Isolation and characterisation of sulfur-oxidising bacteria, including strains of Rhizobium, from calcareous sandy soils and their effects on nutrient uptake and growth of maize (Zea mays L.)
Khaled A. El-Tarabily A D , Abdou A. Soaud B , Maher E. Saleh B and Satoshi Matsumoto CA Department of Biology, Faculty of Science, United Arab Emirates University, Al-Ain 17551, United Arab Emirates.
B Department of Aridland Agriculture, Faculty of Food Systems, United Arab Emirates University, Al-Ain 17555, United Arab Emirates.
C Faculty of Bioresources Science, Akita Prefectural University, Akita 010-0195, Japan.
D Corresponding author. Email: ktarabily@uaeu.ac.ae
Australian Journal of Agricultural Research 57(1) 101-111 https://doi.org/10.1071/AR04237
Submitted: 14 October 2004 Accepted: 30 August 2005 Published: 30 January 2006
Abstract
Four sulfur-oxidising bacteria were selected among 427 bacterial isolates from calcareous sandy soils in the United Arab Emirates (UAE). These isolates were selected based on their strong ability to oxidise elemental sulfur (S°) in vitro and were identified as Paracoccus versutus CBS 114155, Paracoccus pantotrophus CBS 114154, and 2 strains as Rhizobium spp. NCCB 100053 and NCCB 100054. This is the first published report of a Rhizobium species capable of S° oxidation and also the first record of sulfur-oxidising bacteria from UAE soils. These isolates were tested in a greenhouse in the presence and absence of S° to study their effects on maize growth. Best growth was observed in the treatment with P. versutus application combined with S°, which significantly reduced soil pH, increased soil SO4 level and the uptake of N, S, Fe, Mn, and Zn in maize roots and shoots. The P and Cu uptake in the shoots of maize plants was not significant compared with the treatment that received the application of S° alone. There was no response in plant growth to treatments that included the application of S° combined with P. pantotrophus or Rhizobium strain NCCB 100053 compared with the treatment that received the application of S° alone. There was significant growth inhibition of maize plants in the treatment receiving Rhizobium strain NCCB 100054 with or without the application of S° compared with the treatment that included the application of S° alone. This growth inhibition was associated with a significant decrease in the levels of N, P, S, Fe, Mn, Zn, and Cu in roots and shoots in the absence of S°. Rhizobium strain NCCB 100054 applied with S° significantly decreased the levels of N, S, and Fe in the roots and the levels of N, P, S, Fe, Mn, and Cu in the shoots of maize, with no significant differences in the levels of P and Mn in the roots and in the levels of Zn in the shoots, compared with the treatment with S° alone. These results indicate that the treatment P. versutus combined with S° can be effective as a soil conditioner for horticultural production in calcareous sandy soils.
Additional keywords: arid lands, calcareous soils, elemental sulfur, sulfur-oxidation, United Arab Emirates.
Acknowledgments
This research was part of the project on ‘Using Sulfur By-Product from Gas Production Plants for Increasing Crop Productivity in Calcareous Sandy Soils’ (JCCP Research A), supported by the Japan Cooperation Center, Petroleum (JCCP). The authors thank M. Abdel-Wahab for sample collection, and field staff at the United Arab Emirates University for valuable assistance.
Abd-Elfattah A, Saber MS, Hilal M
(1992) The use of Thiobacillus in regulating the metabolism in a clay loam soil supplemented with elemental sulfur. ‘Proceedings Middle East Sulphur Symposium’. Cairo, Egypt. (The Sulphur Institute: Washington, DC)
Abu Dhabi National Oil Company (ADNOC) (2001).
Afif E,
Matar A, Torrent J
(1993) Availability of phosphate applied to calcareous soils of West Asia and North Africa. Soil Science Society of America Journal 57, 756–760.
Bardischewsky F, Friedrich CG
(2001) The shxVW locus is essential for oxidation of inorganic sulfur and molecular hydrogen by Paracoccus pantotrophus GB17: a novel function for lithotrophy. FEMS Microbiology Letters 202, 215–220.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Besharaty H, Khavazi K, Saleh-Rastin N
(2001) Evaluation of some carriers for Thiobacillus inoculants used along with sulphur to increase uptake of some nutrients by corn and improve its performance. ‘Plant nutrition: food security and sustainability of agro-ecosystems through basic and applied research. 14th International Plant Nutrition Colloquium’. Hanover, Germany. (Ed. WJ Horst ,
MK Schenk ,
A Burkert ,
N Claassen ,
H Flessa ,
WB Frommer ,
H Goldbach ,
HW Olfs ,
V Romheld )
pp. 672–673. (Kluwer Academic Publishers: Dordrecht, The Netherlands)
Boras IJ
(1968) Reclamation of alkali soils in Armenian S.S.R. Agrokemia es Talajtan 17, 343–354.
Brady, NC ,
and
Weil, RR (1998).
Burns GR
(1984) Oxidation of sulphur in soils. The Sulphur Institute Technical Bulletin, No.13.
Chapman SJ
(1990) Thiobacillus populations in some agricultural soils. Soil Biology and Biochemistry 22, 479–482.
| Crossref | GoogleScholarGoogle Scholar |
El-Fayoumy ME, El-Gamal AM
(1998) Effects of sulfur application rates on nutrients availability, uptake and potato quality and yield in calcareous soil. Egyptian Journal of Soil Science 38, 271–286.
El-Tarabily KA, Soaud AA, Al-Darwish FH, Saleh ME
(2004) Using sulfur by-product from gas production plants for increasing crop productivity in calcareous sandy soils: selection of a suitable carrier for the sulfur-oxidizing bacterial inoculants. ‘The 5th Annual Research Conference, UAE University’. Al-Ain, United Arab Emirates. (United Arab Emirates University Press: Al-Ain, UAE)
Germida JJ
(1985) Modified sulfur containing media for studying sulfur-oxidizing microorganisms. ‘Planetary ecology’. (Eds DE Caldwell, JA Brierley, CL Brierley)
pp. 333–344. (Van Nostrand Reinhold: New York)
Germida JJ, Janzen HH
(1993) Factors affecting the oxidation of elemental sulfur in soils. Fertilizer Research 35, 101–114.
| Crossref | GoogleScholarGoogle Scholar |
Grayston SJ, Germida JJ
(1990) Influence of crop rhizospheres on populations and activity of heterotrophic sulfur-oxidizing microorganisms. Soil Biology and Biochemistry 22, 457–463.
| Crossref | GoogleScholarGoogle Scholar |
Grayston SJ, Germida JJ
(1991) Sulfur-oxidizing bacteria as plant growth promoting rhizobacteria for canola. Canadian Journal of Microbiology 37, 521–529.
Gupta RK, Abrol IP
(1990) Salt affected soils: their reclamation and management for crop production. Advances in Soil Science 11, 223–288.
Gupta VVSR,
Lawrence JR, Germida JJ
(1988) Impact of elemental sulfur fertilization on agricultural soils. I. Effects on microbial biomass and enzyme activities. Canadian Journal of Soil Science 68, 463–473.
Jones JB, Case VW
(1990) Sampling, handling and analyzing plant tissue samples. ‘Soil testing and plant analysis’. (Ed. RL Westerman)
pp. 389–427. (Soil Science Society of America: Madison, WI)
Katayama Y,
Hiraishi A, Kuraishi H
(1995) Paracoccus thiocyanatus sp. nov., a new species of thiocyanate-utilizing facultative chemolithotroph, and transfer of Thiobacillus versutus to the genus Paracoccus as Paracoccus versutus comb. nov. with emendation of the genus. Microbiology 141, 1469–1477.
| PubMed |
Kelly P
(1989) Physiology and biochemistry of unicellular sulfur bacteria. ‘Autotrophic bacteria’. (Eds HG Schlegal, B Bowien)
pp. 193–217. (Springer-Verlag: Berlin, Germany)
Kovda VA
(1965) Alkaline soda-saline soils. Agrokemia es Talajtan 14, 15–48.
Kuenen JG,
Robertson LA, van Gemerden H
(1985) Microbial interactions among aerobic and anaerobic sulfur-oxidizing bacteria. Advances in Microbial Ecology 8, 1–59.
Kuenen JG, Robertson LA, Tuovinen OH
(1992) The Genera Thiobacillus, Thiomicrospira and Thiosphaera. ‘The Prokaryotes. A handbook on the biology of bacteria. Ecophysiology, isolation, identification, and application’. (Eds A Balows, HG Truper, M Dworkin, W Harder, K Schileifer)
pp. 2638–2657. (Springer-Verlag: Berlin, Germany)
Kuo S
(1996) Phosphorus. ‘Methods of soil analysis’. (Ed. DL Sparks)
pp. 869–919. (Soil Science Society of America: Madison, WI)
Lawrence JR, Germida JJ
(1991) Enumeration of sulfur-oxidizing populations in Saskatchewan agricultural soils. Canadian Journal of Soil Science 71, 127–136.
Lawrence JR,
Gupta VV, Germida JJ
(1988) Impact of elemental sulfur fertilization on agricultural soils. II. Effects on sulfur-oxidizing populations and oxidation rates. Canadian Journal of Soil Science 68, 475–483.
Lee A,
Watkinson JH, Lauren DR
(1988) Factors affecting oxidation rates of elemental sulfur in a soil under a ryegrass dominant sward. Soil Biology and Biochemistry 20, 809–816.
| Crossref | GoogleScholarGoogle Scholar |
Lindemann WC,
Aburto JJ,
Haffner WM, Bono AA
(1991) Effect of sulfur source on sulfur oxidation. Soil Science Society of America Journal 55, 85–90.
Lindsay, WL (1979).
Lopez-Aguirre JG,
Farias-Larios J,
Guzman-Gonzalez S,
Michel-Rosales A, de Freitas JR
(1999) Effect of sulfur application on chemical properties and microbial populations in a tropical alkaline soil. Pedobiologia 43, 183–191.
Lynch, JM (1990).
Mahler RJ, Maples RL
(1987) Effect of sulfur additions on soil and the nutrition of wheat. Communications in Soil Science and Plant Analysis 18, 653–673.
Maynard DG,
Germida JJ, Addison PA
(1986) The effect of elemental sulfur on certain chemical and biological properties of surface organic horizons of a forest soil. Canadian Journal of Forest Research 16, 1050–1054.
McCready RG, Krouse HR
(1982) Sulfur isotope fractionation during the oxidation of elemental sulfur by thiobacilli in solonetzic soil. Canadian Journal of Soil Science 62, 105–110.
Modaihsh AS,
Al-Mustafa WA, Metwally AI
(1989) Effect of elemental sulphur on chemical changes and nutrient availability in calcareous soils. Plant and Soil 116, 95–101.
Mortvedt, JJ ,
Murphy, LS ,
and
Follet, RH (1999).
Munsinger RA, McKinney R
(1982) Modern Kjeldahl system. American Labs 14, 76–79.
Neilsen D,
Hogue EJ,
Hoyt PB, Drought BG
(1993) Oxidation of elemental sulphur and acidulation of calcareous orchard soils in southern British Columbia. Canadian Journal of Soil Science 73, 103–114.
Rainey FA,
Kelly DP,
Stackebrandt E,
Burghardt J,
Hiraishi A,
Katayama Y, Wood A
(1999) A re-evaluation of the taxonomy of Paracoccus denitrificans and a proposal for the combination Paracoccus pantotrophus comb. nov. International Journal of Systematic Bacteriology 49, 645–651.
| PubMed |
Santini JM,
Lindsay IS,
Schnagl RD, Macy JM
(2000) A new chemolithoautotrophic arsenite-oxidizing bacterium isolated from a gold mine: phylogenetic, physiological, and preliminary biochemical studies. Applied and Environmental Microbiology 66, 92–97.
| PubMed |
Satchell JE
(1978) Ecology and environment in the United Arab Emirates. Journal of Arid Environments 1, 201–226.
Scott NM,
Dyson PW,
Ross J, Sharp GS
(1984) The effect of sulphur on the yield and chemical composition of winter barely. Journal of Agricultural Science 103, 699–702.
Sharma P, Swarup A
(1997) Comparison of pyrites varying in water-soluble sulfur with gypsum for the reclamation of alkali soils under a rice-wheat rotation. Biology and Fertility of Soils 24, 96–101.
| Crossref | GoogleScholarGoogle Scholar |
Shata SM, Selim AM, Abdel-Fattah A
(1992) Growth response of corn and wheat to sulfur-oxidizing bacteria under certain soil and irrigation conditions. ‘Proceedings Middle East Sulphur Symposium’. Cairo, Egypt. (The Sulphur Institute: Washington, DC)
Shinde DB,
Patil PL, Patil BR
(1996) Potential use of sulphur-oxidizing microorganisms as soil inoculant. Crop Research 11, 291–295.
Soaud AA, Saleh ME, El-Tarabily KA, Al-Darwish FH
(2004) Using sulfur by-product from gas production plants for increasing crop productivity in calcareous sandy soils: Effect of elemental sulfur application to UAE soils on ammonia volatilization. ‘The 5th Annual Research Conference, UAE University’. Al-Ain, United Arab Emirates. (United Arab Emirates University Press: Al-Ain, UAE)
Stamford NP,
Freitas AD,
Ferraz DS, Santos CE
(2002) Effect of sulphur inoculated with Thiobacillus on saline soils amendment and growth of cowpea and yam bean legumes. Journal of Agricultural Science 139, 275–281.
| Crossref | GoogleScholarGoogle Scholar |
Starkey R
(1935) Isolation of some bacteria which oxidize thiosulfate. Soil Science 39, 197–219.
Wainwright M
(1984) Sulfur oxidation in soils. Advances in Agronomy 37, 349–396.
Wainwright M,
Nevell W, Grayston SJ
(1986) Effects of organic matter on sulphur oxidation in soil and influence of sulphur oxidation on soil nitrification. Plant and Soil 96, 369–376.
Wellington EMH, Williams ST
(1978) Preservation of actinomycete inoculum in frozen glycerol. Microbios Letters 6, 151–157.
Wiezler F
(1998) Comparative assessment of the efficacy of various nitrogen fertilizers. ‘Nutrient use in crop production’. (Ed. Z Rengel)
pp. 81–114. (Food Products Press: Binghampton, NY)
Wlodarczyk M, Jadwig B
(1997) Genetic analysis of Paracoccus/Thiobacillus versutus. Bulletin of the Polish Academy of Sciences, Biological Sciences 55, 231–243.
Yagi S,
Kitai S, Kimura T
(1971) Oxidation of elemental sulfur to thiosulphate by Streptomyces. Applied Microbiology 22, 157–159.
| PubMed |
Yesmin L, Banerjee MR
(2000) Comparison of inoculant media for sulfur-oxidizing plant growth promoting rhizobacteria in canola. ‘Proceedings of Soils and Crops Workshop’. Saskatoon, Saskatchewan, Canada.. (University of Saskatchewan: Saskatoon, Canada)
