Comparative overview of red kidney bean (Phaseolus valgaris) rhizospheric bacterial diversity in perspective of altitudinal variations

Abstract

Red kidney bean (RKB) is an important cash crop of the Western Indian Himlayan (WIH) regions. Despite of having a long cultivation history, very little has known about its rhizospheric microbial diversity, which is becoming important for employing sustainable agricultural plans. In this perspective, the bacterial diversity and community structure of Himalayan RKB rhizosphere were studied and compared across the altitudinal zones of WIH. Metagenomic analysis revealed that Proteobacteria (31%) was the major phylum with the dominance of the genera Sphingomonas in the Garhwal while Pseudomonas in the Kumaun regions of Western Indian Himalaya (WIH), followed by Bacteroidetes (20%), Fermicutes (9%), Acidobacteria (7%), Actinobacteria (6%), Chloroflexi (5%), Gemmatimonadetes (3%) and Planctomyces (2%). Furthermore, the Garhwal soil was found to harbor more bacterial diversity than the Kumaun with unique genera Conexibacter, Ornithobacterium, Lacibacter, Salinibacter, Fervidicola, Haliangium, Pirellula, Caloramator, Desulfitobacterium, Edaphobacter, Holophaga and Massilia. The principal component analysis revealed that the bacterial diversity was associated with the content of “total solids” as well as “volatile acids” present in the respective soils. Additionally, large number of unclassified clone sequences suggesting the need of culture dependent studies to trap “yet not cultivated” bacterial species. Conclusively, the present study provides an overview of RKB associated bacterial diversity which must be explored for sustainable hill agricultural plans.

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References

  1. Arya R, Mishra AK, Chaudhry S (2018) Variation in soil properties and carbon stocks under roadside plantation and rice-wheat cropping system in north western Haryana, India. Int J Curr Microbiol App Sci 7(4):1939–1949. https://doi.org/10.20546/ijcmas.2018.704.222

    CAS  Article  Google Scholar 

  2. Cetecioglu Z, Ince BK, Kolukirik M, Ince O (2009) Biogeographical distribution and diversity of bacterial and archaeal communities within highly polluted anoxic marine sediments from the Marmara Sea. Mar Pollut Bull 58(3):384–395. https://doi.org/10.1016/j.marpolbul.2008.10.009

    CAS  Article  PubMed  Google Scholar 

  3. Chai ZY, He ZL, Deng YY, Yang YF, Tang YZ (2018) Cultivation of seaweed Gracilaria lemaneiformis enhanced biodiversity in a eukaryotic plankton community as revealed via metagenomic analyses. Mol Ecol 27(4):1081–1093. https://doi.org/10.1111/mec.14496

    Article  PubMed  Google Scholar 

  4. Debbarma P, Raghuwanshi S, Singh J, Suyal DC, Zaidi MGH, Goel R (2017) Comparative in situ biodegradation studies of polyhydroxybutyrate film composites. 3Biotech 7(178). https://doi.org/10.1007/s13205-017-0789-3

  5. Diaz-Alcantara CA, Ramirez-Bahena MH, Mulas D, Garcia- Fraile P, Gomez-Moriano A, Peix A, Velazquez E, Gonzalez-Andres F (2013) Analysis of rhizobial strains nodulating Phaseolus vulgaris from Hispaniola Island, a geographic bridge between Meso and South America and the first historical link with. Europe Syst Appl Microbiol 37:149–156. https://doi.org/10.1016/j.syapm.2013.09.005

    Article  PubMed  Google Scholar 

  6. Igiehon NO, Babalola OO (2018) Rhizosphere microbiome modulators: contributions of nitrogen fixing bacteria towards sustainable agriculture. Int J Environ Res Public Health 15(4):574. https://doi.org/10.3390/ijerph15040574

    CAS  Article  PubMed Central  Google Scholar 

  7. Jackson ML (1973) Soil chemical analysis. Prentice Hall of India Private Limited, New Delhi

    Google Scholar 

  8. Joshi D, Chandra R, Suyal DC, Kumar S, Goel R (2019) Impact of bioinoculants Pseudomonas jesenii MP1 and Rhodococcus qingshengii S10107 on Cicer arietinum yield and soil nitrogen status. Pedosphere. 29(3):388–399. https://doi.org/10.1016/S1002-0160(19)60807-6

    Article  Google Scholar 

  9. Kumar S, Suyal DC, Dhauni N, Bhoriyal M, Goel R (2014) Relative plant growth promoting potential of Himalayan psychrotolerant Pseudomonas jesenii strain MP1 against native Cicer arietinum L., Vigna mungo (L.) Hepper; Vigna radiata (L.) Wilczek., Cajanus cajan (L.) Millsp. and Eleusine coracana (L.) Gaertn. Afri J Microbiol 8(50):3931–3943. https://doi.org/10.5897/AJMR2014.7035

    Article  Google Scholar 

  10. Kumar S, Suyal DC, Yadav A, Shouche Y, Goel R (2019) Microbial diversity and soil physiochemical characteristic of higher altitude. PLoS One 14(3):e0213844. https://doi.org/10.1371/journal.pone.0213844

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  11. Olsen RA, Rhodes MB, Dreier AF (1954) Available phosphorus status of Nebraska soils in relation to series classification, time of sampling and method of measurement. Agron J 46:175–180

    Article  Google Scholar 

  12. Pradhan S, Srinivas TNR, Pindi PK, Kishore KH, Begum Z, Singh PK, Singh AK, Pratibha MS, Yasala AK, Reddy GS, Shivaji S (2010) Bacterial biodiversity from Roopkund glacier, Himalayan mountain ranges, India. Extremophiles 14:377–395. https://doi.org/10.1007/s00792-010-0318-3

    CAS  Article  PubMed  Google Scholar 

  13. Rajwar J, Chandra R, Suyal DC, Tomer S, Kumar S, Goel R (2018) Comparative phosphate solubilizing efficiency of psychrotolerant Pseudomonas jesenii MP1 and Acinetobacter sp. ST02 against chickpea for sustainable hill agriculture. Biologia 73(8):793–802. https://doi.org/10.2478/s11756-018-0089-3

    CAS  Article  Google Scholar 

  14. Ren B, Hu Y, Baodong C, Zhang Y, Thiele J, Shi R, Liu M, Bu R (2018) Soil pH and plant diversity shape soil bacterial community structure in the active layer across the latitudinal gradients in continuous permafrost region of northeastern China. Sci Rep 8(5619). https://doi.org/10.1038/s41598-018-24040-8

  15. Sanchez AC, Gutierrez RT, Santana RC, Urrutia AB, Fauvart M, Michiels J, Vanderleyden J (2014) Effects of coinoculation of native Rhizobium and Pseudomonas strains on growth parameters and yield of two contrasting Phaseolus vulgaris L. genotypes under Cuban soil conditions. Eur J Soil Biol 62:105–112. https://doi.org/10.1016/j.ejsobi.2014.03.004

    Article  Google Scholar 

  16. Shannon C (1948) A mathematical theory of communication. Bell Syst Tech J 27:379–423

    Article  Google Scholar 

  17. Shivaji S, Pratibha MS, Sailaja B, Kishore KH, Singh AK, Begum Z, Anarasi U, Prabagaran SR, Reddy GSN, Srinivas TNR (2011) Bacterial diversity of soil in the vicinity of Pindari glacier, Himalayan mountain ranges, India, using culturable bacteria and soil 16S rRNA gene clones. Extremophiles 15:1–22. https://doi.org/10.1007/s00792-010-0333-4

    CAS  Article  PubMed  Google Scholar 

  18. Simpson EH (1949) Measurement of diversity. Nature 163:688

    Article  Google Scholar 

  19. Singh P, Singh SS, Elster J, Mishra AK (2013) Molecular phylogeny, population genetics, and evolution of heterocystous cyanobacteria using nifH gene sequences. Protoplasma 250(3):751–764. https://doi.org/10.1007/s00709-012-0460-0

    Article  PubMed  Google Scholar 

  20. Soni R, Suyal DC, Agrawal K, Yadav A, Souche Y, Goel R (2015) Differential proteomic analysis of Himalayan psychrotolerant diazotroph Pseudomonas palleroniana N26 strain under low temperature diazotrophic conditions. CryoLetters 36(2):74–82

    PubMed  Google Scholar 

  21. Soni R, Suyal DC, Sai S, Goel R (2016) Exploration of nifH gene through soil metagenomes of the western Indian Himalayas. 3Biotech 6(1):1–4. https://doi.org/10.1007/s13205-015-0324-3

    Article  Google Scholar 

  22. Subbiah BV, Asija GL (1956) A rapid procedure for the estimation of nitrogen in soils. Curr Sci 25:259–260

    CAS  Google Scholar 

  23. Surakasi VP, Antony CP, Sharma S, Patole MS, Shouche YS (2010) Temporal bacterial diversity and detection of putative methanotrophs in surface mats of Lonar crater lake. J Basic Microbiol 50:465–474. https://doi.org/10.1002/jobm.201000001

    CAS  Article  PubMed  Google Scholar 

  24. Suyal DC, Yadav A, Shouche Y, Goel R (2014) Differential proteomics in response to low temperature diazotrophy of Himalayan psychrophilic nitrogen fixing Pseudomonas migulae S10724 strain. Curr Microbiol 68:543–550. https://doi.org/10.1007/s00284-013-0508-1

    CAS  Article  PubMed  Google Scholar 

  25. Suyal DC, Yadav A, Shouche Y, Goel R (2015a) Diversified diazotrophs associated with the rhizosphere of Western Indian Himalayan native red kidney beans (Phaseolus vulgaris L.). 3Biotech 5:433–441. https://doi.org/10.1007/s13205-014-0238-5

    Article  Google Scholar 

  26. Suyal DC, Yadav A, Shouche Y, Goel R (2015b) Bacterial diversity and community structure of Western Indian Himalayan red kidney bean (Phaseolus vulgaris L.) rhizosphere as revealed by 16S rRNA gene sequences. Biologia 70(3):305–313. https://doi.org/10.1515/biolog-2015-0048

    CAS  Article  Google Scholar 

  27. Suyal DC, Kumar S, Yadav A, Shouche Y, Goel R (2017) Cold stress and nitrogen deficiency affected protein expression of psychrotrophic Dyadobacter psychrophilus B2 and Pseudomonas jessenii MP1. Front Microbiol 8(430):1–6. https://doi.org/10.3389/fmicb.2017.00430

    Article  Google Scholar 

  28. Suyal DC, Kumar S, Joshi D, Soni R, Goel R (2018) Quantitative proteomics of psychotrophic diazotroph in response to nitrogen deficiency and cold stress. J Proteome 187:235–242. https://doi.org/10.1016/j.jprot.2018.08.005

    CAS  Article  Google Scholar 

  29. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739. https://doi.org/10.1093/molbev/msr121

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  30. Tomer S, Suyal DC, Rajwar J, Yadav A, Shouche Y, Goel R (2017) Isolation and characterization of phosphate solubilizing bacteria from Western Indian Himalayan soils. 3Biotech 7(2):95. https://doi.org/10.1007/s13205-017-0738-1

    Article  Google Scholar 

  31. Wei Y, Zhao Y, Xi B, Wei Z, Li X, Cao Z (2015) Changes in phosphorus fractions during organic wastes composting from different sources. Bioresour Technol 189:349–356. https://doi.org/10.1016/j.biortech.2015.04.031

    CAS  Article  PubMed  Google Scholar 

  32. Wei Y, Wei Z, Cao Z, Zhao Y, Zhao X, Lu Q, Wang X, Zhang X (2016) A regulating method for the distribution of phosphorus fractions based on environmental parameters related to the key phosphate-solubilizing bacteria during composting. Bioresour Technol 211:610–617. https://doi.org/10.1016/j.biortech.2016.03.141

    CAS  Article  PubMed  Google Scholar 

  33. Williams CH (1980) Soil acidification under clover pasture. Austr J Exp Agri Ani Husb 20(106):561–567

    Article  Google Scholar 

Download references

Acknowledgements

The author (DCS) acknowledges the Science and Engineering Research Board (SERB) young scientist scheme, Grant No. YSS/2015/001214 during the course of this study. Also Senior Research Fellowship (CSIR Award No: 09/171(0126)/2015-EMR-I) to SK is acknowledged. Dr. Prabha Pant, Assistant professor, Department of Humanities & Social Sciences, GBPUAT Pantnagar is duly acknowledged for manuscript editing and improvement.

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Correspondence to Reeta Goel.

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Suyal, D.C., Kumar, S., Joshi, D. et al. Comparative overview of red kidney bean (Phaseolus valgaris) rhizospheric bacterial diversity in perspective of altitudinal variations. Biologia 74, 1405–1413 (2019). https://doi.org/10.2478/s11756-019-00292-1

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Keywords

  • Red kidney bean
  • Himalayan agro-ecosystems
  • 16S rDNA
  • Bacterial diversity
  • Rhizosphere