse J, Martinoia E, Northen T (2018) Feed your friends: do plant exudates shape the root microbiome? Trends Plant Sci 23:25–41. https://doi.org/10.1016/j.tplants.2017.09.003

    Article  CAS  PubMed  Google Scholar 

  69. Braissant O, Wirz D, Göpfert B, Daniels AU (2010) Use of isothermal microcalorimetry to monitor microbial activities. FEMS Microbiol Lett 303:1–8. https://doi.org/10.1111/j.1574-6968.2009.01819.x

    Article  CAS  PubMed  Google Scholar 

  70. Harris JA, Ritz K, Coucheney E et al (2012) The thermodynamic efficiency of soil microbial communities subject to long-term stress is lower than those under conventional input regimes. Soil Biol Biochem 47:149–157. https://doi.org/10.1016/j.soilbio.2011.12.017

    Article  CAS  Google Scholar 

  71. Thiele-Bruhn S, Schloter M, Wilke B-M et al (2020) Identification of new microbial functional standards for soil quality assessment. SOIL 6:17–34. https://doi.org/10.5194/soil-6-17-2020

    Article  CAS  Google Scholar 

  72. Lewis G, (Dan) Daniels AU (2003) Use of isothermal heat-conduction microcalorimetry (IHCMC) for the evaluation of synthetic biomaterials. J Biomed Mater Res B Appl Biomater 66B:487–501. https://doi.org/10.1002/jbm.b.10044

    Article  CAS  Google Scholar 

  73. Nannipieri P, Giagnoni L, Renella G et al (2012) Soil enzymology: classical and molecular approaches. Biol Fertil Soils 48:743–762. https://doi.org/10.1007/s00374-012-0723-0

    Article  Google Scholar 

  74. Mangalassery S, Mooney SJ, Sparkes DL et al (2015) Impacts of zero tillage on soil enzyme activities, microbial characteristics and organic matter functional chemistry in temperate soils. Eur J Soil Biol 68:9–17. https://doi.org/10.1016/j.ejsobi.2015.03.001

    Article  CAS  Google Scholar 

  75. Guangming L, Xuechen Z, Xiuping W et al (2017) Soil enzymes as indicators of saline soil fertility under various soil amendments. Agric Ecosyst Environ 237:274–279. https://doi.org/10.1016/j.agee.2017.01.004

    Article  CAS  Google Scholar 

  76. Knight TR, Dick RP (2004) Differentiating microbial and stabilized β-glucosidase activity relative to soil quality. Soil Biol Biochem 36:2089–2096. https://doi.org/10.1016/j.soilbio.2004.06.007

    Article  CAS  Google Scholar 

  77. Pawlik M, Płociniczak T, Thijs S et al (2020) Comparison of two inoculation methods of endophytic bacteria to enhance phytodegradation efficacy of an aged petroleum hydrocarbons polluted soil. Agronomy 10:1196. https://doi.org/10.3390/agronomy10081196

    Article  CAS  Google Scholar 

  78. El Azhari N, Devers-Lamrani M, Chatagnier G et al (2010) Molecular analysis of the catechol-degrading bacterial community in a coal wasteland heavily contaminated with PAHs. J Hazard Mater 177:593–601. https://doi.org/10.1016/j.jhazmat.2009.12.074

    Article  CAS  PubMed  Google Scholar 

  79. El Azhari N, Bru D, Sarr A, Martin-Laurent F (2008) Estimation of the density of the protocatechuate-degrading bacterial community in soil by real-time PCR. Eur J Soil Sci 59:665–673. https://doi.org/10.1111/j.1365-2389.2008.01029.x

    Article  CAS  Google Scholar 

  80. He Z, Gentry TJ, Schadt CW et al (2007) GeoChip: a comprehensive microarray for investigating biogeochemical, ecological and environmental processes. ISME J 1:67–77. https://doi.org/10.1038/ismej.2007.2

    Article  CAS  PubMed  Google Scholar 

  81. Creamer RE, Stone D, Berry P, Kuiper I (2016) Measuring respiration profiles of soil microbial communities across Europe using MicroResp™ method. Appl Soil Ecol 97:36–43. https://doi.org/10.1016/j.apsoil.2015.08.004

    Article  Google Scholar 

  82. Marchante E, Kjøller A, Struwe S, Freitas H (2008) Invasive Acacia longifolia induce changes in the microbial catabolic diversity of sand dunes. Soil Biol Biochem 40:2563–2568. https://doi.org/10.1016/j.soilbio.2008.06.017

    Article  CAS  Google Scholar 

  83. Sall SN, Masse D, Ndour NYB, Chotte J-L (2006) Does cropping modify the decomposition function and the diversity of the soil microbial community of tropical fallow soil? Appl Soil Ecol 31:211–219. https://doi.org/10.1016/j.apsoil.2005.05.007

    Article  Google Scholar 

  84. Grządziel J, Furtak K, Gałązka A (2019) Community-level physiological profiles of microorganisms from different types of soil that are characteristic to Poland—a long-term microplot experiment. Sustainability 11:56. https://doi.org/10.3390/su11010056

    Article  CAS  Google Scholar 

  85. Degens BP, Schipper LA, Sparling GP, Vojvodic-Vukovic M (2000) Decreases in organic C reserves in soils can reduce the catabolic diversity of soil microbial communities. Soil Biol Biochem 32:189–196. https://doi.org/10.1016/S0038-0717(99)00141-8

    Article  CAS  Google Scholar 

  86. Gomez E, Ferreras L, Toresani S (2006) Soil bacterial functional diversity as influenced by organic amendment application. Bioresour Technol 97:1484–1489. https://doi.org/10.1016/j.biortech.2005.06.021

    Article  CAS  PubMed  Google Scholar 

  87. van der Bom F, Nunes I, Raymond NS et al (2018) Long-term fertilisation form, level and duration affect the diversity, structure and functioning of soil microbial communities in the field. Soil Biol Biochem 122:91–103. https://doi.org/10.1016/j.soilbio.2018.04.003

    Article  CAS  Google Scholar 

  88. Lagomarsino A, Grego S, Kandeler E (2012) Soil organic carbon distribution drives microbial activity and functional diversity in particle and aggregate-size fractions. Pedobiologia 55:101–110. https://doi.org/10.1016/j.pedobi.2011.12.002

    Article  CAS  Google Scholar 

  89. Fierer N, Jackson RB (2006) The diversity and biogeography of soil bacterial communities. Proc Natl Acad Sci U S A 103:626–631. https://doi.org/10.1073/pnas.0507535103

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  90. Lemanceau P, Maron P-A, Mazurier S et al (2015) Understanding and managing soil biodiversity: a major challenge in agroecology. Agron Sustain Dev 35:67–81. https://doi.org/10.1007/s13593-014-0247-0

    Article  CAS  Google Scholar 

  91. Wakelin SA, Macdonald LM, Rogers SL et al (2008) Habitat selective factors influencing the structural composition and functional capacity of microbial communities in agricultural soils. Soil Biol Biochem 40:803–813. https://doi.org/10.1016/j.soilbio.2007.10.015

    Article  CAS  Google Scholar 

  92. Sradnick A, Murugan R, Oltmanns M et al (2013) Changes in functional diversity of the soil microbial community in a heterogeneous sandy soil after long-term fertilization with cattle manure and mineral fertilizer. Appl Soil Ecol 63:23–28. https://doi.org/10.1016/j.apsoil.2012.09.011

    Article  Google Scholar 

  93. Andruschkewitsch M, Wachendorf C, Sradnick A et al (2014) Soil substrate utilization pattern and relation of functional evenness of plant groups and soil microbial community in five low mountain NATURA 2000. Plant Soil 383:275–289. https://doi.org/10.1007/s11104-014-2167-9

    Article  CAS  Google Scholar 

  94. McDaniel MD, Grandy AS (2016) Soil microbial biomass and function are altered by 12 years of crop rotation. SOIL 2:583–599. https://doi.org/10.5194/soil-2-583-2016

    Article  CAS  Google Scholar 

  95. Iwai CB, Oo AN, Topark-ngarm B (2012) Soil property and microbial activity in natural salt affected soils in an alternating wet–dry tropical climate. Geoderma 189–190:144–152. https://doi.org/10.1016/j.geoderma.2012.05.001

    Article  CAS  Google Scholar 

  96. Frąc M, Oszust K, Lipiec J (2012) Community level physiological profiles (CLPP), characterization and microbial activity of soil amended with dairy sewage sludge. Sensors 12:3253–3268. https://doi.org/10.3390/s120303253

    Article  PubMed  PubMed Central  Google Scholar 

  97. Chakraborty A, Chakrabarti K, Chakraborty A, Ghosh S (2011) Effect of long-term fertilizers and manure application on microbial biomass and microbial activity of a tropical agricultural soil. Biol Fertil Soils 47:227–233. https://doi.org/10.1007/s00374-010-0509-1

    Article  Google Scholar 

  98. Arslan M, Afzal M, Amin I et al (2014) Nutrients can enhance the abundance and expression of alkane hydroxylase CYP153 gene in the rhizosphere of ryegrass planted in hydrocarbon-polluted soil. Plos One 9:e111208. https://doi.org/10.1371/journal.pone.0111208

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  99. Sun B, Jia S, Zhang S et al (2016) No tillage combined with crop rotation improves soil microbial community composition and metabolic activity. Environ Sci Pollut Res 23:6472–6482. https://doi.org/10.1007/s11356-015-5812-9

    Article  CAS  Google Scholar 

  100. Gomez E, Garland J, Conti M (2004) Reproducibility in the response of soil bacterial community-level physiological profiles from a land use intensification gradient. Appl Soil Ecol 26:21–30. https://doi.org/10.1016/j.apsoil.2003.10.007

    Article  Google Scholar 

  101. Ma T, Luo Y, Christie P et al (2012) Removal of phthalic esters from contaminated soil using different cropping systems: a field study. Eur J Soil Biol 50:76–82. https://doi.org/10.1016/j.ejsobi.2011.12.001

    Article  CAS  Google Scholar 

  102. Pankhurst CE, Stirling GR, Magarey RC et al (2005) Quantification of the effects of rotation breaks on soil biological properties and their impact on yield decline in sugarcane. Soil Biol Biochem 37:1121–1130. https://doi.org/10.1016/j.soilbio.2004.11.011

    Article  CAS  Google Scholar 

  103. Wu L, Li Z, Li J et al (2013) Assessment of shifts in microbial community structure and catabolic diversity in response to Rehmannia glutinosa monoculture. Appl Soil Ecol 67:1–9. https://doi.org/10.1016/j.apsoil.2013.02.008

    Article  Google Scholar 

  104. Kavamura VN, Hayat R, Clark IM, et al (2018) Inorganic nitrogen application affects both taxonomical and predicted functional structure of wheat rhizosphere bacterial communities. Front Microbiol 9:

  105. Wu L, Wang H, Zhang Z et al (2011) Comparative Metaproteomic analysis on consecutively Rehmannia glutinosa-monocultured rhizosphere soil. Plos One 6:e20611. https://doi.org/10.1371/journal.pone.0020611

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  106. Ceccanti B, Doni S, Macci C et al (2008) Characterization of stable humic–enzyme complexes of different soil ecosystems through analytical isoelectric focussing technique (IEF). Soil Biol Biochem 40:2174–2177. https://doi.org/10.1016/j.soilbio.2008.02.004

    Article  CAS  Google Scholar 

  107. el ZaharHaichar F, Santaella C, Heulin T, Achouak W (2014) Root exudates mediated interactions belowground. Soil Biol Biochem 77:69–80. https://doi.org/10.1016/j.soilbio.2014.06.017

    Article  CAS  Google Scholar 

  108. Ndour PMS, Heulin T, Achouak W et al (2020) The rhizosheath: from desert plants adaptation to crop breeding. Plant Soil 456:1–13. https://doi.org/10.1007/s11104-020-04700-3

    Article  CAS  Google Scholar 

  109. Giagnoni L, Pastorelli R, Mocali S et al (2016) Availability of different nitrogen forms changes the microbial communities and enzyme activities in the rhizosphere of maize lines with different nitrogen use efficiency. Appl Soil Ecol 98:30–38. https://doi.org/10.1016/j.apsoil.2015.09.004

    Article  Google Scholar 

  110. Ndour PMS, Barry CM, Tine D et al (2021) Pearl millet genotype impacts microbial diversity and enzymatic activities in relation to root-adhering soil aggregation. Plant Soil 464:109–129. https://doi.org/10.1007/s11104-021-04917-w

    Article  CAS  Google Scholar 

  111. Pathan SI, Ceccherini MT, Pietramellara G et al (2015) Enzyme activity and microbial community structure in the rhizosphere of two maize lines differing in N use efficiency. Plant Soil 387:413–424. https://doi.org/10.1007/s11104-014-2306-3

    Article  CAS  Google Scholar 

  112. Söderberg KH, Probanza A, Jumpponen A, Bååth E (2004) The microbial community in the rhizosphere determined by community-level physiological profiles (CLPP) and direct soil– and cfu–PLFA techniques. Appl Soil Ecol 25:135–145. https://doi.org/10.1016/j.apsoil.2003.08.005

    Article  Google Scholar 

  113. Brolsma KM, Vonk JA, Mommer L et al (2017) Microbial catabolic diversity in and beyond the rhizosphere of plant species and plant genotypes. Pedobiologia 61:43–49. https://doi.org/10.1016/j.pedobi.2017.01.006

    Article  Google Scholar 

  114. Wang L, Wang J, Guo D, Jiang A (2020) Catabolic activity and structural diversity of bacterial community in soil covered by halophytic vegetation. Curr Microbiol 77:1821–1828. https://doi.org/10.1007/s00284-020-02001-7

    Article  CAS  PubMed  Google Scholar 

  115. Wahbi S, Prin Y, Thioulouse J et al (2016) Impact of wheat/faba bean mixed cropping or rotation systems on soil microbial functionalities. Front Plant Sci 7:1364. https://doi.org/10.3389/fpls.2016.01364

    Article  PubMed  PubMed Central  Google Scholar 

  116. Aulakh MS, Wassmann R, Bueno C et al (2001) Characterization of root exudates at different growth stages of ten rice (Oryza sativa L.) cultivars. Plant Biol 3:139–148. https://doi.org/10.1055/s-2001-12905

    Article  CAS  Google Scholar 

  117. Micallef SA, Shiaris MP, Colón-Carmona A (2009) Influence of Arabidopsis thaliana accessions on rhizobacterial communities and natural variation in root exudates. J Exp Bot 60:1729–1742. https://doi.org/10.1093/jxb/erp053

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  118. Mönchgesang S, Strehmel N, Schmidt S et al (2016) Natural variation of root exudates in Arabidopsis thaliana-linking metabolomic and genomic data. Sci Rep 6:29033. https://doi.org/10.1038/srep29033

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  119. Dietz S, Herz K, Gorzolka K et al (2020) Root exudate composition of grass and forb species in natural grasslands. Sci Rep 10:10691. https://doi.org/10.1038/s41598-019-54309-5

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  120. Tang X, Bernard L, Brauman A et al (2014) Increase in microbial biomass and phosphorus availability in the rhizosphere of intercropped cereal and legumes under field conditions. Soil Biol Biochem 75:86–93. https://doi.org/10.1016/j.soilbio.2014.04.001

    Article  CAS  Google Scholar 

  121. Gentsch N, Boy J, Batalla JDK et al (2020) Catch crop diversity increases rhizosphere carbon input and soil microbial biomass. Biol Fertil Soils 56:943–957. https://doi.org/10.1007/s00374-020-01475-8

    Article  CAS  Google Scholar 

  122. Cardozo Junior FM, Carneiro RFV, Rocha SMB et al (2018) The impact of pasture systems on soil microbial biomass and community-level physiological profiles. Land Degrad Dev 29:284–291. https://doi.org/10.1002/ldr.2565

    Article  Google Scholar 

  123. Mureva A, Ward D (2017) Soil microbial biomass and functional diversity in shrub-encroached grasslands along a precipitation gradient. Pedobiologia 63:37–45. https://doi.org/10.1016/j.pedobi.2017.06.006

    Article  Google Scholar 

  124. Vives-Peris V, de Ollas C, Gómez-Cadenas A, Pérez-Clemente RM (2020) Root exudates: from plant to rhizosphere and beyond. Plant Cell Rep 39:3–17. https://doi.org/10.1007/s00299-019-02447-5

    Article  CAS  PubMed  Google Scholar 

  125. Marilley L, Aragno M (1999) Phylogenetic diversity of bacterial communities differing in degree of proximity of Lolium perenne and Trifolium repens roots. Appl Soil Ecol 13:127–136. https://doi.org/10.1016/S0929-1393(99)00028-1

    Article  Google Scholar 

  126. Schreiter S, Ding G-C, Heuer H, et al (2014) Effect of the soil type on the microbiome in the rhizosphere of field-grown lettuce. Front Microbiol 5:. https://doi.org/10.3389/fmicb.2014.00144

  127. Shi S, Nuccio E, Herman DJ et al (2015) Successional trajectories of rhizosphere bacterial communities over consecutive seasons. mBio 6:e00746-15. https://doi.org/10.1128/mBio.00746-15

    Article  PubMed  PubMed Central  Google Scholar 

  128. Ling N, Wang T, Kuzyakov Y (2022) Rhizosphere bacteriome structure and functions. Nat Commun 13:836. https://doi.org/10.1038/s41467-022-28448-9

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  129. Reid TE, Kavamura VN, Abadie M et al (2021) Inorganic chemical fertilizer application to wheat reduces the abundance of putative plant growth-promoting rhizobacteria. Front Microbiol 12:642587. https://doi.org/10.3389/fmicb.2021.642587

  130. Kumar A, Jha MN, Singh D et al (2021) Prospecting catabolic diversity of microbial strains for developing microbial consortia and their synergistic effect on lentil (Lens esculenta) growth, yield and iron biofortification. Arch Microbiol. https://doi.org/10.1007/s00203-021-02446-9

    Article  PubMed  PubMed Central  Google Scholar 

  131. Figueiredo MVB, Burity HA, Martínez CR, Chanway CP (2008) Alleviation of drought stress in the common bean (Phaseolus vulgaris L.) by co-inoculation with Paenibacillus polymyxa and Rhizobium tropici. Appl Soil Ecol 40:182–188. https://doi.org/10.1016/j.apsoil.2008.04.005

    Article  Google Scholar 

  132. Hungria M, Nogueira MA, Araujo RS (2013) Co-inoculation of soybeans and common beans with rhizobia and azospirilla: strategies to improve sustainability. Biol Fertil Soils 49:791–801. https://doi.org/10.1007/s00374-012-0771-5

    Article  Google Scholar 

  133. Korir H, Mungai NW, Thuita M et al (2017) Co-inoculation effect of rhizobia and plant growth promoting rhizobacteria on common bean growth in a low phosphorus soil. Front Plant Sci 8:141. https://doi.org/10.3389/fpls.2017.00141

    Article  PubMed  PubMed Central  Google Scholar 

  134. Kumar P, Thakur S, Dhingra GK et al (2018) Inoculation of siderophore producing rhizobacteria and their consortium for growth enhancement of wheat plant. Biocatal Agric Biotechnol 15:264–269. https://doi.org/10.1016/j.bcab.2018.06.019

    Article  Google Scholar 

  135. Ye B, Saito A, Minamisawa K (2005) Effect of inoculation with anaerobic nitrogen-fixing consortium on salt tolerance of Miscanthus sinensis. Soil Sci Plant Nutr 51:243–249. https://doi.org/10.1111/j.1747-0765.2005.tb00028.x

    Article  Google Scholar 

  136. Ge J, Li D, Ding J et al (2023) Microbial coexistence in the rhizosphere and the promotion of plant stress resistance: a review. Environ Res 222:115298. https://doi.org/10.1016/j.envres.2023.115298

    Article  CAS  PubMed  Google Scholar 

  137. Geller AM, Levy A (2023) “What I cannot create, I do not understand”: elucidating microbe–microbe interactions to facilitate plant microbiome engineering. Curr Opin Microbiol 72:102283. https://doi.org/10.1016/j.mib.2023.102283

    Article  PubMed  Google Scholar 

  138. Poppeliers SW, Sánchez-Gil JJ, de Jonge R (2023) Microbes to support plant health: understanding bioinoculant success in complex conditions. Curr Opin Microbiol 73:102286. https://doi.org/10.1016/j.mib.2023.102286

    Article  PubMed  Google Scholar 

  139. Moore JAM, Abraham PE, Michener JK et al (2022) Ecosystem consequences of introducing plant growth promoting rhizobacteria to managed systems and potential legacy effects. New Phytol n/a. https://doi.org/10.1111/nph.18010

    Article  Google Scholar 

  140. Ndour PMS, Hatté C, Achouak W et al (2022) Rhizodeposition efficiency of pearl millet genotypes assessed on short growing period by carbon isotopes (δ13C and F14C). SOIL 8:49–57. https://doi.org/10.5194/soil-8-49-2022

    Article  CAS  Google Scholar 

  141. Mawarda PC, Le Roux X, Dirk van Elsas J, Salles JF (2020) Deliberate introduction of invisible invaders: a critical appraisal of the impact of microbial inoculants on soil microbial communities. Soil Biol Biochem 148:107874. https://doi.org/10.1016/j.soilbio.2020.107874

    Article  CAS  Google Scholar 

  142. Ma M, Jiang X, Wang Q, et al (2018) Isolation and identification of PGPR strain and its effect on soybean growth and soil bacterial community composition. Int J Agric Biol 20:. https://doi.org/10.17957/IJAB/15.0627

  143. Kim KY, Jordan D, McDonald GA (1997) Effect of phosphate-solubilizing bacteria and vesicular-arbuscular mycorrhizae on tomato growth and soil microbial activity. Biol Fertil Soils 26:79–87. https://doi.org/10.1007/s003740050347

    Article  Google Scholar 

  144. Sun YM, Zhang NN, Wang ET et al (2009) Influence of intercropping and intercropping plus rhizobial inoculation on microbial activity and community composition in rhizosphere of alfalfa (Medicago sativa L.) and Siberian wild rye (Elymus sibiricus L.). FEMS Microbiol Ecol 70:218–226. https://doi.org/10.1111/j.1574-6941.2009.00752.x

    Article  CAS  Google Scholar 

  145. Garcia C, Hernandez T, Roldan A et al (2000) Organic amendment and mycorrhizal inoculation as a practice in afforestation of soils with Pinus halepensis Miller: effect on their microbial activity. Soil Biol Biochem 32:1173–1181. https://doi.org/10.1016/S0038-0717(00)00033-X

    Article  CAS  Google Scholar 

  146. Alguacil MM, Caravaca F, Roldán A (2005) Changes in rhizosphere microbial activity mediated by native or allochthonous AM fungi in the reafforestation of a Mediterranean degraded environment. Biol Fertil Soils 41:59–68. https://doi.org/10.1007/s00374-004-0788-5

    Article  Google Scholar 

  147. Xiao L, Bi Y, Du S et al (2019) Effects of re-vegetation type and arbuscular mycorrhizal fungal inoculation on soil enzyme activities and microbial biomass in coal mining subsidence areas of Northern China. CATENA 177:202–209. https://doi.org/10.1016/j.catena.2019.02.019

    Article  CAS  Google Scholar 

  148. Lebrun M, Miard F, Bucci A et al (2021) Evaluation of direct and biochar carrier-based inoculation of Bacillus sp. on As- and Pb-contaminated technosol: effect on metal(loid) availability, Salix viminalis growth, and soil microbial diversity/activity. Environ Sci Pollut Res 28:11195–11204. https://doi.org/10.1007/s11356-020-11355-1

    Article  CAS  Google Scholar 

  149. Duponnois R, Colombet A, Hien V, Thioulouse J (2005) The mycorrhizal fungus Glomus intraradices and rock phosphate amendment influence plant growth and microbial activity in the rhizosphere of Acacia holosericea. Soil Biol Biochem 37:1460–1468. https://doi.org/10.1016/j.soilbio.2004.09.016

    Article  CAS  Google Scholar 

  150. Dabire AP, Hien V, Kisa M et al (2007) Responses of soil microbial catabolic diversity to arbuscular mycorrhizal inoculation and soil disinfection. Mycorrhiza 17:537–545. https://doi.org/10.1007/s00572-007-0126-5

    Article  CAS  PubMed  Google Scholar 

  151. Dinsdale EA, Edwards RA, Hall D et al (2008) Functional metagenomic profiling of nine biomes. Nature 452:629–632. https://doi.org/10.1038/nature06810

    Article  CAS  PubMed  Google Scholar 

  152. Delmont TO, Prestat E, Keegan KP et al (2012) Structure, fluctuation and magnitude of a natural grassland soil metagenome. ISME J 6:1677–1687. https://doi.org/10.1038/ismej.2011.197

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  153. Yang Y, Gao Y, Wang S et al (2014) The microbial gene diversity along an elevation gradient of the Tibetan grassland. ISME J 8:430–440. https://doi.org/10.1038/ismej.2013.146

    Article  CAS  PubMed  Google Scholar 

  154. Clark IM, Hughes DJ, Fu Q et al (2021) Metagenomic approaches reveal differences in genetic diversity and relative abundance of nitrifying bacteria and archaea in contrasting soils. Sci Rep 11:15905. https://doi.org/10.1038/s41598-021-95100-9

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  155. Jones DL, Hill PW, Smith AR et al (2018) Role of substrate supply on microbial carbon use efficiency and its role in interpreting soil microbial community-level physiological profiles (CLPP). Soil Biol Biochem 123:1–6. https://doi.org/10.1016/j.soilbio.2018.04.014

    Article  CAS  Google Scholar 

  156. Cantarel BL, Coutinho PM, Rancurel C et al (2009) The Carbohydrate-Active EnZymes database (CAZy): an expert resource for glycogenomics. Nucleic Acids Res 37:D233–D238. https://doi.org/10.1093/nar/gkn663

    Article  CAS  PubMed  Google Scholar 

  157. Lombard V, Golaconda Ramulu H, Drula E et al (2014) The carbohydrate-active enzymes database (CAZy) in 2013. Nucleic Acids Res 42:D490–D495. https://doi.org/10.1093/nar/gkt1178

    Article  CAS  PubMed  Google Scholar 

  158. Rawlings ND, O’Brien E, Barrett AJ (2002) MEROPS: the protease database. Nucleic Acids Res 30:343–346. https://doi.org/10.1093/nar/30.1.343

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  159. Radajewski S, Webster G, Reay DS et al (2002) Identification of active methylotroph populations in an acidic forest soil by stable-isotope probing. Microbiology 148:2331–2342. https://doi.org/10.1099/00221287-148-8-2331

    Article  CAS  PubMed  Google Scholar 

  160. Ginige MP, Hugenholtz P, Daims H et al (2004) Use of stable-isotope probing, full-cycle rRNA analysis, and fluorescence in situ hybridization-microautoradiography to study a methanol-fed denitrifying microbial community. Appl Environ Microbiol 70:588–596. https://doi.org/10.1128/AEM.70.1.588-596.2004

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  161. Lemanski K, Scheu S (2014) Incorporation of 13C labelled glucose into soil microorganisms of grassland: effects of fertilizer addition and plant functional group composition. Soil Biol Biochem 69:38–45. https://doi.org/10.1016/j.soilbio.2013.10.034

    Article  CAS  Google Scholar 

  162. Ai C, Liang G, Sun J et al (2015) Reduced dependence of rhizosphere microbiome on plant-derived carbon in 32-year long-term inorganic and organic fertilized soils. Soil Biol Biochem 80:70–78. https://doi.org/10.1016/j.soilbio.2014.09.028

    Article  CAS  Google Scholar 

  163. Oburger E, Gruber B, Wanek W et al (2016) Microbial decomposition of 13C-labeled phytosiderophores in the rhizosphere of wheat: mineralization dynamics and key microbial groups involved. Soil Biol Biochem 98:196–207. https://doi.org/10.1016/j.soilbio.2016.04.014

    Article  CAS  Google Scholar 

  164. Eichorst SA, Kuske CR (2012) Identification of cellulose-responsive bacterial and fungal communities in geographically and edaphically different soils by using stable isotope probing. Appl Environ Microbiol 78:2316–2327. https://doi.org/10.1128/AEM.07313-11

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  165. Štursová M, Žifčáková L, Leigh MB et al (2012) Cellulose utilization in forest litter and soil: identification of bacterial and fungal decomposers. FEMS Microbiol Ecol 80:735–746. https://doi.org/10.1111/j.1574-6941.2012.01343.x

    Article  CAS  PubMed  Google Scholar 

  166. Lueders T, Manefield M, Friedrich MW (2004) Enhanced sensitivity of DNA- and rRNA-based stable isotope probing by fractionation and quantitative analysis of isopycnic centrifugation gradients. Environ Microbiol 6:73–78. https://doi.org/10.1046/j.1462-2920.2003.00536.x

    Article  CAS  PubMed  Google Scholar 

Download references

Funding

This research, part of the Project N° FP01 Microbiome, was funded by OCP Group under the UM6P—RRs—Cranfield Uni. SAFA Program granted to MHT (RRs), BA (UM6P), and HJ (CU). The authors wish to express their appreciation for funding the Postdoctoral position for Ndour PMS. Rothamsted Research also acknowledges S2N – Soil to nutrition – Work package 1 – Optimizing nutrient flows and pools in the soil-plant-biota system” (BBS/E/C/000I0310) and “Growing Health” (BB/X010953/1) Institute Strategic Programmes.

Author information

Authors and Affiliations

  1. College for Sustainable Agriculture and Environmental Sciences, AgroBioSciences, Mohammed VI Polytechnic University, Ben Guerir, Morocco

    Papa Mamadou Sitor Ndour, Adnane Bargaz & Karim Lyamlouli

  2. Cranfield Soil and AgriFood Institute, School of Applied Sciences, Cranfield University, Cranfield, MK43 0AL, UK

    Papa Mamadou Sitor Ndour, Mark Pawlett & Jim Harris

  3. Institute of Biological Sciences (ISSB), Faculty of Medical Sciences, Mohammed VI Polytechnic University, Ben Guerir, Morocco

    Zineb Rchiad

  4. Sustainable Agriculture Sciences, Rothamsted Research, Harpenden, Hertfordshire, UK

    Ian M. Clark & Tim H. Mauchline

Authors
  1. Papa Mamadou Sitor Ndour
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Adnane Bargaz
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Zineb Rchiad
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Mark Pawlett
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Ian M. Clark
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Tim H. Mauchline
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Jim Harris
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Karim Lyamlouli
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

Papa Mamadou Sitor Ndour, Adnane Bargaz, and Karim Lyamlouli conceptualized the paper; Papa Mamadou Sitor Ndour and Adnane Bargaz wrote the original draft. All authors contributed to the editing, review, and validation of the manuscript.

Corresponding author

Correspondence to Papa Mamadou Sitor Ndour.

Ethics declarations

Competing Interests

The authors declare no competing interests.

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Ndour, P.M.S., Bargaz, A., Rchiad, Z. et al. Microbial Catabolic Activity: Methods, Pertinence, and Potential Interest for Improving Microbial Inoculant Efficiency. Microb Ecol 86, 2211–2230 (2023). https://doi.org/10.1007/s00248-023-02250-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00248-023-02250-6

Keywords

Search

Navigation