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Halotolerant Bacillus Species as Plant Growth Promoting Rhizobacteria from Hyper – Arid Area of Algeria

Year 2024, Volume: 30 Issue: 2, 400 - 412, 26.03.2024
https://doi.org/10.15832/ankutbd.1249228

Abstract

The aim of this study was to determine the diversity of aerobic halotolerant Bacillus plant growth promoting rhizobacteria (PGPR), their production of hydrolytic exo-enzymes and their inoculation effect on two cowpea plants. The soil dilution plate technique was performed on tryptic soy agar complemented with thermal pretreatment to select Bacillus strains associated with the Phoenix dactylifera rhizosphere growing in hypersaline and arid soil in Algeria (In Salah, Tamanrasset). The inoculation effect of these strains on cowpea plant growth was assessed based on biometric and physiological parameters. As a result, thirteen halophilic, halotolerant and non-halophilic Bacillus strains were isolated. Upon screening, all strains were capable of producing at least two hydrolytic enzymes under saline conditions and most of the strains (n=10/13) showed at least two plant growth promoting (PGP) traits. Strains were identified as members of Bacillus genera based on their phenotypic and biochemical characteristics. The inoculation of these strains in cowpeas significantly improved biometrics and physiological growth parameters of the inoculated plants. Based on their PGP effects, five strains were identified: RP 7 (B. coagulans), RP 8 (B. circulans), RP 10 (Paenibacillus polymyxa), RP 12 (B. circulans) and RP 13 (B. cereus). The isolation and characterization of halophilic and halotolerant Bacillus strains increased knowledge about the microflora in the rhizosphere associated with date palms in saline and arid soils. Bacillus-PGPR strains proved to be highly effective to improve cowpea plant growth and development.

References

  • Aida B, Sihem T, Ines B & Hatem L (2021). Biochemical variability and functional properties of cowpea landraces grown in Hoggar: The Algerian arid region. Journal of Food Measurements 15:3509–3522. https://doi.org/10.1007/s11694-021-00919-5
  • Arora N K, Fatima T, Mishra J, Mishra I, Verma S, Verma R, Bhattacharyaa A, Vermaa P, Mishra P & Bharti C (2020). Halo-tolerant plant growth promoting rhizobacteria for improving productivity and remediation of saline soils. Journal of Advanced Research 26: 69-82. https://doi.org/10.1016/j.jare.2020.07.003
  • Atlas R M (2010). Handbook of Microbiological Media. 4th ed. Taylor & Francais Group, UK. https://doi.org/10.1201/9781420039726
  • Barrs H (1968). Determination of water deficit in plant tissues. In: Kozlowski TT, editor. Water deficit and plant growth. Vol.1. New York : Academic Press; pp. 235–368
  • Benaissa A (2019). Plant growth promoting rhizobacteria a review. Algerian Journal of Environmental Sciences and Technology 5(1): 873-880. https://www.aljest.net/index.php/aljest/article/view/39
  • Benaissa A, Djebbar R & Abderrahmani A (2018). Diversity and physiological properties of plant growth promoting rhizobacteria of Rhus tripartitus Rhizosphere from Ahaggar (Algeria). Advances in Horticultural Sciences 32(4): 525-534. https://doi.org/10.13128/ahs-22424
  • Castro-Escarpulli G, Figueras V, Aguilera-Arreola G, Soler L, Fernández-Rendón E, Aparicio G O, Guarro J & Chacon M R. (2003). Characterisation of Aeromonas spp. isolated from frozen fish intended for human consumption in Mexico. International Journal of Food Microbiology 84(1): 41-49.
  • https://doi.org/10.1016/S0168-1605(02)00393-8 Das P P, Singh K R, Nagpure G, Mansoori A, Singh R P, Ghazi I A, Anirudh K & Singh J (2022). Plant-soil-microbes: A tripartite interaction for nutrient acquisition and better plant growth for sustainable agricultural practices. Environmental Research 214: 113821. https://doi.org/10.1016/j.envres.2022.113821
  • Delarras C (2007). Microbiologie pratique pour le laboratoire d’analyses ou de contrôle sanitaire. Edition Tec & Doc, Lavoisier, Paris, France. 476 pp
  • Delarras C (2014). Pratique en microbiologie de laboratoire. Recherche de bactéries et de levures-moisissures. Tec & Doc. Poiteaux C, Lavoisier, Paris 978 pp
  • de Lourdes Moreno M, Pérez D, García M T, Mellado E (2013) Halophilic bacteria as a source of novel hydrolytic enzymes. Life 3(1): 38-51. https://doi.org/10.3390/life3010038
  • Egamberdiyeva D & Höflich G (2004). Effect of plant growth-promoting bacteria on growth and nutrient uptake of cotton and pea in a semi-arid region of Uzbekistan. Journal of Arid Environments 56(2): 293-301. https://doi.org/10.1016/S0140-1963(03)00050-8
  • FAO (2006). World reference base for soil resources—a framework for international classification, correlation and communication, Rome. 97p. https://www.fao.org/3/a0510e/A0510E.pdf
  • Han H & Lee K (2005). Plant growth promoting rhizobacteria effect on antioxidant status, photosynthesis, mineral uptake and growth of lettuce under soil salinity. Research Journal of Agriculture and Biological Sciences 1(3): 210-215
  • Hussain A, Ahmad M, Nafees M, Iqbal Z, Luqman M, Jamil M, Maqsood A, Mora-Poblete F, Ahmar S, Chen JT, Alyemeni MN & Ahmad P (2020). Plant-growth-promoting Bacillus and Paenibacillus species improve the nutritional status of Triticum aestivum L. Plos one 15(12): e0241130. https://doi.org/10.1371/journal.pone.0241130 Ibekwe A M, Poss J A, Grattan S R, Grieve C M & Uarez D S (2010). Bacterial diversity in cucumber (Cucumis sativus) rhizosphere in response to salinity, soil pH, and boron. Soil Biology and Biochemistry 42(4): 567-575. https://doi.org/10.1016/j.soilbio.2009.11.033
  • Jiang H, Qi P, Wang T, Wang M, Chen M, Chen N, Pan L & Chi X (2018). Isolation and characterization of halotolerant phosphate-solubilizing microorganisms from saline soils. 3 Biotech 8(11):461. https://doi.org/10.1007/s13205-018-1485-7.
  • Kashyap B K, Solanki M K, Pandey A K, Prabha S, Kumar P & Kumari B (2019). Bacillus as plant growth promoting rhizobacteria (PGPR): a promising green agriculture technology. In Plant health under biotic stress (pp. 219-236). Springer, Singapore. https://doi.org/10.1007/978-981-13-6040-4_11
  • Kloepper J W & Beauchamp C J (1992). A review of issues related to measuring colonization of plant roots by bacteria. Canadian Journal of Microbiology 38(12): 1219-1232. https://doi.org/10.1139/m92-202
  • Kushner D J (1978). Life in high salt and solute concentrations: halophilic bacteria. In Microbial Life in Extreme Environments, pp. 317–368. Edited by D. J. Kushner. London: Academic Press.
  • Lesel R, Fromageot C & Lesel M (1986). Cellulose digestibility in grass carp, Ctenopharyngodon idella and in goldfish, Carassius auratus. Aquaculture 54(1-2):11-17. https://doi.org/10.1016/0044-8486(86)90249-8
  • Li Y, Xu S, Gao J, Pan S & Wang G (2016). Bacillus subtilis-regulation of stomatal movement and instantaneous water use efficiency in Vicia faba. Journal of Plant Growth Regulation 78:43–55. https://doi.org/10.1007/s10725-015-0073-7
  • Lichtenthaler H K (1987). Chlorophylls and carotenoids: pigments of photosynthetic biomembranes. In Methods in enzymology. Academic Press 148: 350-382. https://doi.org/10.1016/0076-6879(87)48036-1
  • Lima D, Coelho B, Lima Moro A, Santos A C P, Bonifacio A, Araujo A S F & de Araujo F F (2019). Bacillus subtilis ameliorates water stress tolerance in maize and common bean. Journal of Plant Interactions 14(1): 432-439. https://doi.org/10.1080/17429145.2019.1645896
  • Lorck H (1948). Production of hydrocyanic acid by bacteria. Physiologia Plantarum 1(2): 142-146. https://doi.org/10.1111/j.1399-3054.1948.tb07118.x
  • Mahdi I, Fahsi N, Hafidi M, Allaoui A & Biskri L (2020). Plant growth enhancement using rhizospheric halotolerant phosphate solubilizing bacterium Bacillus licheniformis QA1 and Enterobacter asburiae QF11 isolated from Chenopodium quinoa willd. Microorganisms 8(6): 948. https://doi.org/10.3390/microorganisms8060948
  • Mapelli F, Marasco R, Rolli E, Barbato M, Cherif H, Guesmi A, Ouzari I, Daffonchio D & Borin S (2013). Potential for plant growth promotion of rhizobacteria associated with Salicornia growing in Tunisian hypersaline soils. BioMed Research International 1-13. https://doi.org/10.1155/2013/248078
  • Mathieu C & Pieltain F (1998) Analyses physiques des sols : Méthodes choisies. Lavoisier Tec et Doc, Paris 265p. https://www.documentation.ird.fr/hor/fdi:010015707 Mathieu C & Pieltain F (2003). Analyses physiques des sols : Méthodes choisies. Lavoisier Tec et Doc, Paris, 388 pp
  • Mukhtar S, Zareen M, Khaliq Z, Mehnaz S & Malik KA (2020). Phylogenetic analysis of halophyte‐associated rhizobacteria and effect of halotolerant and halophilic phosphate‐solubilizing biofertilizers on maize growth under salinity stress conditions. Journal of Applied Microbiology 128(2): 556-573. https://doi.org/10.1111/jam.14497
  • Nautiyal C S (1999). An efficient microbiological growth medium for screening phosphate solubilizing microorganisms. FEMS Microbiological Letters 170(1):265-270. https://doi.org/10.1111/j.1574-6968.1999.tb13383.x
  • Shivanand P & Mugeraya G (2011). Halophilic bacteria and their compatible solutes–osmoregulation and potential applications. Current Science 100(10):1516–1521. http://www.jstor.org/stable/24076671
  • Ventosa A, Nieto J J & Oren A (1998). Biology of moderately halophilic aerobic bacteria. Microbiology and Molecular Biology Reviews 62(2):504-544. https://doi.org/10.1128/MMBR.62.2.504-544.1998
  • Weisser J & Truper H G (1985). Osmoregulation in a new haloalkaliphilic Bacillus from the Wadi Natrun (Egypt). Systematic and Applied Microbiology 6(1):7-11. https://doi.org/10.1016/S0723-2020(85)80003-5
  • Yasin N A, Akram W, Khan W U, Ahmad S R, Ahmad A (2018). A Halotolerant plant-growth promoting rhizobacteria modulate gene expression and osmolyte production to improve salinity tolerance and growth in Capsicum annum L Environmental Science and Pollution Research 25(23): 23236-23250 https://doi.org/10.1007/s11356-018-2381-8
  • Zafar-ul-Hye M, Danish S, Abbas M, Ahmad M, Munir T M (2019). ACC deaminase producing PGPR Bacillus amyloliquefaciens and Agrobacterium fabrum along with biochar improve wheat productivity under drought stress. Agronomy 9(7):343. https://doi.org/10.3390/agronomy9070343
  • Zahran H (1997). Diversity adaptation and activity of the bacterial flora in saline environments. Biology and Fertility of Soils 25(3): 211-223. https://doi.org/10.1007/s003740050306
Year 2024, Volume: 30 Issue: 2, 400 - 412, 26.03.2024
https://doi.org/10.15832/ankutbd.1249228

Abstract

References

  • Aida B, Sihem T, Ines B & Hatem L (2021). Biochemical variability and functional properties of cowpea landraces grown in Hoggar: The Algerian arid region. Journal of Food Measurements 15:3509–3522. https://doi.org/10.1007/s11694-021-00919-5
  • Arora N K, Fatima T, Mishra J, Mishra I, Verma S, Verma R, Bhattacharyaa A, Vermaa P, Mishra P & Bharti C (2020). Halo-tolerant plant growth promoting rhizobacteria for improving productivity and remediation of saline soils. Journal of Advanced Research 26: 69-82. https://doi.org/10.1016/j.jare.2020.07.003
  • Atlas R M (2010). Handbook of Microbiological Media. 4th ed. Taylor & Francais Group, UK. https://doi.org/10.1201/9781420039726
  • Barrs H (1968). Determination of water deficit in plant tissues. In: Kozlowski TT, editor. Water deficit and plant growth. Vol.1. New York : Academic Press; pp. 235–368
  • Benaissa A (2019). Plant growth promoting rhizobacteria a review. Algerian Journal of Environmental Sciences and Technology 5(1): 873-880. https://www.aljest.net/index.php/aljest/article/view/39
  • Benaissa A, Djebbar R & Abderrahmani A (2018). Diversity and physiological properties of plant growth promoting rhizobacteria of Rhus tripartitus Rhizosphere from Ahaggar (Algeria). Advances in Horticultural Sciences 32(4): 525-534. https://doi.org/10.13128/ahs-22424
  • Castro-Escarpulli G, Figueras V, Aguilera-Arreola G, Soler L, Fernández-Rendón E, Aparicio G O, Guarro J & Chacon M R. (2003). Characterisation of Aeromonas spp. isolated from frozen fish intended for human consumption in Mexico. International Journal of Food Microbiology 84(1): 41-49.
  • https://doi.org/10.1016/S0168-1605(02)00393-8 Das P P, Singh K R, Nagpure G, Mansoori A, Singh R P, Ghazi I A, Anirudh K & Singh J (2022). Plant-soil-microbes: A tripartite interaction for nutrient acquisition and better plant growth for sustainable agricultural practices. Environmental Research 214: 113821. https://doi.org/10.1016/j.envres.2022.113821
  • Delarras C (2007). Microbiologie pratique pour le laboratoire d’analyses ou de contrôle sanitaire. Edition Tec & Doc, Lavoisier, Paris, France. 476 pp
  • Delarras C (2014). Pratique en microbiologie de laboratoire. Recherche de bactéries et de levures-moisissures. Tec & Doc. Poiteaux C, Lavoisier, Paris 978 pp
  • de Lourdes Moreno M, Pérez D, García M T, Mellado E (2013) Halophilic bacteria as a source of novel hydrolytic enzymes. Life 3(1): 38-51. https://doi.org/10.3390/life3010038
  • Egamberdiyeva D & Höflich G (2004). Effect of plant growth-promoting bacteria on growth and nutrient uptake of cotton and pea in a semi-arid region of Uzbekistan. Journal of Arid Environments 56(2): 293-301. https://doi.org/10.1016/S0140-1963(03)00050-8
  • FAO (2006). World reference base for soil resources—a framework for international classification, correlation and communication, Rome. 97p. https://www.fao.org/3/a0510e/A0510E.pdf
  • Han H & Lee K (2005). Plant growth promoting rhizobacteria effect on antioxidant status, photosynthesis, mineral uptake and growth of lettuce under soil salinity. Research Journal of Agriculture and Biological Sciences 1(3): 210-215
  • Hussain A, Ahmad M, Nafees M, Iqbal Z, Luqman M, Jamil M, Maqsood A, Mora-Poblete F, Ahmar S, Chen JT, Alyemeni MN & Ahmad P (2020). Plant-growth-promoting Bacillus and Paenibacillus species improve the nutritional status of Triticum aestivum L. Plos one 15(12): e0241130. https://doi.org/10.1371/journal.pone.0241130 Ibekwe A M, Poss J A, Grattan S R, Grieve C M & Uarez D S (2010). Bacterial diversity in cucumber (Cucumis sativus) rhizosphere in response to salinity, soil pH, and boron. Soil Biology and Biochemistry 42(4): 567-575. https://doi.org/10.1016/j.soilbio.2009.11.033
  • Jiang H, Qi P, Wang T, Wang M, Chen M, Chen N, Pan L & Chi X (2018). Isolation and characterization of halotolerant phosphate-solubilizing microorganisms from saline soils. 3 Biotech 8(11):461. https://doi.org/10.1007/s13205-018-1485-7.
  • Kashyap B K, Solanki M K, Pandey A K, Prabha S, Kumar P & Kumari B (2019). Bacillus as plant growth promoting rhizobacteria (PGPR): a promising green agriculture technology. In Plant health under biotic stress (pp. 219-236). Springer, Singapore. https://doi.org/10.1007/978-981-13-6040-4_11
  • Kloepper J W & Beauchamp C J (1992). A review of issues related to measuring colonization of plant roots by bacteria. Canadian Journal of Microbiology 38(12): 1219-1232. https://doi.org/10.1139/m92-202
  • Kushner D J (1978). Life in high salt and solute concentrations: halophilic bacteria. In Microbial Life in Extreme Environments, pp. 317–368. Edited by D. J. Kushner. London: Academic Press.
  • Lesel R, Fromageot C & Lesel M (1986). Cellulose digestibility in grass carp, Ctenopharyngodon idella and in goldfish, Carassius auratus. Aquaculture 54(1-2):11-17. https://doi.org/10.1016/0044-8486(86)90249-8
  • Li Y, Xu S, Gao J, Pan S & Wang G (2016). Bacillus subtilis-regulation of stomatal movement and instantaneous water use efficiency in Vicia faba. Journal of Plant Growth Regulation 78:43–55. https://doi.org/10.1007/s10725-015-0073-7
  • Lichtenthaler H K (1987). Chlorophylls and carotenoids: pigments of photosynthetic biomembranes. In Methods in enzymology. Academic Press 148: 350-382. https://doi.org/10.1016/0076-6879(87)48036-1
  • Lima D, Coelho B, Lima Moro A, Santos A C P, Bonifacio A, Araujo A S F & de Araujo F F (2019). Bacillus subtilis ameliorates water stress tolerance in maize and common bean. Journal of Plant Interactions 14(1): 432-439. https://doi.org/10.1080/17429145.2019.1645896
  • Lorck H (1948). Production of hydrocyanic acid by bacteria. Physiologia Plantarum 1(2): 142-146. https://doi.org/10.1111/j.1399-3054.1948.tb07118.x
  • Mahdi I, Fahsi N, Hafidi M, Allaoui A & Biskri L (2020). Plant growth enhancement using rhizospheric halotolerant phosphate solubilizing bacterium Bacillus licheniformis QA1 and Enterobacter asburiae QF11 isolated from Chenopodium quinoa willd. Microorganisms 8(6): 948. https://doi.org/10.3390/microorganisms8060948
  • Mapelli F, Marasco R, Rolli E, Barbato M, Cherif H, Guesmi A, Ouzari I, Daffonchio D & Borin S (2013). Potential for plant growth promotion of rhizobacteria associated with Salicornia growing in Tunisian hypersaline soils. BioMed Research International 1-13. https://doi.org/10.1155/2013/248078
  • Mathieu C & Pieltain F (1998) Analyses physiques des sols : Méthodes choisies. Lavoisier Tec et Doc, Paris 265p. https://www.documentation.ird.fr/hor/fdi:010015707 Mathieu C & Pieltain F (2003). Analyses physiques des sols : Méthodes choisies. Lavoisier Tec et Doc, Paris, 388 pp
  • Mukhtar S, Zareen M, Khaliq Z, Mehnaz S & Malik KA (2020). Phylogenetic analysis of halophyte‐associated rhizobacteria and effect of halotolerant and halophilic phosphate‐solubilizing biofertilizers on maize growth under salinity stress conditions. Journal of Applied Microbiology 128(2): 556-573. https://doi.org/10.1111/jam.14497
  • Nautiyal C S (1999). An efficient microbiological growth medium for screening phosphate solubilizing microorganisms. FEMS Microbiological Letters 170(1):265-270. https://doi.org/10.1111/j.1574-6968.1999.tb13383.x
  • Shivanand P & Mugeraya G (2011). Halophilic bacteria and their compatible solutes–osmoregulation and potential applications. Current Science 100(10):1516–1521. http://www.jstor.org/stable/24076671
  • Ventosa A, Nieto J J & Oren A (1998). Biology of moderately halophilic aerobic bacteria. Microbiology and Molecular Biology Reviews 62(2):504-544. https://doi.org/10.1128/MMBR.62.2.504-544.1998
  • Weisser J & Truper H G (1985). Osmoregulation in a new haloalkaliphilic Bacillus from the Wadi Natrun (Egypt). Systematic and Applied Microbiology 6(1):7-11. https://doi.org/10.1016/S0723-2020(85)80003-5
  • Yasin N A, Akram W, Khan W U, Ahmad S R, Ahmad A (2018). A Halotolerant plant-growth promoting rhizobacteria modulate gene expression and osmolyte production to improve salinity tolerance and growth in Capsicum annum L Environmental Science and Pollution Research 25(23): 23236-23250 https://doi.org/10.1007/s11356-018-2381-8
  • Zafar-ul-Hye M, Danish S, Abbas M, Ahmad M, Munir T M (2019). ACC deaminase producing PGPR Bacillus amyloliquefaciens and Agrobacterium fabrum along with biochar improve wheat productivity under drought stress. Agronomy 9(7):343. https://doi.org/10.3390/agronomy9070343
  • Zahran H (1997). Diversity adaptation and activity of the bacterial flora in saline environments. Biology and Fertility of Soils 25(3): 211-223. https://doi.org/10.1007/s003740050306
There are 35 citations in total.

Details

Primary Language English
Subjects Agricultural Engineering (Other)
Journal Section Makaleler
Authors

Asmaa Benaissa 0000-0003-1221-1887

Aida Basseddik 0000-0002-8903-8392

Abdallah Chegga This is me 0000-0003-0502-7408

Réda Djebbar This is me 0000-0003-3166-3299

Publication Date March 26, 2024
Submission Date February 8, 2023
Acceptance Date December 21, 2023
Published in Issue Year 2024 Volume: 30 Issue: 2

Cite

APA Benaissa, A., Basseddik, A., Chegga, A., Djebbar, R. (2024). Halotolerant Bacillus Species as Plant Growth Promoting Rhizobacteria from Hyper – Arid Area of Algeria. Journal of Agricultural Sciences, 30(2), 400-412. https://doi.org/10.15832/ankutbd.1249228

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