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Prokaryotic Community Structure in the Rapeseed (Brassica napus L.) Rhizosphere Depending on Addition of 1-Aminocyclopropane-1-Carboxylate-Utilizing Bacteria

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Abstract

The taxonomic structure of the microbiomes colonizing the rapeseed rhizosphere soil was investigated using high-throughput sequencing of the 16S rRNA gene amplicon libraries. Effect of introduction of bacteria with ACC deaminase activity into the rapeseed rhizosphere community on rapeseed yeild was studied. In the prokaryotic complex, Proteobacteria, Actinobacteria, Gemmatimonadetes, and Acidobacteria predominated. An inverse correlation was found between abundance of the taxa Crenarchaeota and Proteobacteria (r = ‒0.71, P < 0.01). All detected archaeal sequences belonged to the family Nitrososphaeraceae, which is directly involved in intensification of plant nitrogen nutrition. Independent of the mineral nutrition, addition of ACC-utilizing strain resulted in a significant decrease in the shares of Crenarchaeota (63‒72%), Verrucomicrobia (42‒53%), and Bacteroidetes (50‒56%) and an increase in the share of the Proteobacteria (38%). Introduced bacteria were shown to have a positive effect on the relative abundance of the metabolically significant Proteobacteria classes in the rapeseed rhizosphere due to improved condition of the plants. A reliable correlation was found between relative abundance of the Proteobacteria and production of the plant‒microbial system (r = 0.85, P < 0.01) on addition of the strains Pseudomonas oryzihabitans Ep4 and Variovorax paradoxus 3-P4, which possess an ACC deaminase complex. Observed differences in the composition of microbial populations were primarily associated with the effect of introduced strains, rather than with addition of mineral fertilizers.

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REFERENCES

  1. 1

    Ahmed, V., Verma, M.K., Gupta, S., Mandhan, V., and Chauhan, N.S., Metagenomic profiling of soil microbes to mine salt stress tolerance genes, Front. Microbiol., 2018, vol. 9, p. 159.

  2. 2

    Arinushkina, E.V., Rukovodstvo po khimicheskomu analizy pochv (Guidelines for the Chemical Analysis of Soils), Moscow: Mos. Gos. Univ., 1979.

  3. 3

    Bates, S.T., Berg-Lyons, D., Caporaso, J.G., Walters, W.A., Knight, R., and Fierer, N., Examining the global distribution of dominant archaeal populations in soil, ISME J., 2010, vol. 5, pp. 908–917.

  4. 4

    Belimov, A.A. and Safronov, V.I., ACC diaminase and plant-microbial interactions, Sel’skokhoz. Biol., 2011, no. 3, pp. 23‒27.

  5. 5

    Belimov, A.A., Dodd, I.C., and Safronova, V.I., ACC deaminase-containing rhizobacteria improve vegetative development and yield of potato plants grown under water-limited conditions, Aspects Appl. Biol., 2009, vol. 98, pp. 163‒169.

  6. 6

    Beregovaya, Yu.V., Tychinskaya, I.L., Petrova, S.N., Parakhin, N.V., Pukhal’skii, Yu.V., Makarova, N.M., Shaposhnikov, A.I., and Belimov, A.I., Variety-dependent specificity of the effect of rhizobacteria on nitrogen fixation symbiosis and mineral nutrition of soybeans in an agrocenosis, Sel’skokhoz.Biol., 2018, vol. 53, no. 5, pp. 977‒993.

  7. 7

    Canfora, L., Bacci, G., Pinzari, F., Lo Papa, G., Dazzi, C., and Benedetti, A., Salinity and bacterial diversity: to what extent does the concentration of salt affect the bacterial community in a saline soil?, PLoS One, 2014, vol. 9. e106662.

  8. 8

    Gamalero, E. and Glick, B.R., Bacterial modulation of plant ethylene levels, Plant Physiol., 2015, vol. 169, pp. 13‒22.

  9. 9

    Gamzaeva, R.S., Effect of biopreparations and mineral fertilizers on the total soil biological activity and on barley yield, Izv. SPbGAU, 2016, pp. 86‒90.

  10. 10

    Gkarmiri, K., Mahmood, S., Ekblad, A., Alström, S., Högberg, N., and Finlay, R., Identifying the active microbiome associated with roots and rhizosphere soil of oilseed rape, Appl. Environ.Microbiol., 2017, vol. 83. pii: e01938-17.

  11. 11

    Inceoğlu, O., Abu Al-Soud, W., Salles, J.F., Semenov, A.V., and van Elsas, J.D., Comparative analysis of bacterial communities in a potato field as determined by pyrosequencing, PLoS One, 2011, vol. 6. e23321.

  12. 12

    Jiang, H., Dong, H., Yu, B., Liu, X., Li, Y., and Ji, S., Microbial response to salinity change in Lake Chaka, a hypersaline lake on Tibetan plateau, Environ. Microbiol., 2007, vol. 9, pp. 2603–2621.

  13. 13

    Laktionov, Yu.V., Popova, T.A., Andreev, O.A., Ibatullina, R.P., and Kozhemyakov, A.P., Development of a stable form of growth-stimulating microbiological preparations and their efficiency, Sel’skokhoz. Biol., 2011. vol. 3, pp. 116‒118.

  14. 14

    Nikovskaya, G.N. and Kalinichenko, K.V., Bioleaching of heavy metals from sludge after biological treatment of municipal effluent, J. Water Chem. Technol., 2013, vol. 35, no. 2, pp. 80‒85.

  15. 15

    Pérez-Montaco, F., Alías-Villegas, C., Bellogín, R.A., del Cerro, P., Espuny, M.R., Jiménez-Guerrero, I., López-Baena, F.J., Ollero, F.J., and Cubo, T., Plant growth promotion in cereal and leguminous agricultural important plants: from microorganism capacities to crop production, Microbiol. Res., 2014, vol. 169, pp. 325‒336.

  16. 16

    Pester, M., Rattei, T., Flench, S., Gröngröft, A., Richter, A., and Overmann, J., amoA-based consensus phylogeny of ammonia-oxidizing archaea and deep sequencing of amoA genes from soils of four different geographic regions, Environ. Microbiol., 2012, vol. 14, pp. 525–539.

  17. 17

    Petrova, S.N. and Denshchikov, V.A., Variations of microbial abundance in the rhizosphere of pea varieties during formation of nitrogen-fixing symbioses, Zemledelie, 2013, no. 5, pp. 17‒19.

  18. 18

    Pinevich, A.V., Mikrobiologiya. Biologiya prokariotov (Microbiology. Prokaryotic Biology), S.-Pb., S.-Pb. Gos. Univ., 2007.

  19. 19

    Pishchik, V.N., Vorobyev, N.I., Moiseev, K.G., Sviridova, O.V., and Surin, V.G., Influence of Bacillus subtilis on the physiological state of wheat and the microbial community of the soil under different rates of nitrogen fertilizers, Euras. Soil Sci., 2015, vol. 48, pp. 77‒84.

  20. 20

    Pusenkova, L.I., Il’yasova, E.Yu., and Kireeva, N.A., Effect of biopreparations on sugar beet productivity, Agrokhimiya, 2012, no. 10, pp. 20–26.

  21. 21

    Shaposhnikov, A.I., Belimov, A.A., Kravchenko, L.V., and Vivanko, D.M., Interaction of rhizosphere bacteria with plants: mechanisms of formation and factors of efficiency of associative symbioses, Sel’skokhoz. Biol., 2011, no. 3, pp. 16‒22.

  22. 22

    Singh, S.P., Raval, V.H., Purohit, M.K., Thumar, J.T., Gohel, S.D., Pandey, S., Akbari, V.G., and Rawal, C.M., Haloalkaliphilic bacteria and actinobacteria from the saline habitats: new opportunities for biocatalysis and bioremediation, in MicroorganismsinEnvironmental Management: Microbes and Environment, Satyanarayana, T. and Johri, B.N., Eds., Dordrecht: Springer, 2012, pp. 415–429.

  23. 23

    Treusch, A.H., Leininger, S., Kletzin, A., Schuster, S.C., Klenk, H.P., and Schleper, C., Novel genes for nitrite reductase and Amo-related proteins indicate a role of uncultivated mesophilic crenarchaeota in nitrogen cycling, Environ. Microbiol., 2005, vol. 7, pp. 1985–1995.

  24. 24

    van der Heijden, M.G.A., de Bruin, S., Luckerhoff, L., van Logtestijn, R.S.P., and Schlaeppi, K., A widespread plant-fungal-bacterial symbiosis promotes plant biodiversity, plant nutrition and seedling recruitment, ISME J., 2016, vol. 10, pp. 389–399.

  25. 25

    van Elsas, J.D., Chiurazzi, M., Mallon, C.A., Elhottova, D., Kristufek, V., and Salles, J.F., Microbial diversity determines the invasion of soil by a bacterial pathogen, Proc. Natl. Acad. Sci. U. S. A., 2012, vol. 109, pp. 1159–1164.

  26. 26

    Wang, Q., Garrity, G.M., Tiedje, J.M., and Cole, J.R., Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy, Appl. Environ. Microbiol., 2007, vol. 73, pp. 5261–5267.

  27. 27

    Wu, Q.L., Zwart, G., Schauer, M., Agterveld, M.P.K., and Bahn, M.W., Bacterioplankton community composition along a salinity gradient of sixteen high-mountain lakes located on the Tibetan Plateau, China, Appl. Environ. Microbiol., 2006, vol. 72, pp. 5478–5485.

  28. 28

    Yergeau, E., Shifts in soil microorganisms in response to warming are consistent across a range of Antarctic environments, ISME J., 2011, vol. 6, pp. 692–702.

  29. 29

    Zhang, H., Sekiguchi, Y., Hanada, S., Hugenholtz, P., Kim, H., and Kamagata, Y., Gemmatimonas aurantiaca gen. nov., sp. nov., a gram-negative, aerobic, polyphosphate-accumulating micro-organism, the first cultured representative of the new bacterial phylum Gemmatimonadetes phyl. nov., Int. J. Syst. Evol. Microbiol., 2003, vol. 53, pp. 1155–1163.

  30. 30

    Zvyagintsev, D.G., Bab’eva, I.P., and Zenova, G.M., Biologiya pochv (Soil Biology), Moscow: Mos. Gos. Univ., 2005.

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Funding

The studies were supported by the Russian Science Foundation (projects nos. 17-76-10039 and 18-16-00073 (High-throughput sequencing and data analysis)), the Russian Foundation for Basic Research (project no. 11-04-90813), and the Ministry of Agriculture of the Russian Federation.

Author information

Correspondence to S. N. Petrova.

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The authors declare that they have no conflict of interest. This article does not contain any studies involving animals or human participants performed by any of the authors.

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Translated by E. Makeeva

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Petrova, S.N., Andronov, E.E., Belimov, A.A. et al. Prokaryotic Community Structure in the Rapeseed (Brassica napus L.) Rhizosphere Depending on Addition of 1-Aminocyclopropane-1-Carboxylate-Utilizing Bacteria. Microbiology 89, 115–121 (2020). https://doi.org/10.1134/S0026261720010117

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Keywords:

  • rhizosphere microbiome
  • high-throughput sequencing
  • rhizosphere
  • bacterial introduction
  • ACC deaminase
  • Brassica napus
  • mineral nutrition
  • growth stimulation