Evaluation of the long-term effects of the permanent cropping on soil microbial communities

The study of soil microbial communities under different agricultural crops (flax, clover, barley, potato, winter rye) grown in permanent cropping and crop rotation was carried out. The effect of permanent cropping and crop rotation on the taxonomic profile of the prokaryotic and fungal components of the soil microbiome was studied. The effect of permanent cropping and crop rotation on the metabolic intensity and stability of soil biota in the absence of mineral and organic fertilisers was assessed. The subject of the research was the long-term experience established in 1912 by Professor A.G. Doyarenko at the Russian State Agrarian University – Moscow Timiryazev Agricultural Academy, founded in 1912 by Professor A.G. Doyarenko. It was shown that the highest OUT (operational taxonomic units) values for fungi were found in soils under fallow and crop rotation. For prokaryotes, however, the crop rotation variant had the lowest number of OTUs. Ascomycetes were found to be the dominant fungal taxon in all samples studied. Prokaryotes were dominated by Proteobacteria and Acidobacteriota, followed by Actinobacteriota and Firmicutes, and Chloroflexi were represented to a lesser extent. Among the archaea, the Crenarcheota phylum was dominant. It was shown that continuous cultivation of crops generally has a negative effect on the functioning of the microbial community. With an optimal metabolic coefficient of 0.2 in monoculture, they reached 0.6. The sustainability of the soil microbial community is reduced by the continuous cultivation of potatoes, flax and clover without organic and mineral fertilizers, as well as by the “perpetual fallow” option. Particularly unfavorable conditions were found in potato monoculture. Continuous cultivation of cereals, especially winter rye, does not lead to a significant decrease in the activity of soil biota and the stability of soil microbial communities. Crop rotation makes it possible to optimize microbiological processes in the soil and to increase the stability of the soil microbial community.

1. Grodzinskiy A.M. Plant allelopathy and soil fatigue: selectas. Ed. by V.D. Romanenko (chief editor) et al. Academy of Sciences of the Ukrainian SSR. Central Republican Botanical Garden. Kiev, Ukrain: Nauk. dumka, 1991:432. (In Russ.)

2. Anan’eva N.D. Microbiological aspects of self-purification and soil stability. Moscow, Russia: Nauka, 2003:223. (Iin Russ.)

3. Antonov A.A., Baranova E.N., Gulevich A.A., Kurenina L.V. et al. Modified composition of microbial community in the rhizosphere of transgenic tomato plants with a glycine betaine syntesis gene. Izvestiya of Timiryazev Agricultural Academy (TAA). 2020;(5):18–29. (In Russ.)

4. Blagodatskaya E.V., Anan’eva N.D. Assessment of the resistance of soil microbial communities to pollutants. Eurasian Soil Science. 1996;11:1341–1346. (In Russ.)

5. Vorob’eva L.I. Archaea. Moscow, Russia: Akademkniga, 2007:447. (In Russ.)

6. Dobrovolskiy G.V. Ecological role of soil in the biosphere and in human life. Doklady po ekologicheskomu pochvovedeniyu. 2007;2(6):1–16. (In Russ.)

7. Dospehov B.A., Kiryushin B.D. Soil fertility in conditions of crop rotation and permanent crops. S. kh. za rubezhom. 1979;11:2–7. (In Russ.)

8. Dumova V.A., Pershina E.V., Merzlyakova Ya.V., Kruglov Yu.V., Andronov E.E. The main trends in dynamics of soil microbiom during a long-term field experiment as indicated by high throughput sequencing 16S-rRNA gene libraries. Agricultural Biology. 2013;48(5):85–92. (In Russ.)

9. Corvigo I.O., Pershina E.V., Ivanova E.A., Chirak E.L. et al. Effect of long-term application of agrotechnical techniques and crops on soil microbial communities. Microbiology. 2016;85(2):199–210. (In Russ.)

10. Krasilnikov A.K. Soil microorganisms and higher plants. Moscow, USSR: Publishing House of the USSR Academy of Sciences, 1958:466. (In Russ.)

11. Rogovaia S.V., Elsukova E.Yu., Ananyeva N.D. Soil microbial component and its respiratory activity in coniferous forests of the Northwest Priladozhje area. Vestnik of Saint Petersburg University. Earth Sciences. 2016;3:129–137. (In Russ.)

12. Sorokin N.D. Microbiological monitoring of disturbed ground ecosystems of Siberia. Proceedings of the Russian Academy of Sciences. Biological Series. 2009;6:728–733. (In Russ.)

13. Sushko S.V., Anan’eva N.D., Ivashchenko K.V., Kudeyarov V.N. CO2 emission, microbial biomass and basal respiration of chernozem under different land uses. Eurasian Soil Science. 2019;9:1081–1091. (In Russ.)

14. Terekhova V.A., Prudnikova E.V., Kulachkova S.A., Gorlenko M.V. et al. Microbiological indicators of heavy metals and carbon-containing preparations to agrosoddy-podzolic soils differing in humus content. Eurasian Soil Science. 2021;3:372–384. (In Russ.)

15. Chernov T.I., Tkhakakhova A.K., Lebedeva M.P., Zhelezova A.D. et al. Microbiomes of the soils of solonetzic complex with contrasting salinization on the Volga–Ural interfluve. Eurasian Soil Science. 2018;9:1115–1124. (In Russ.)

16. Chirak E.L., Pershina E.V., Dol’nik A.S., Kutovaya O.V. et al. Taxonomic structure of microbial association indifferent soils investigated by high-throughputsequencing of 16S-rRNA gene library. Agricultural Biology. 2013;48(3):100–109. (In Russ.)

17. Shumilova L.P., Kuimova N.G. The study of microbial association in city soils by the gas chromatography-mass spectrometry method. Bulletin Physiology and Pathology of Respiration. 2013;(50):121–125. (In Russ.)

18. Alvarez R., Alvarez C.R., Lorenzo G. Carbon dioxide fluxes following tillage from a mollisol in the Argentine Rolling Pampa. Eur. J. Soil Biol. 2001;37:161–166. https://doi.org/10.1016/S1164-5563(01)01085-8

19. Balvanera P., Pfisterer A.B., Buchmann N., He J.S. et al. Quantifying the evidence for biodiversity effects on ecosystem functioning and services. Ecology Letters. 2006;9(10):1146–1156.

20. Bay G., Lee C., Chen C., Mahal N.K. et al. Agricultural management affects the active rhizosphere bacterial community composition and nitrification. Msystems. 2021;6(5): e00651–21. https://doi.org/10.1128/mSystems.00651-21

21. Bonfante P., Venice F. Mucoromycota: going to the roots of plant-interacting fungi. Biology Reviews. 2020;34(2):100–113.

22. Challacombe J.F., Hesse C.N., Bramer L.M., McCue L.A. et al. Genomes and secretomes of Ascomycota fungi reveal diverse functions in plant biomass decomposition and pathogenesis. BMC Genomics. 2019;20(1):1–27.

23. Delgado-Baquerizo M. Microbial diversity drives multifunctionality in terrestrial ecosystems. Nature Communications. 2016;7(1):10541.

24. Edgar R.C. Search and clustering orders of magnitude faster than BLAST. Bioinformatics. 2010;26(19):2460–2461.

25. Egidi E., Delgado-Baquerizo M., Plett J.M., Wang J. et al. A few Ascomycota taxa dominate soil fungal communities worldwide. Nature Communications. 2019;10(1):2369.

26. Frąc M., Hannula S.E., Bełka M., Jędryczka M. Fungal biodiversity and their role in soil health. Front. Microbial. 2018;9:707. https://doi.org/10.3389/fmicb.2018.00707

27. Frey B., Rime T., Phillips M., Stierli B. et al. Microbial diversity in European alpine permafrost and active layers. FEMS Microbiology Ecology. 2016;92(3): fiw018.

28. Graham E.B., Knelman J.E., Schindlbacher A., Siciliano S. et al. Microbes as Engines of Ecosystem Function: When Does Community Structure Enhance Predictions of Ecosystem Processes? Front. Microbiol., 24 February 2016: Sec. Terrestrial Microbiology. 2016;7:214. https://doi.org/10.3389/fmicb.2016.00214

29. Hartmann A., Schmid M., Van D. Tuinen, Berg G. Plant-driven selection of microbes. Plant and Soil. 2009;321:235–257

30. Hawksworth D.L., Lücking R. Fungal diversity revisited: 2.2 to 3.8 million species. Microbiology Spectrum. 2017;5(4):10–1128.

31. Klaubauf S., Inselsbacher E., Zechmeister-Boltenstern S., Wanek W. et al. Molecular diversity of fungal communities in agricultural soils from lower Austria. Fungal Div. 2010;44:65–75. https://doi.org/10.1007/s13225-010-0053-1

32. Ling N., Wang T., Kuzyakov Y. Rhizosphere bacteriome structure and funtions. Nature Communications. 2022;13(1):836.

33. Magoč T., Salzberg S.L. FLASH: fast length adjustment of short reads to improve genome assemblies. Bioinformatics. 2011;27(21):2957–2963.

34. Magurran A.E. Measuring biological diversity. Current Biology. 2021;31(19): R1174-R1177.

35. Marschner P., Yang C.H., Lieberei R., Crowley D.E. Soil and plant specific effects on bacterial community composition in the rhizosphere. Soil Biology and Biochemistry. 2001;33(11):1437–1445

36. Morgan J.A., Bending G.D., White P.J. Biological costs and benefits to plant–microbe interactions in the rhizosphere. Journal of Experimental Botany. 2005;56(417):1729–1739.

37. Navarro-Noya Y.E., Gómez-Acata S., Rojas-Valdez N. Relative impacts of tillage, residue management and crop-rotation on soil bacterial communities in a semi-arid agroecosystem. Soil Biology and Biochemistry. 2013;65:86–95.

38. Orrù L., Canfora L., Trinchera A., Migliore M. et al. How tillage and crop rotation change the distribution pattern of fungi. Frontiers in Microbiology. 2021:1469.

39. Prasad P.V., Bheemanahalli R., Jagadish S.K. Field crops and the fear of heat stress – opportunities, challenges and future directions. Field Crops Research. 2017;200:114–121.

40. Quesada-Moraga E., Garrido-Jurado I., González-Mas N., Yousef-Yousef M. Ecosystem services of entomopathogenic ascomycetes. Journal of Invertebrate Pathology. 2023;201:108015.

41. Reed H.E., Martiny J.B.H. Testing the functional significance of microbial composition in natural communities. FEMS Microbiology Ecology. 2007;62(2):161–170.

42. Ritz K., Black H.I.J., Campbell C.D., Harris J.A., Wood C. Selecting biological indicators for monitoring soils: A framework for balancing scientific and technical opinion to assist policy development. Ecological Indicators. 2009;9:1212–1221. https://doi.org/10.1016/j.ecolind.2009.02.009

43. Servin J.A., Herbold C.W., Skophammer R.G., Lake J.A. Evidence excluding the root of the tree of life from the actinobacteria. Molecular Biology and Evolution. 2008;25(1):1–4.

44. Shu X., Zhang K., Zhang Q., Wang W. Changes in the composition of rhizosphere bacterial communities in response to soil types and acid rain. Journal of Environmental Management. 2023;325:116493.

45. Shuming Mo. Jinhui Li, Bin Li, Ran Yu et al. Impacts of Crenarchaeota and Halobacterota on sulfate reduction in the subtropical mangrove ecosystem as revealed by SMDB analysis. BioRxiv. 2020:08. https://doi.org/10.1101/2020.08.16.252635

46. Simon H.M., Jahn C.E., Bergerud L.T., Sliwinski M.K. et al. Cultivation of mesophilic soil crenarchaeotes in enrichment cultures from plant roots. Applied and Environmental Microbiology. 2005;71(8):4751–4760.

47. Sommermann L., Geistlinger J., Wibberg D., Deubel A. et al. Fungal community profiles in agricultural soils of a long-term field trial under different tillage, fertilization and crop rotation conditions analyzed by high-throughput ITS-amplicon sequencing. PLOS ONE. 2018;13(4): e0195345.

48. Stromberger М. Fire vs. Metal: A Laboratory Study Demonstrating Microbial Responses to Soil Disturbances. Journal of Natural Resources and Life Sciences Education. 2005;34(1):1–7. https://doi.org/10.2134/jnrlse.2005.0001

49. Tedersoo L., Smith M.E. Lineages of ectomycorrhizal fungi revisited: Foraging strategies and novel lineages revealed by sequences from belowground. Fungal Biology Reviews. 2013;27(3–4):83–99.

50. Tedersoo L., Mikryukov V., Anslan S., Bahram M. et al. The Global Soil Mycobiome consortium dataset for boosting fungal diversity research. Fungal Diversity. 2021;111:573–588. https://doi.org/10.1007/s13225-021-00493-7

51. Van Der Heijden M.G.A., Bardgett R.D., Van Straalen N.M. The unseen majority: soil microbes as drivers of plant diversity and productivity in terrestrial ecosystems. Ecology Letters. 2008;11(3):296–310.

52. Vancov T., Keen B. Amplification of soil fungal community DNA using the ITS86F and ITS4 primers. FEMS Microbiology Letters. 2009;296(1):91–96.

53. Vega F.E., Meyling N.V., Luangsa-ard J.J., Blackwell M. Fungal Entomopathogens. Insect Pathology (Second Edition). 2012:171–220.

54. Wang Q., Garrity G.M., Tiedje J.M., Cole J.R. Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Applied and Environmental Microbiology. 2007;73(16):5261–5267.

55. Zharkova E.K., Vankova A.A., Selitskaya O.V., Malankina E.L. et al. Bacterial communities of Lamiacea L. medical plants: structural features and rhizospyere effect. Microorganisms. 2023;11(1):197.