PLANT BIOLOGY
ANIMAL BIOLOGY
SUBSCRIPTION
E-SUBSCRIPTION
 
MAP
MAIN PAGE

 

 

 

 

Kamalova A.R., Danilova N.V., Kuryntseva P.A., Galitskaya P.Yu., Selivanovskaya S.Yu. Technical hemp Cannabis sativa L. growth and functional diversity of soil microbiota in a model cultivation under elevated air temperatures. Sel'skokhozyaistvennaya Biologiya [Agricultural Biology], 2025, Vol. 60, № 1, p. 110-124.
(how to cite this article)

doi: 10.15389/agrobiology.2025.1.110eng

UDC: 633.522:581.1:631.46

Acknowledgements:
Funded by the subsidy allocated to Kazan Federal University for the state assignment in the sphere of scientific activities, project № FZSM-2022-0003

 

TECHNICAL HEMP Cannabis sativa L. GROWTH AND FUNCTIONAL DIVERSITY OF SOIL MICROBIOTA IN A MODEL CULTIVATION UNDER ELEVATED AIR TEMPERATURES

A.R. Kamalova✉, N.V. Danilova, P.A. Kuryntseva,
P.Yu. Galitskaya, S.Yu. Selivanovskaya

Department of Applied Ecology, Institute of environmental sciences, Kazan (Volga region) Federal University, 18, Kremlevskaja, Kazan, 420008 Russia, e-mail akhtjamovaalina07@gmail.com (✉ corresponding author) natasha-danilova91@mail.ru, polinazwerewa@yandex.ru, gpolina33@yandex.ru, Svetlana.Selivanovskaya@kpfu.ru

Kamalova A.R. orcid.org/0000-0002-7857-8756
Galitskaya P.Yu. orcid.org/0000-0002-5070-786X
Danilova N.V. orcid.org/0000-0001-8750-0929
Selivanovskaya S.Yu. orcid.org/0000-0001-6379-7166
Kuryntseva P.A. orcid.org/0000-0002-9274-7077

Final revision received April 15, 2024
Accepted June 01, 2024

Global climate change on Earth and the resulting ecological, economic, and social risks are linked to the accumulation of greenhouse gases in the atmosphere, particularly CO2. The use of CO2 super-absorbing plants is considered an effective method for reducing (sequestering) CO2 levels in the air, with technical hemp (Cannabis sativa L.) recently attracting significant attention. This crop is characterized by rapid growth, resilience to environmental factors, low cultivation costs, and versatile biomass use as raw material for various industries. Currently, there are no programs or regulations in Russia for using technical hemp to sequester atmospheric CO2. When developing such programs, it is essential to consider the ability of plants to alter the composition and functional activity of soil microbiota, which can, in turn, affect plant growth rates, soil fertility indicators, and CO2 emissions from the soil cover. Additionally, it is important to determine whether the high efficiency of CO2 sequestration in the plant-soil-microorganism ecosystem will persist under global temperature increases and how soil conditions and its microbial components will change. To address these objectives, we conducted a model experiment in a greenhouse setting to evaluate the impact of temperatures (15 °С is typical for the growing season in central Russia; 20 °С and 30 °С are elevated temperatures) on the growth of technical hemp and chlorophyll content, carbon accumulation in the soil beneath plants, biodiversity, and functional activity of soil microbiota. This included assessing microorganisms' ability to decompose carbon-containing substrates using Biolog EcoPlates™. All measurements, except for soil carbon content, morphometric characteristics of hemp plants, and chlorophyll content, were carried out dynamically on 7th, 28th, 56th, and 98th days (average duration of the growing season in central Russia). Soil carbon content was determined on 1st and 98thdays; chlorophyll content on 28th, 56th, and 98th days; and morphometric measurements were made on 98th day (end of the experiment). The research was conducted from March 14 to June 19 in a greenhouse at Kazan Federal University in 2023. The results showed that technical hemp exhibited maximum growth for both aboveground and underground parts at 30 °С, with plant height reaching 64.57 cm and root length 25.27 cm. In comparison to 20 °С where minimum values were observed (36.70 cm and 14.36 cm, respectively) growth at 30 °С was 76 % higher (p < 0.05). Chlorophyll content in hemp leaves varied with time and temperature; significant differences in chlorophyll content (p < 0.05) were found on 28th day for all temperatures, with maximum values observed only on 56th day of the experiment. By the end of the experiment, chlorophyll levels decreased across all variants without statistically significant differences (p > 0.05). At the same temperature, samples with soil without hemp did not significantly differ from those with hemp concerning soil microbial biomass: at 15 °С, values were respectively 0.92-0.64 mg/kg and 0.96-0.62 mg/kg; at 20 °С 1.92-0.84 mg/kg and 1.74-1.03 mg/kg; at 30 °С 3.58-2.06 mg/kg and 3.08-2.24 mg/kg (p > 0.05). Increased temperatures led to higher microbial biomass both in the absence and presence of plants (3.58 mg/kg and 3.08 mg/kg on 7th day, respectively; p < 0.05). Functional activity of microorganisms was assessed based on average consumption of 31 substrates (AWCD, average well-color development) on 28th day for samples without plants (0.49; 0.66; 0.54) and with plants (0.29; 0.64; 0.30), as well as on 98th day for samples without plants (0.13; 0.36; 0.14) and with plants (0.55; 1.17; 0.54), which did not show significant differences (p > 0.05). However, on 7th day an increase in microbial activity was noted in samples with plants, especially at temperatures of 20 °С and 30 °С (1.23; 0.89; p < 0.05). Similar patterns on 7th day were established when assessing the alpha diversity (Shannon index) of soil microbial communities: the highest diversity was noted at 15 °С, 20 °С, and 30 °С both in samples without plants (2.31; 1.90; and 1.60) and with plants (2.58; 2.46; and 2.32; p < 0.05). The most sought-after carbon-containing substrate for the microbial communities (SWCD, substrate well-color development) in control samples was D-xylulose, particularly at 20 °С (1.89-3.53; p < 0.05), with its consumption increasing throughout the experiment. The results of comparison of beta diversity of the soil bacterial community (based on SWCD) using the NMDS (non-metric multidimensional scaling) method showed no differences between soils (without and with plants) incubated at different temperatures and sampled on the 7th and 28th days. Samples incubated under plants at all three temperatures on 98th day formed a separate group, indicating greater uniformity in microbial communities. The contents of total organic carbon (TOC) and soil organic carbon (SOC) in the soil remained within error margins and did not depend on the presence of plants or temperature (p > 0.05). Thus, it has been shown that in hemp, with an increase in temperature during the growing season, the length of the above-ground and underground parts of the plant increases, which leads to an increase in the efficiency of atmospheric carbon sequestration. The amount of microbial biomass in the soil changes, and the metabolic activity of microorganisms increases already on the 7th day of the experiment. The presented model system can be used to assess the efficiency of sequestration and the state of functional groups of the soil microbial community when developing programs for growing industrial hemp (C. sativa L.) as a superabsorbent plant, including at elevated temperatures, when it is important to maintain the diversity of soil microbial community.

Keywords: sequestration, carbon superabsorbent plants, microbial biomass, technical hemp, carbon substrates, microbial functional activity.

 

REFERENCES

  1. Abbass K., Qasim M.Z., Song H., Murshed M., Mahmood H., Younis I. A review of the global climate change impacts, adaptation, and sustainable mitigation measures. Environmental Science and Pollution Research, 2022, 29(28): 42539‑42559 CrossRef
  2. Han J., Tan Z., Chen M., Zhao L., Yang L., Chen S. Carbon footprint research based on input–output model — a global scientometric visualization analysis. International Journal of Environmental Research and Public Health, 2022, 19(18): 11343 CrossRef
  3. Stips A., MacIas D., Coughlan C., Garcia-Gorriz E., Liang X.S. On the causal structure between CO2 and global temperature. Scientific Reports, 2016, 6: 21691 CrossRef
  4. Devi A.S., Singh K.S. Carbon storage and sequestration potential in aboveground biomass of bamboos in North East India. Scientific Reports, 2021, 11(1): 837 CrossRef
  5. McCalmont J.P., Hastings A., McNamara N.P., Richter G.M., Robson P., Donnison I.S., Clifton-Brown J. Environmental costs and benefits of growing Miscanthus for bioenergy in the UK. GCB Bioenergy, 2017, 9(3): 489-507 CrossRef
  6. Bai J., Luo L., Li A., Lai X., Zhang X., Yu Y., Wang H., Wu N., Zhang L. Effects of biofuel crop switchgrass (Ranicum virgatum) cultivation on soil carbon sequestration and greenhouse gas emissions: a review. Life, 2022, 12: 2105 CrossRef
  7. Hourfane S., Mechqoq H., Bekkali A.Y., Rocha J.M., El Aouad N. A comprehensive review on Cannabis sativa ethnobotany, phytochemistry, molecular docking and biological activities. Plants, 2023, 12(6): 1245 CrossRef
  8. Shen Z., Tiruta-Barna L., Hamelin L. From hemp grown on carbon-vulnerable lands to long-lasting bio-based products: Uncovering trade-offs between overall environmental impacts, sequestration in soil, and dynamic influences on global temperature. Science of the Total Environment, 2022, 846: 157331 CrossRef
  9. Parvez A.M., Lewis J.D., Afzal M.T. Potential of industrial hemp (Cannabis sativa L.) for bioenergy production in Canada: status, challenges and outlook. Renewable and Sustainable Energy Reviews, 2021, 141: 110784 CrossRef
  10. Ahmed A.T.M.F., Islam M.Z., Mahmud M.S., Sarker M.E., Islam M.R. Hemp as a potential raw material toward a sustainable world: A review. Heliyon, 2022, 8(1): e08753 CrossRef
  11. Rehman M., Fahad S., Du G., Cheng X., Yang Y., Tang K., Liu L., Liu F.H., Deng G. Evaluation of hemp (Cannabis sativa L.) as an industrial crop: a review. Environmental Science and Pollution Research, 2021, 28(13): 1-12 CrossRef
  12. Madden S.M., Ryan A., Walsh P. A systems thinking approach investigating the estimated environmental and economic benefits and limitations of industrial hemp cultivation in Ireland from 2017-2021. Sustainability (Switzerland), 2022, 14: 4159 CrossRef
  13. Scalabrin E., Radaelli M., Capodaglio G., Pierobon M., Vecchio S. Del, Buffa G. Hemp cultivation opportunities for marginal lands development. PLoS ONE, 2024, 19(3): e0299981 CrossRef
  14. Rivas-Aybar D., John M., Biswas W. Environmental life cycle assessment of a novel hemp-based building material. Materials, 2023, 16: 7208 CrossRef
  15. Schluttenhofer C., Yuan L. Challenges towards revitalizing hemp: a multifaceted crop. Trends in Plant Science, 2017, 22(11): 917-929 CrossRef
  16. Odieka A.E., Obuzor G.U., Oyedeji A.O., Gondwe M., Hosu Y.S. The medicinal natural products of Cannabis sativa Linn.: a review. Molecules Journal, 2022, 27(5): 1689 CrossRef
  17. Cerino P., Buonerba C., Cannazza G., D’Auria J., Ottoni E., Fulgione A., Di Stasio A., Pierri B., Gallo A. A review of hemp as food and nutritional supplement. Cannabis and cannabinoid research, 2021, 6(1): 19-27 CrossRef
  18. Crini G., Lichtfouse E., Chanet G., Morin-Crini N. Applications of hemp in textiles, paper industry, insulation and building materials, horticulture, animal nutrition, food and beverages, nutraceuticals, cosmetics and hygiene, medicine, agrochemistry, energy production and environment: a review. Environmental Chemistry Letters, 2020, 18(5): 1451-1476 CrossRef
  19. Vosper J. The role of industrial hemp in carbon farming. GoodEarth Resources PTY LTD, 2011: 1‑6.
  20. Krasutskiy B.V. Vestnik Tyumenskogo gosudarstvennogo universiteta, 2018, 4(3): 57-68 CrossRef (in Russ.).
  21. Heinze J., Gensch S., Weber E., Joshi J. Soil temperature modifies effects of soil biota on plant growth. Journal of Plant Ecology, 2016, 1-14 CrossRef
  22. Nishar A., Bader M.K.F., O’Gorman E.J., Deng J., Breen B., Leuzinger S. Temperature effects on biomass and regeneration of vegetation in a geothermal area. Frontiers in Plant Science, 2017, 8: 249 CrossRef
  23. Luo Y., Sherry R., Zhou X., Wan S. Terrestrial carbon-cycle feedback to climate warming: experimental evidence on plant regulation and impacts of biofuel feedstock harvest. GCB Bioenergy, 2009, 1(1): 62-74 CrossRef
  24. Nazir N., Kamili A.N., Zargar M.Y., Khan I., Shah D., Parray J.A., Tyub S. Effect of root exudates on rhizosphere soil microbial communities. Journal of Research & Development, 2016, 16: 88‑95.
  25. Berendsen R.L., Pieterse C.M.J., Bakker P.A.H.M. The rhizosphere microbiome and plant health. Trends in Plant Science, 2012, 17(8): 478-486 CrossRef
  26. Mendes R., Garbeva P., Raaijmakers J.M. The rhizosphere microbiome: Significance of plant beneficial, plant pathogenic, and human pathogenic microorganisms. FEMS Microbiology Reviews, 2013, 37(5): 634‑63 CrossRef
  27. Sanon A., Andrianjaka Z.N., Prin Y., Bally R., Thioulouse J., Comte G., Duponnois R. Rhizosphere microbiota interfers with plant-plant interactions. Plant and Soil, 2009, 321: 259-278 CrossRef
  28. Chiaramonte J.B., Mendes L.W., Mendes R. Rhizosphere microbiome and soil-borne diseases In: Rhizosphere biology: interactions between microbes and plants. V.V.S.R. Gupta, A.K. Sharma (eds.). Uttarakhand, India, 2021: 155-168 CrossRef
  29. Li Y.Z., Bao X.L., Tang S.X., Xiao K.Q., Ge C.J., Xie H.T., He H.B., Mueller C.W., Liang C. Toward soil carbon storage: the influence of parent material and vegetation on profile-scale microbial community structure and necromass accumulation. Soil Biology and Biochemistry, 2024, 193: 109399 CrossRef
  30. Garcia Arredondo M., Fang Y., Jones M., Yabusaki S., Cardon Z., Keiluweit M. Resolving dynamic mineral-organic interactions in the rhizosphere by combining in-situ microsensors with plant-soil reactive transport modeling. Soil Biology and Biochemistry, 2023, 184: 109097 CrossRef
  31. Kuht J., Eremeev V., Talgre L., Loit E., Mäeorg E., Margus K., Runno-Paurson E., Madsen H., Luik A. Soil microbial activity in different cropping systems under long-term crop rotation. Agriculture (Switzerland), 2022, 12(4): 532 CrossRef
  32. Odlare M., Arthurson V., Pell M., Svensson K., Nehrenheim E., Abubaker J. Land application of organic waste — effects on the soil ecosystem. Applied Energy, 2011, 88(6): 2210‑2218 CrossRef
  33. Odlare M., Pell M., Svensson K. Changes in soil chemical and microbiological properties during 4 years of application of various organic residues. Waste Management, 2008, 28(7): 1246-1253 CrossRef
  34. Lugtenberg B. Principles of plant-microbe interactions: microbes for sustainable agriculture. Leiden, The Netherlands, 2015.
  35. Wutzler T., Reichstein M. Priming and substrate quality interactions in soil organic matter models. Biogeosciences, 2013, 10(3): 2089-2103 CrossRef
  36. Pantigoso H.A., Newberger D., Vivanco J.M. The rhizosphere microbiome: Plant—microbial interactions for resource acquisition. Journal of Applied Microbiology, 2022, 133(5): 2864-2876 CrossRef
  37. Shree B., Jayakrishnan U., Bhushan S. Impact of key parameters involved with plant-microbe interaction in context to global climate change. Frontiers in Microbiology, 2022, 13: 1008451 CrossRef
  38. Fang K., Kou Y.P., Tang N., Liu J., Zhang X.Y., He H.L., Xia R.X., Zhao W.Q., Li D.D., Liu Q. Differential responses of soil bacteria, fungi and protists to root exudates and temperature. Microbiological Research, 2024, 286: 127829 CrossRef
  39. GOST ISO 10694:2024 Kachestvo pochvy. Opredelenie soderzhaniya organicheskogo i obshchego ugleroda posle sukhogo szhiganiya (elementnyy analiz) [GOST ISO 10694:2024 Soil quality. Determination of organic and total carbon content after dry combustion (elemental analysis)]. Moscow, 2024 (in Russ.).
  40. Sun Z. C., Li G. T., Zhang C. L., Wang Z. M., Lin Q. M., Zhao X-R. Contrasting resilience of soil microbial biomass, microbial diversity and ammonification enzymes under three applied soil fumigants. Journal of Integrative Agriculture, 2020, 19(10): 2561-2570 CrossRef
  41. ISO 14240-1:1997 Soil quality — Determination of soil microbial biomass. Part 1: Substrate-induced respiration method.
  42. Rutgers M., Wouterse M., Drost S.M., Breure A.M., Mulder C., Stone D., Creamer R.E., Winding A., Bloem J. Monitoring soil bacteria with community-level physiological profiles using BiologTM ECO-plates in the Netherlands and Europe. Applied Soil Ecology, 2016, 97: 23-35 CrossRef
  43. Zak J., Willig M., Moorhead D., Wildman H. Functional diversity of microbial communities: A quantitative approach. Soil Biology and Biochemistry, 1994, 26(9): 1101‑1108 CrossRef
  44. Cheng C., Zhao D., Lv D., Shuang L., Du G. Comparative study on microbial community structure across orchard soil, cropland soil, and unused soil. Soil and Water Research, 2017, 12(4): 237-245 CrossRef
  45. Gomez E., Ferreras L., Toresani S. Soil bacterial functional diversity as influenced by organic amendment application. Bioresource Technology, 2006, 97: 1484-1489 CrossRef
  46. McCune B., Grace J.B., Urban D.L. Analysis of ecological communities. MjM Software Design, Oregon, 2002.
  47. Kruskel J.B., Wish M. Multidimensional scaling and other structure search methods. Sage, 1978.
  48. Islamgulov D.R., Bikbaeva G.G. Biologicheskie osobennosti konopli posevnoy. Rossiyskiy elektronnyy nauchnyy zhurnal,2021,3(41): 48-56 CrossRef (in Russ.).
  49. Baker N.R. Chlorophyll fluorescence: A probe of photosynthesis in vivo. Annual Review of Plant Biology, 2008, 59: 89-113 CrossRef
  50. Shi W., Gao D., Zhang Z., Wang H., Hagedorn F., Ding J., Zhao C. Exploring global data sets to detect changes in soil microbial carbon and nitrogen over three decades. Earth's Future, 2024, 12: e2024EF004733 CrossRef
  51. Schmidt M.W.I., Reichstein M., Carvalhais N., Ciais P., Jiang L., Viatkin K., Vargas R., Yigini Y., Omuto C., Malik A.A. Microbial carbon use efficiency promotes global soil carbon storage. Nature, 2023, 618(7967): 1-5 CrossRef
  52. Prikhod’ko V.E., Sizemskaya M.L. Pochvovedenie, 2015, 8: 974-983 CrossRef (in Russ.).
  53. Sushko S.V., Anan’eva N.D., Ivashchenko K.V., Vasenev V.I., Sarzhanov D.A. Agrofizika, 2016, 4: 17‑23 (in Russ.).
  54. Muraškienė M., Aleinikovienė J., Skuodienė R., Tomchuk D., Armolaitis K. Soil respiration and microbial biomass peculiarities as influenced by different land use intensity. Zemdirbyste, 2020, 107(1): 3-10 CrossRef
  55. De Deyn G.B., Cornelissen J.H.C., Bardgett R.D. Plant functional traits and soil carbon sequestration in contrasting biomes. Ecology Letters, 2008, 11(5): 516-531 CrossRef
  56. Blagodatskaya E.V., Semenov M.V. Aktivnost’ i biomassa pochvennykh mikroorganizmov v izmenyayushchikhsya usloviyakh okruzhayushchey sredy [Activity and biomass of soil microorganisms under changing environmental conditions]. Moscow, 2016 (in Russ.).
  57. Dornbush M.E. Grasses, litter, and their interaction affect microbial biomass and soil enzyme activity. Soil Biology and Biochemistry, 2007, 39(9): 2241-2249 CrossRef
  58. Ajayi O.O., Dianda M. Plants and their microbes. In: Symbiosis in nature. E. Rigobelo (ed.). IntechOpen, London, UK, 2023 CrossRef
  59. Chauhan P., Sharma N., Tapwal A., Kumar A., Verma G.S., Meena M., Seth C.S., Swapnil P. Soil microbiome: diversity, benefits and interactions with plants. Sustainability (Switzerland), 2023, 15: 14643 CrossRef
  60. Yadav R. H. Soil-plant-microbial interactions for soil fertility management and sustainable agriculture. Microbes in Land Use Change Management, 2021, 341-362 CrossRef
  61. Xue R., Shen Y., Marschner P. Soil water content during and after plant growth influence nutrient availability and microbial biomass. Journal of Soil Science and Plant Nutrition, 2017, 17(3): 702-715 CrossRef
  62. Rabary B., Sall S., Letourmy P., Husson O., Ralambofetra E., Moussa N., Chotte J.L. Effects of living mulches or residue amendments on soil microbial properties in direct seeded cropping systems of Madagascar. Applied Soil Ecology, 2008, 39(2): 236‑243 CrossRef
  63. Liu B., Li Y., Zhang X., Wang J., Gao M. Effects of chlortetracycline on soil microbial communities: Comparisons of enzyme activities to the functional diversity via Biolog EcoPlatesTM. European Journal of Soil Biology, 2015, 68: 69-76 CrossRef
  64. Garland J.L., Mills A.L. Classification and characterization of heterotrophic microbial communities on the basis of patterns of community-level sole-carbon-source utilization. Applied and Environmental Microbiology, 1991, 57(8): 2351-2359 CrossRef
  65. Rutgers M., Wouterse M., Drost S.M., Breure A.M., Mulder C., Stone D., Creamer R.E., Winding A., Bloem J. Monitoring soil bacteria with community-level physiological profiles using BiologTM ECO-plates in the Netherlands and Europe. Applied Soil Ecology, 2016, 97: 23-35 CrossRef
  66. Bengtson P., Barker J., Grayston S.J. Evidence of a strong coupling between root exudation, C and N availability, and stimulated SOM decomposition caused by rhizosphere priming effects. Ecology and Evolution,2012, 2(8): 1843-1852 CrossRef
  67. Yin H., Li Y., Xiao J., Xu Z., Cheng X., Liu Q. Enhanced root exudation stimulates soil nitrogen transformations in a subalpine coniferous forest under experimental warming. Global Change Biology, 2013, 19(7): 2158-2167 CrossRef
  68. Fahad S., Hasanuzzaman M., Alam M., Ullah H., Saeed M., Ali I., Muhammad K. Plant-microbes interactions and functions in changing climate In: Environment, climate, plant and vegetation growth. S. Fahad et al. (eds.). Springer, 2020: 397-419 CrossRef
  69. Tyagi S., Plants A., Singh R. Effect of climate change on plant-microbe interaction: an overview. European Journal of Molecular Biotechnology, 2014, 5(3): 149-156 CrossRef
  70. Markovskaya G.K., Chugunova O.A. Izvestiya Samarskoy gosudarstvennoy sel’skokhozyaystvennoy akademii, 2008, 3(4): 22-27 (in Russ.).
  71. Galieva G.Sh., Galitskaya P.Yu., Selivanovskaya S.Yu. Uchenye zapiski Kazanskogo universiteta, 2023, 165(2): 231-262 CrossRef (in Russ.).
  72. Tardy V., Mathieu O., Lévêque J., Terrat S., Chabbi A., Lemanceau P., Ranjard L., Maron P.A. Stability of soil microbial structure and activity depends on microbial diversity. Environmental Microbiology Reports, 2014, 6(2): 173-183 CrossRef
  73. Shilova A.V. Filogeneticheskoe raznoobrazie i gidroliticheskiy potentsial bakterial’nogo soobshchestva sodovogo shlamokhranilishcha. Avtoreferat kandidatskoy dissertatsii [Phylogenetic diversity and hydrolytic potential of the bacterial community of a soda sludge storage facility. PhD Thesis]. Perm’, 2021 (in Russ.).

 

back

 


CONTENTS

 

Full article PDF (Rus)

Supplement