PLANT BIOLOGY
ANIMAL BIOLOGY
SUBSCRIPTION
E-SUBSCRIPTION
 
MAP
MAIN PAGE

 

 

 

 

doi: 10.15389/agrobiology.2022.5.821eng

UDC: 631.52:581.557:579.64:575

Acknowledgements:
Supported financially by Russian Science Foundation (project № 19-16-00081P)

 

AGRICULTURAL MICROBIOLOGY AND SYMBIOGENETICS: SYNTHESIS OF CLASSICAL IDEAS AND CONSTRUCTION OF HIGHLY PRODUCTIVE AGROCENOSES (review)

N.A. Provorov1 , I.A. Tikhonovich1, 2

1All-Russian Research Institute for Agricultural Microbiology, 3, sh. Podbel’skogo, St. Petersburg, 196608 Russia,
e-mail provorovnik@yandex.ru (✉ corresponding author);
2Saint-Petersburg State University, 7-9, Universitetskaya nab., Petersburg, 199034 Russia, e-mail arriam2008@yandex.ru

ORCID:
Provorov N.A. orcid.org/0000-0001-9091-9384
Tikhonovich I.A. orcid.org/0000-0001-8968-854X

Received June 16, 2022

Agricultural microbiology (AM) is presented as a discipline addressing the prokaryotic and eukaryotic microorganisms that influence operation of the major components of agrocenosis — plants, animals and soils. Development of AM is based on the synthesis of ideas and methods of microbiology, plant physiology, soil science and genetics. This synthesis is aimed to study the organization and evolution of biosystems in which symbiotic microorganisms perform adaptively important functions in cooperation with each other and with host organisms. Upon migration from environment into the endosymbiotic niches of plants and animals, microorganisms form with them multicomponent complexes — holobionts (E. Rosenberg, I. Zilber-Rosenberg, 2018). They possess own systems of heredity, symbiogenomes and hologenomes, which have become the subjects of a new discipline, symbiogenetics (I.A. Tikhonovich, N.A. Provorov, 2012). Microorganisms forming symbioses with plants perform the important adaptive functions — nutritional (N2 fixation, absorption of soil nutrients, firstly phosphates), defensive (biocontrol of pathogens and phytophagans) and regulatory (synthesis of phytohormones that optimize plant development and improve their resistance to adverse environment) (I.A. Tikhonovich, N.A. Provorov, 2009). The broadly studied and practically important plant symbionts include: a) nodule bacteria or rhizobia (Rhizobiales) — N2-fixing symbionts of legumes; b) arbuscular mycorrhizal fungi (Glomeromycota) — phosphate-mobilizing symbionts of a wide range (more than 80 % species) of plants (A. Berruti et al., 2016); c) rhizospheric and endophytic bacteria (e.g., Azospirillum,Bacillus, Pseudomonas) which stimulate the development of plants and determine their resistance to antagonists (pathogens, pests) and stresses (drought, salinity of soils, their contamination with xenobiotics or heavy metals) (M.A. Hassani et al., 2018). In animals, trophic symbionts determine the assimilation of plant biomass (intestinal or rumen microbiota), synthesis of essential amino acids and cofactors (intestinal and intracellular symbionts), and N2 fixation (symbionts of some herbivorous animals) (E. Rinninella et al., 2019). The study of microbial effects on plants and animals makes it possible to create microbial preparations that improve the nutrition of hosts, their resistance to biotic and abiotic stresses, and increase the soil fertility. In crop production, preparations of N2-fixing and growth-stimulating bacteria are widely used, which ensure a drastic reduction in application of environmentally hazardous nitrogen and phosphorus fertilizers. Preparations of microorganisms that are antagonists of phytopathogens — Pseudomonas, Bacillus(B.J. Lugtenberg et al., 2001; V.K. Chebotar et al., 2009), rodents — Salmonella enteritidis, Serratia plymuthica (A. Soenens, J. Imperial, 2019) or phytophagous insects — Bacillus thuringiensis, Beauveria bassiana (A.V. McGuire, T.D. Northfield, 2020) are used broadly for their biocontrol to significantly reduce the pesticide load on agrocenoses. By studying the integrative functions of agronomically valuable microorganisms, AM invests a significant contribution to the fundamental biological research, including the genetic and molecular interactions of prokaryotes and eukaryotes, evolution of cell and of its genome, and formation of supraorganismal genetic systems (I.A. Tikhonovich, N.A. Provorov, 2012). Based on these studies, methods of symbiotic engineering are being developed aimed at constructing the highly productive biosystems, including the cereal and vegetable cultivars capable of symbiosis with rhizobia, as well as N2-fixing plants.

Keywords: agricultural microbiology (AM), symbiogenetics, genetic engineering, symbiotic nitrogen fixation, biocontrol of pathogens and pests, microbial preparations, sustainable agriculture.

 

REFERENCES

  1. Voznyakovskaya Yu.M. Mikroflora rasteniy i urozhay [Plant microflora and yield performance]. Moscow, 1969 (in Russ.).
  2. Kandybin N.V. Bakterial’nye sredstva bor’by s gryzunami i vrednymi nasekomymi: teoriya i praktika [Bacterial means of control of rodents and harmful insects: theory and practice]. Moscow, 1989 (in Russ.).
  3. Flor H.H. Genetics of pathogenicity in Melampsora lini. J. Agric. Res., 1946, 73: 335-357.
  4. Nutman P.S. Genetic factors concerned in the symbiosis of clover and nodule bacteria. Nature, 1946, 157: 463-465 CrossRef
  5. Lobashev M.E. Genetika [Genetics]. Leningrad, 1967 (in Russ.). 
  6. Provorov N.A., Vorob’ev N.I. Geneticheskie osnovy еvolyutsii rastitel’no-mikrobnogo simbioza [Genetic bases of the evolution of plant-microbial symbiosis]. St. Petersburg, 2012 (in Russ.).
  7. Rosenberg E., Zilber-Rosenberg I. The hologenome concept of evolution after 10 years. Microbiome, 2018, 6: 78 CrossRef
  8. Tikhonovich I.A., Provorov N.A. Agricultural microbiology as the basis of ecologically sustainable agriculture: fundamental and applied aspects. Sel'skokhozyaistvennaya biologiya [Agricultural Biology], 2011, 3: 3-9 (in Russ.).
  9. Provorov N.A., Onishchuk O.P. Evolutionary-genetic bases for symbiotic engineering in plants — a mini review. Sel'skokhozyaistvennaya biologiya [Agricultural Biology], 2018, 53(3): 464-474 CrossRef
  10. Kostychev S.P. Fiziologiya rasteniy [Plant physiology]. Moscow-Leningrad, 1937 (in Russ.).
  11. Karatygin I.V. Trudy Botanicheskogo instituta RAN. Vyp. 9 [Proceedings of the Botanical Institute of the Russian Academy of Sciences]. St. Petersburg, 1993 (in Russ.).
  12. Provorov N.A., Shtark O.Yu. Mikologiya i fitopatologiya, 2014, 48(3): 151-160 (in Russ.).
  13. Izrail’skiy V.P., Runov E.V., Bernard V.V. Kluben’kovye bakterii i nitragin [Nodule bacteria and nitragin]. Moscow, 1933 (in Russ.).
  14. Mishustin E.N. Mikroorganizmy i produktivnost’ zemledeliya [Microorganisms and agricultural productivity]. Moscow, 1972 (in Russ.).
  15. Dorosinskiy L.M. Kluben’kovye bakterii i nitragin [Nodule bacteria and nitragin]. Leningrad, 1970 (in Russ.).
  16. Provorov N.A., Simarov B.V. Genetika, 1992, 28(6): 5-14 (in Russ.).
  17. Provorov N.A., Tikhonovich I.A. Genetic resources for improving nitrogen fixation in legume-rhizobia symbiosis. Genetic Resources and Crop Evolution, 2003, 50(1): 89-99 CrossRef
  18. Onishchuk O.P., Vorob’ev N.I., Provorov N.A. Prikladnaya biokhimiya i mikrobiologiya, 2017, 53(2): 127-135 (in Russ.).
  19. Carelli M., Gnocchi S., Fancelli S., Mengoni A., Paffetti D., Scotti C., Bazzicalupo M. Genetic diversity and dynamics of Sinorhizobium meliloti populations nodulating different alfalfa cultivars in Italian soils. Applied and Environmental Microbiology, 2000, 66(11): 4785-4789 CrossRef
  20. Masson-Boivin C., Sachs J.L. Symbiotic nitrogen fixation by rhizobia-the roots of a success story. Curr. Opin. Plant Biol., 2018, 44: 7-15 CrossRef
  21. Barnes D.K., Heichel G.H., Vance C.P., Ellis W.R. A multiple-trait breeding program for improving the symbiosis for N2 fixation between Medicago sativa L. and Rhizobium meliloti. Plant and Soil,1984, 32(2): 303-314 CrossRef
  22. El Yahyaoui F., Küster H., Ben Amor B., Hohnjec N., Pühler A., Becker A., Gouzy J., Vernié T., Gough C., Niebel A., Godiard L., Gamas P. Expression profiling in Medicago truncatula identifies more than 750 genes differentially expressed during nodulation, including many potential regulators of the symbiotic program. Plant Physiology, 2004, 136(2): 3159-3176 CrossRef
  23. Awika H.O., Mishra A.K., Gill H., DiPiazza J., Avila C.A., Joshi V. Selection of nitrogen responsive root architectural traits in spinach using machine learning and genetic correlations. Sci. Rep., 2021, 11: 9536 CrossRef
  24. Simarov B.V., Aronshtam A.A., Novikova N.I., Sharypova L.A., Bazhenova O.V., Provorov N.A. Geneticheskie osnovy selektsii kluben’kovykh bakteriy [Genetic basis for the selection of nodule bacteria]. Leningrad, 1990 (in Russ.).
  25. Simon R., Priefer U., Pühler A. A broad host range mobilization system for in vivo genetic engineering: transposon mutagenesis in gram negative bacteria. Nat. Biotechnol., 1983, 1(3): 784-791 CrossRef
  26. Sharypova L.A., Onishchuk O.P., Chesnokova O.N., Fomina-Eshenko J.G., Simarov B.V. Isolation and characterization of Rhizobium meliloti Tn5 mutants showing enhanced symbiotic effectiveness. Microbiology, 1994, 140(3)): 463-470 CrossRef
  27. Onishchuk O.P., Vorob’ev N.I., Provorov N.A., Simarov B.V. Еkologicheskaya genetika, 2009, 7(2): 3-10 (in Russ.).
  28. Provorov N.A., Onishchuk O.P., Yurgel’ S.N., Kurchak O.N., Chizhevskaya E.P., Vorob’ev N.I., Zatovskaya T.V., Simarov B.V. Genetika, 2014, 50(11): 1273-1285 (in Russ.).
  29. Ferguson B.J., Indrasumunar A., Hayshi S., Lin H.M., Lin Y.H., Reid D.E. Gresshoff P.M. Molecular analysis of legume nodule development and autoregulation. Journal of Integrative Plant Biology, 2010, 52(1): 61-76 CrossRef
  30. Denison R.F., Kiers E.T. Lifestyle alternatives for rhizobia: mutualism, parasitism and foregoing symbiosis. FEMS Microbiology Letters, 2004, 237(2): 187-193 CrossRef
  31. Vorob’ev N.I., Provorov N.A. Еkologicheskaya genetika, 2013, 11(4): 73-85 CrossRef (in Russ.).
  32. Hassani M.A., Durán P., Hacquard S. Microbial interactions within the plant holobiont. Microbiome, 2018. 6: 58 CrossRef
  33. Laptev G.Yu., Yyldyrym E.A., Dunyashev T.P., Il’ina L.A., Tyurina D.G., Filippova V.A., Brazhnik E.A., Tarlavin N.V., Dubrovin A.V., Novikova N.I. Peculiarities of taxonomic and functional characteristics of rumen microbiota of dairy cows suffered from ketosis. Sel'skokhozyaistvennaya biologiya [Agricultural Biology], 2021, 56(2): 356-373 CrossRef
  34. Laptev G.Yu., Yyldyrym E.A., Dunyashev T.P., Il’ina L.A., Tyurina D.G., Filippova V.A., Brazhnik E.A., Tarlavin N.V., Dubrovin A.V., Novikova N.I., Bol’shakov V.N., Ponomareva E.S. Biodiversity and predicted metabolic functions of the rumen microbiota depending on feeding habits at different stages of the physiological cycle of dairy cows. Sel'skokhozyaistvennaya biologiya [Agricultural Biology], 2021, 56(4): 619-640 CrossRef
  35. Li W., Tapiainen T., Brinkac L., Lorenzi H.A., Moncera K., Tejesvi M.V., Salo J., Nelson K.E. Vertical transmission of gut microbiome and antimicrobial resistance genes in infants exposed to antibiotics at birth. The Journal of Infectious Diseases, 224(7): 1236-1246 CrossRef
  36. Vorob’ev N.I., Egorov I.A., Kochish I.I., Nikonov I.N., Lenkova T.N. Fractal analysis of frequency-taxonomic profile of broiler's gut microbiota for studying the influence of probiotics on bird development. Sel'skokhozyaistvennaya biologiya [Agricultural Biology], 2021, 56(2): 400-410 CrossRef
  37. Tikhonovich I.A., Provorov N.A. From plant-microbe interactions to Symbiogenetics: a universal paradigm for the inter-species genetic integration. Annals of Applied Biology, 2009, 154(3): 341-350 CrossRef
  38. Tikhonovich I.A., Provorov N.A. Genetika, 2012, 48(4): 437-450 (in Russ.).
  39. Provorov N.A., Tikhonovich I.A., Vorob’ev N.I. Simbioz i simbiogenez [Symbiosis and symbiogenesis]. St. Petersburg, 2018 (in Russ.). 
  40. Provorov N.A. Genetic individuality and inter-species altruism: modelling of symbiogenesis using different types of symbiotic bacteria. Biologocal Communications, 2021, 66(1): 65-71 CrossRef
  41. Smith D.R., Keeling P.J. Mitochondrial and plastid genome architecture: reoccurring themes, but significant differences at the extremes. Proc. Natl. Acad. Sci. USA, 2015, 112(33): 10177-10184.
  42. Curatti L., Rubio L.M. Challenges to develop nitrogen-fixing cereals by direct nif-gene transfer. Plant Sci., 2014, 225: 130-137 CrossRef
  43. Burén S., Pratt K., Jiang X., Guo Y., Jimenez-Vicente E., Echavarri-Erasun C., Dean D.R., Saaem I., Gordon D.B., Voigt C.A., Rubio L.M. Biosynthesis of the nitrogenase active-site cofactor precursor NifB-co in Saccharomyces cerevisiae. Proceedings of the National Academy of Sciences, 2019, 116(50): 25078-25086 CrossRef
  44. Tovar J., León-Avila G., Sánchez L.B., Sutak R., Tachezy J., van der Giezen M., Hernández M., Müller M., Lucocq J.M. Mitochondrial remnant organelles of Giardia function in iron-sulphur protein maturation. Nature, 2003, 426(6963): 172-176 CrossRef
  45. Lugtenberg B.J.J., Dekkers L., Bloemberg G. Molecular determinants of rhizosphere colonization by Pseudomonas. Annual Review of Phytopathology, 39: 461-490 CrossRef
  46. Chebotar V.K., Makarova N.M., Shaposhnikov A.I., Kravchenko L.V. Antifungal and phytostimulating characteristics of Bacillus subtilis Ch-13 rhizospheric strain, producer of bioprepations. Appl. Biochem. Microbiol., 2009, 4: 419-423 CrossRef
  47. Soenens A., Imperial J. Biocontrol capabilities of the genus Serratia. Phytochemistry Reviews, 2019, 19: 577-587 CrossRef
  48. McGuire1 A.V., Northfield T.D. Tropical occurrence and agricultural importance of Beauveria bassiana and Metarhizium anisopliae. Front. Sustain. Food Syst., 2020, 4: 6 CrossRef
  49. Berruti A., Lumini E., Balestrini R., Bianciotto V. Arbuscular mycorrhizal fungi as natural biofertilizers: let's benefit from past successes. Frontiers in Microbiology, 2016, 6: 1559 CrossRef
  50. Zavalin A., Chebotar V., Alferov A., Chernova L., Shcherbakova E., Chizhevskaya E. Nitrogen use by plants and nitrogen flows after application of standard and biomodified nitrogen fertilizers on barley. Biological Communications, 2021, 66(4): 4283-4289.
  51. Rinninella E., Raoul P., Cintoni M., Franceschi F., Miggiano G.A.D., Gasbarrini A., Mele M.C. What is the healthy gut microbiota composition? A changing ecosystem across age, environment, diet and diseases. Microorganisms, 2019, 7(1): 14 CrossRef
  52. Savel’eva N.V., Burlakovskiy M.S., Emel’yanov V.V., Lutova L.A. Еkologicheskaya genetika, 2015, 13(2): 77-99 (in Russ.).
  53. Green B.R. Chloroplast genomes of photosynthetic eukaryotes. The Plant Journal, 2011, 66(1): 34-44 CrossRef
  54. Serôdio J., Cruz S., Cartaxana P., Calado R. Photophysiology of kleptoplasts: photosynthetic use of light by chloroplasts living in animal cells. Phil. Trans. R. Soc. B.,2014, 369(1640): 20130242 CrossRef
  55. Ševčíková T., Horák A., Klimeš V., Zbránková V., Demir-Hilton E., Sudek S., Jenkins J., Schmutz J., Přibyl P., Fousek J., Vlček C., Lang B.F., Oborník M., Worden A.Z., Eliáš M.  Updating algal evolutionary relationships through plastid genome sequencing: did alveolate plastids emerge through endosymbiosis of an ochrophyte? Sci. Rep., 2015, 5: 10134 CrossRef
  56. Vavilov N.I. Selektsiya kak nauka. Obshchaya selektsiya rasteniy [Selection as a science. General plant breeding]. Moscow, 1934 (in Russ.).

 

back

 


CONTENTS

 

 

Full article PDF (Rus)

Full article PDF (Eng)