1887

Abstract

Soybean is the most important legume cropped worldwide and can highly benefit from the biological nitrogen fixation (BNF) process. Brazil is recognized for its leadership in the use of inoculants and two strains, CPAC 15 (=SEMIA 5079) and CPAC 7 (=SEMIA 5080) compose the majority of the 70 million doses of soybean inoculants commercialized yearly in the country. We studied a collection of natural variants of these two strains, differing in properties of competitiveness and efficiency of BNF. We sequenced the genomes of the parental strain SEMIA 566 of , of three natural variants of this strain (S 204, S 340 and S 370), and compared with another variant of this group, strain CPAC 15. We also sequenced the genome of the parental strain SEMIA 586 of , of three natural variants of this strain (CPAC 390, CPAC 392 and CPAC 394) and compared with the genome of another natural variant, strain CPAC 7. As the main genes responsible for nodulation (, , ) and BNF (, ) in soybean are located in symbiotic islands, our objective was to identify genetic variations located in this region, including single nucleotide polymorphisms (SNPs) and insertions and deletions (indels), that could be potentially related to their different symbiotic phenotypes. We detected 44 genetic variations in the strains and three in . As the strains have gone through a longer period of adaptation to the soil, the higher number of genetic variations could be explained by survival strategies under the harsh environmental conditions of the Brazilian Cerrado biome. Genetic variations were detected in genes enconding proteins such as a dephospho-CoA kinase, related to the CoA biosynthesis; a glucosamine-fructose-6-phosphate aminotransferase, key regulator of the hexosamine biosynthetic pathway; a LysR family transcriptional regulator related to nodulation genes; and NifE and NifS proteins, directly related to the BNF process. We suggest potential genetic variations related to differences in the symbiotic phenotypes.

Funding
This study was supported by the:
  • INCT - Plant Growth-Promoting Microorganisms for Agricultural Sustainability and Environmental Responsibility (Award CNPq 465133/2014-4, Fundação Araucária-STI 043/2019, CAPES)
    • Principle Award Recipient: MariangelaHungria
  • This is an open-access article distributed under the terms of the Creative Commons Attribution NonCommercial License.
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2022-04-19
2024-03-29
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References

  1. Lloret L, Martínez-RomerO E. Evolución y filogenia de rhizobium. Rev Latinoam Microbiol 2005; 47:43–60
    [Google Scholar]
  2. Sachs JL, Skophammer RG, Regus JU. Evolutionary transitions in bacterial symbiosis. Proc Natl Acad Sci U S A 2011; 108 Suppl 2:10800–10807 [View Article] [PubMed]
    [Google Scholar]
  3. Werner GDA, Cornwell WK, Sprent JI, Kattge J, Kiers ET. A single evolutionary innovation drives the deep evolution of symbiotic N2-fixation in angiosperms. Nat Commun 2014; 5:4087 [View Article] [PubMed]
    [Google Scholar]
  4. Daubech B, Remigi P, Doin de Moura G, Marchetti M, Pouzet C et al. Spatio-temporal control of mutualism in legumes helps spread symbiotic nitrogen fixation. elife 2017; 6:e28683 [View Article] [PubMed]
    [Google Scholar]
  5. Hungria M, Mendes IC. Nitrogen fixation with soybean: the perfect symbiosis. In de Bruijn FJ. eds Biological Nitrogen Fixation vol 2 New Jersey: John Wiley & Sons; 2015 pp 1005–1019
    [Google Scholar]
  6. Hungria M, Barcellos FG, Mendes IC, Chueire LMO, Ribeiro RA et al. Introdução, Estabelecimento e Adaptação de Bradirrizóbios Simbiontes da Soja em Solos Brasileiros. In Yamada-Ogata SF, Nakazato G, Furlaneto MC, Nogueira MA. eds Tópicos Especiais Em Microbiologia Londrina: UEL; 2015 pp 243–261
    [Google Scholar]
  7. Hungria M, Menna P, Delamuta JRM. Bradyrhizobium, the ancestor of all rhizobia: phylogeny of housekeeping and nitrogen-fixation genes. In de Bruijn FJ. eds Biological Nitrogen Fixation vol 1 New Jersey: John Wiley & Sons; 2015 pp 191–202
    [Google Scholar]
  8. de Souza GK, Sampaio J, Longoni L, Ferreira S, Alvarenga S et al. Soybean inoculants in Brazil: an overview of quality control. Braz J Microbiol 2019; 50:205–211 [View Article] [PubMed]
    [Google Scholar]
  9. Jaiswal SK, Dakora FD. Widespread distribution of highly adapted Bradyrhizobium species nodulating diverse legumes in Africa. Front Microbiol 2019; 10:310 [View Article] [PubMed]
    [Google Scholar]
  10. MacLean AM, Finan TM, Sadowsky MJ. Genomes of the symbiotic nitrogen-fixing bacteria of legumes. Plant Physiol 2007; 144:615–622 [View Article] [PubMed]
    [Google Scholar]
  11. Menna P, Hungria M. Phylogeny of nodulation and nitrogen-fixation genes in Bradyrhizobium: supporting evidence for the theory of monophyletic origin, and spread and maintenance by both horizontal and vertical transfer. Int J Syst Evol Microbiol 2011; 61:3052–3067 [View Article] [PubMed]
    [Google Scholar]
  12. Kaneko T, Nakamura Y, Sato S, Minamisawa K, Uchiumi T et al. Complete genomic sequence of nitrogen-fixing symbiotic bacterium Bradyrhizobium japonicum USDA110. DNA Res 2002; 9:189–197 [View Article] [PubMed]
    [Google Scholar]
  13. Kaneko T, Maita H, Hirakawa H, Uchiike N, Minamisawa K et al. Complete genome sequence of the soybean symbiont Bradyrhizobium japonicum strain USDA6T. Genes (Basel) 2011; 2:763–787 [View Article] [PubMed]
    [Google Scholar]
  14. Santos MS, Nogueira MA, Hungria M. Microbial inoculants: reviewing the past, discussing the present and previewing an outstanding future for the use of beneficial bacteria in agriculture. AMB Express 2019; 9:205 [View Article] [PubMed]
    [Google Scholar]
  15. Hungria M, Campo RJ, Mendes IC, Graham PH. Contribution of biological nitrogen fixation to the N nutrition of grain crops in the tropics: the success of soybean (Glycine max L. Merr.) in South America. In Singh RP, Shankar N, Jaiwal PK. eds Nitrogen Nutrition and Sustainable Plant Productivity Houston, Texas: Studium Press, LLC; 2006 pp 43–93
    [Google Scholar]
  16. Ferreira MC, Hungria M. Recovery of soybean inoculant strains from uncropped soils in Brazil. Field Crops Res 2002; 79:139–152 [View Article]
    [Google Scholar]
  17. Boddey LH, Hungria M. Phenotypic grouping of Brazilian Bradyrhizobium strains which nodulate soybean. Biol Fertil Soils 1997; 25:407–415 [View Article]
    [Google Scholar]
  18. Santos MA, Vargas MAT, Hungria M. Characterization of soybean Bradyrhizobium strains adapted to the Brazilian savannas. FEMS Microbiol Ecol 1999; 30:261–272 [View Article] [PubMed]
    [Google Scholar]
  19. Vargas MAT, Mendes IC, Suhet AR, Peres JRR. Duas novas cepas de rizóbio para inoculação em soja. Brasília:EMBRAPA-SPI 19921–3
    [Google Scholar]
  20. Peres JRR, Mendes IC, Suhet AR, Vargas MAT. Eficiência e competitividade de estirpes de rizóbios para soja em solos do cerrado. R Bras Ci Solo 1993; 17:357–363
    [Google Scholar]
  21. Hungria M, Boddey LH, Santos MA, Vargas MAT. Nitrogen fixation capacity and nodule occupancy by Bradyrhizobium japonicum and B. elkanii strains. Biol Fertil Soils 1998; 27:393–399 [View Article]
    [Google Scholar]
  22. Barcellos FG, Batista J da S, Menna P, Hungria M. Genetic differences between Bradyrhizobium japonicum variant strains contrasting in N2-fixation efficiency revealed by representational difference analysis. Arch Microbiol 2009; 191:113–122 [View Article] [PubMed]
    [Google Scholar]
  23. Batista JS da S, Torres AR, Hungria M. Towards a two-dimensional proteomic reference map of Bradyrhizobium japonicum CPAC 15: spotlighting “hypothetical proteins.”. Proteomics 2010; 10:3176–3189 [View Article] [PubMed]
    [Google Scholar]
  24. Gomes DF, da Silva Batista JS, Rolla AAP, da Silva LP, Bloch C et al. Proteomic analysis of free-living Bradyrhizobium diazoefficiens: highlighting potential determinants of a successful symbiosis. BMC Genomics 2014; 15:643 [View Article] [PubMed]
    [Google Scholar]
  25. Hungria M, Franchini JC, Campo RJ, Crispino CC, Moraes JZ et al. Nitrogen nutrition of soybean in Brazil: Contributions of biological N2 fixation and N fertilizer to grain yield. Can J Plant Sci 2006; 86:927–939 [View Article]
    [Google Scholar]
  26. Barcellos FG, Menna P, da Silva Batista JS, Hungria M. Evidence of horizontal transfer of symbiotic genes from a Bradyrhizobium japonicum inoculant strain to indigenous diazotrophs Sinorhizobium (Ensifer) fredii and Bradyrhizobium elkanii in a Brazilian Savannah soil. Appl Environ Microbiol 2007; 73:2635–2643 [View Article] [PubMed]
    [Google Scholar]
  27. Chibeba AM, Kyei-Boahen S, Guimarães M de F, Nogueira MA, Hungria M. Isolation, characterization and selection of indigenous Bradyrhizobium strains with outstanding symbiotic performance to increase soybean yields in Mozambique. Agric Ecosyst Environ 2017; 246:291–305 [View Article] [PubMed]
    [Google Scholar]
  28. Siqueira AF, Ormeño-Orrillo E, Souza RC, Rodrigues EP, Almeida LGP et al. Comparative genomics of Bradyrhizobium japonicum CPAC 15 and Bradyrhizobium diazoefficiens CPAC 7: elite model strains for understanding symbiotic performance with soybean. BMC Genomics 2014; 15:1 [View Article] [PubMed]
    [Google Scholar]
  29. Hungria M, O’Hara GW, Zilli JE, Araujo RS, Deaker R et al. Isolation and growth of rhizobia. In Howieson JG, Dilworth MJ. eds Working with Rhizobia Canberra: Australian Centre for International Agriculture Reserch (ACIAR); 2016 pp 39–60
    [Google Scholar]
  30. Hungria M, Vargas MAT, Andrade DS, Campo RJ, Chueire LMO et al. Fixação biológica do nitrogênio em leguminosas de grãos. In Siqueira JO, Moreira FMS, Lopes AS, Guilherme LR, Faquin V. eds Soil Fertility, Soil Biology and Plant Nutrition Interrelationships Lavras: SBCS/UFLA/DCS; 1999 pp 597–620
    [Google Scholar]
  31. Hungria M, Vargas MAT. Environmental factors affecting N2 fixation in grain legumes in the tropics, with an emphasis on Brazil. Field Crops Res 2000; 65:151–164 [View Article]
    [Google Scholar]
  32. Göttfert M, Röthlisberger S, Kündig C, Beck C, Marty R et al. Potential symbiosis-specific genes uncovered by sequencing a 410-kilobase DNA region of the Bradyrhizobium japonicum chromosome. J Bacteriol 2001; 183:1405–1412 [View Article] [PubMed]
    [Google Scholar]
  33. Hungria M, Vargas MAT. Exploring the microbial diversity and soil management practices to optimize the contribution of soil microorganisms to plant nutrition. In Stacey G, Mullin B, Gresshoff P. eds Biology of Plant-Microbe Interactions 1996 pp 493–496
    [Google Scholar]
  34. Spry C, Kirk K, Saliba KJ. Coenzyme A biosynthesis: an antimicrobial drug target. FEMS Microbiol Rev 2008; 32:56–106 [View Article] [PubMed]
    [Google Scholar]
  35. Walia G, Kumar P, Surolia A. The role of UPF0157 in the folding of M. tuberculosis dephosphocoenzyme A kinase and the regulation of the latter by CTP. PLoS One 2009; 4:e7645 [View Article] [PubMed]
    [Google Scholar]
  36. Genschel U, Powell CA, Abell C, Smith AG. The final step of pantothenate biosynthesis in higher plants: cloning and characterization of pantothenate synthetase from Lotus japonicus and Oryza sativum (rice). Biochem J 1999; 341 (Pt 3):669–678 [View Article] [PubMed]
    [Google Scholar]
  37. Abiko Y. Pantothenic acid and coenzyme A: dephospho-coa pyrophosphorylase and dephospho-coa kinase as A possible bifunctional enzyme complex 1 (ATP: pantetheine-4’-phosphate adenyltransferase, EC 2.7.7.3 and ATP: dephospho- coa 3’-phosphotransferase, EC 2.7.1.24). Methods Enzymol 1970358–364
    [Google Scholar]
  38. Hart RJ, Abraham A, Aly ASI. Genetic characterization of coenzyme a biosynthesis reveals essential distinctive functions during malaria parasite development in blood and mosquito. Front Cell Infect Microbiol 2017; 7:260 [View Article] [PubMed]
    [Google Scholar]
  39. Nurkanto A, Jeelani G, Yamamoto T, Hishiki T, Naito Y et al. Biochemical, metabolomic, and genetic analyses of dephospho coenzyme a kinase involved in coenzyme a biosynthesis in the human enteric parasite Entamoeba histolytica. Front Microbiol 2018; 9:2902 [View Article] [PubMed]
    [Google Scholar]
  40. Dunn MF. Tricarboxylic acid cycle and anaplerotic enzymes in rhizobia. FEMS Microbiol Rev 1998; 22:105–123 [View Article] [PubMed]
    [Google Scholar]
  41. Green LS, Li Y, Emerich DW, Bergersen FJ, Day DA. Catabolism of alpha-ketoglutarate by a sucA mutant of Bradyrhizobium japonicum: evidence for an alternative tricarboxylic acid cycle. J Bacteriol 2000; 182:2838–2844 [View Article] [PubMed]
    [Google Scholar]
  42. Oppermann U, Filling C, Hult M, Shafqat N, Wu X et al. Short-chain dehydrogenases/reductases (SDR): the 2002 update. Chem Biol Interact 2003; 143–144:247–253 [View Article] [PubMed]
    [Google Scholar]
  43. Persson B, Kallberg Y, Bray JE, Bruford E, Dellaporta SL et al. The SDR (short-chain dehydrogenase/reductase and related enzymes) nomenclature initiative. Chem Biol Interact 2009; 178:94–98 [View Article] [PubMed]
    [Google Scholar]
  44. Kavanagh KL, Jörnvall H, Persson B, Oppermann U. The SDR superfamily: functional and structural diversity within a family of metabolic and regulatory enzymes. Cell Mol Life Sci 2008; 65:3895–3906 [View Article]
    [Google Scholar]
  45. Lasken RS, Kornberg A. The primosomal protein n’ of Escherichia coli is a DNA helicase. J Biol Chem 1988; 263:5512–5518 [PubMed]
    [Google Scholar]
  46. Huang Y-H, Lien Y, Huang C-C, Huang C-Y, Korolev S. Characterization of Staphylococcus aureus Primosomal DnaD protein: highly conserved C-terminal region is crucial for ssDNA and PriA helicase binding but not for DnaA protein-binding and self-tetramerization. PLoS ONE 2016; 11:e0157593 [View Article]
    [Google Scholar]
  47. Michel B, Sandler SJ. Replication restart in bacteria. J Bacteriol 2017; 199:e00102-17 [View Article] [PubMed]
    [Google Scholar]
  48. Lee EH, Kornberg A. Replication deficiencies in priA mutants of Escherichia coli lacking the primosomal replication n’ protein. Proc Natl Acad Sci U S A 1991; 88:3029–3032 [View Article] [PubMed]
    [Google Scholar]
  49. Sandler SJ, Samra HS, Clark AJ. Differential suppression of priA2::kan phenotypes in Escherichia coli K-12 by mutations in priA, lexA, and dnaC. Genetics 1996; 143:5–13 [View Article] [PubMed]
    [Google Scholar]
  50. McCool JD, Sandler SJ. Effects of mutations involving cell division, recombination, and chromosome dimer resolution on a priA2::kan mutant. Proc Natl Acad Sci U S A 2001; 98:8203–8210 [View Article] [PubMed]
    [Google Scholar]
  51. Henikoff S, Haughn GW, Calvo JM, Wallace JC. A large family of bacterial activator proteins. Proc Natl Acad Sci U S A 1988; 85:6602–6606 [View Article] [PubMed]
    [Google Scholar]
  52. Yang W, Wang W-Y, Zhao W, Cheng J-G, Wang Y et al. Preliminary study on the role of novel LysR family gene kp05372 in Klebsiella pneumoniae of forest musk deer. J Zhejiang Univ Sci B 2020; 21:137–154 [View Article] [PubMed]
    [Google Scholar]
  53. van Rhijn P, Vanderleyden J. The Rhizobium-plant symbiosis. Microbiol Rev 1995; 59:124–142 [View Article] [PubMed]
    [Google Scholar]
  54. Luo L, Yao S-Y, Becker A, Rüberg S, Yu G-Q et al. Two new Sinorhizobium meliloti LysR-type transcriptional regulators required for nodulation. J Bacteriol 2005; 187:4562–4572 [View Article] [PubMed]
    [Google Scholar]
  55. Takeshima K, Hidaka T, Wei M, Yokoyama T, Minamisawa K et al. Involvement of a novel genistein-inducible multidrug efflux pump of Bradyrhizobium japonicum early in the interaction with Glycine max (L.) Merr. Microbes Environ 2013; 28:414–421 [View Article] [PubMed]
    [Google Scholar]
  56. Cooper B, Campbell KB, Beard HS, Garrett WM, Mowery J et al. A proteomic network for symbiotic nitrogen fixation efficiency in Bradyrhizobium elkanii. Mol Plant Microbe Interact 2018; 31:334–343 [View Article] [PubMed]
    [Google Scholar]
  57. Gruer MJ, Artymiuk PJ, Guest JR. The aconitase family: three structural variations on a common theme. Trends Biochem Sci 1997; 22:3–6 [View Article] [PubMed]
    [Google Scholar]
  58. Yasutake Y, Yao M, Sakai N, Kirita T, Tanaka I. Crystal structure of the Pyrococcus horikoshii isopropylmalate isomerase small subunit provides insight into the dual substrate specificity of the enzyme. J Mol Biol 2004; 344:325–333 [View Article] [PubMed]
    [Google Scholar]
  59. Olson JW, Agar JN, Johnson MK, Maier RJ. Characterization of the NifU and NifS Fe-S cluster formation proteins essential for viability in Helicobacter pylori. Biochemistry 2000; 39:16213–16219 [View Article] [PubMed]
    [Google Scholar]
  60. Li Q, Chen S. Transfer of Nitrogen Fixation (nif) Genes to Non-diazotrophic Hosts. Chembiochem 2020; 21:1717–1722 [View Article] [PubMed]
    [Google Scholar]
  61. Aguilar OM, Taormino J, Thöny B, Ramseier T, Hennecke H et al. The nifEN genes participating in FeMo cofactor biosynthesis and genes encoding dinitrogenase are part of the same operon in Bradyrhizobium species. Mol Gen Genet 1990; 224:413–420 [View Article] [PubMed]
    [Google Scholar]
  62. Hu Y, Fay AW, Lee CC, Yoshizawa J, Ribbe MW. Assembly of nitrogenase MoFe protein. Biochemistry 2008; 47:3973–3981 [View Article] [PubMed]
    [Google Scholar]
  63. Kucho K-I, Tamari D, Matsuyama S, Nabekura T, Tisa LS. Nitrogen fixation mutants of the Actinobacterium Frankia casuarinae CcI3. Microbes Environ 2017; 32:344–351 [View Article] [PubMed]
    [Google Scholar]
  64. Kennedy C, Dean D. The nifU, nifS and nifV gene products are required for activity of all three nitrogenases of Azotobacter vinelandii. Mol Gen Genet 1992; 231:494–498 [View Article] [PubMed]
    [Google Scholar]
  65. Kato N, Dasgupta R, Smartt CT, Christensen BM. Glucosamine:fructose-6-phosphate aminotransferase: gene characterization, chitin biosynthesis and peritrophic matrix formation in Aedes aegypti. Insect Mol Biol 2002; 11:207–216 [View Article] [PubMed]
    [Google Scholar]
  66. McKnight GL, Mudri SL, Mathewes SL, Traxinger RR, Marshall S et al. Molecular cloning, cDNA sequence, and bacterial expression of human glutamine:fructose-6-phosphate amidotransferase. J Biol Chem 1992; 267:25208–25212 [View Article]
    [Google Scholar]
  67. Safronova VI, Kuznetsova IG, Sazanova AL, Kimeklis AK, Belimov AA et al. Extra-slow-growing Tardiphaga strains isolated from nodules of Vavilovia formosa (Stev.) Fed. Arch Microbiol 2015; 197:889–898 [View Article] [PubMed]
    [Google Scholar]
  68. Surin BP, Downie JA. Characterization of the Rhizobium leguminosarum genes nodLMN involved in efficient host-specific nodulation. Mol Microbiol 1988; 2:173–183 [View Article] [PubMed]
    [Google Scholar]
  69. Baev N, Endre G, Petrovics G, Banfalvi Z, Kondorosi A. Six nodulation genes of nod box locus 4 in Rhizobium meliloti are involved in nodulation signal production: nodM codes for D-glucosamine synthetase. Mol Gen Genet 1991; 228:113–124 [View Article] [PubMed]
    [Google Scholar]
  70. Dyda F, Klein DC, Hickman AB. GCN5-related N-acetyltransferases: A structural overview. Annu Rev Biophys Biomol Struct 2000; 29:81–103 [View Article] [PubMed]
    [Google Scholar]
  71. Hentchel KL, Escalante-Semerena JC. Acylation of biomolecules in prokaryotes: a widespread strategy for the control of biological function and metabolic stress. Microbiol Mol Biol Rev 2015; 79:321–346 [View Article] [PubMed]
    [Google Scholar]
  72. Shirmast P, Ghafoori SM, Irwin RM, Abendroth J, Mayclin SJ et al. Structural characterization of a GNAT family acetyltransferase from Elizabethkingia anophelis bound to acetyl-CoA reveals a new dimeric interface. Sci Rep 2021; 11:1 [View Article] [PubMed]
    [Google Scholar]
  73. Aravind L, Galperin MY, Koonin EV. The catalytic domain of the P-type ATPase has the haloacid dehalogenase fold. Trends Biochem Sci 1998; 23:127–129 [View Article] [PubMed]
    [Google Scholar]
  74. Lebrun M, Audurier A, Cossart P. Plasmid-borne cadmium resistance genes in Listeria monocytogenes are similar to cadA and cadC of Staphylococcus aureus and are induced by cadmium. J Bacteriol 1994; 176:3040–3048 [View Article] [PubMed]
    [Google Scholar]
  75. Parsons C, Lee S, Jayeola V, Kathariou S. Novel cadmium resistance determinant in Listeria monocytogenes. Appl Environ Microbiol 2017; 83:e02580-16 [View Article] [PubMed]
    [Google Scholar]
  76. Ducret V, Gonzalez MR, Leoni S, Valentini M, Perron K. The CzcCBA efflux system requires the CadA P-Type ATPase for timely expression upon zinc excess in Pseudomonas aeruginosa. Front Microbiol 2020; 11:911 [View Article] [PubMed]
    [Google Scholar]
  77. Zhang X-X, Rainey PB. The role of a P1-type ATPase from Pseudomonas fluorescens SBW25 in copper homeostasis and plant colonization. Mol Plant Microbe Interact 2007; 20:581–588 [View Article] [PubMed]
    [Google Scholar]
  78. Liang J, Zhang M, Lu M, Li Z, Shen X et al. Functional characterization of a csoR-cueA divergon in Bradyrhizobium liaoningense CCNWSX0360, involved in copper, zinc and cadmium cotolerance. Sci Rep 2016; 6:35155 [View Article] [PubMed]
    [Google Scholar]
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