Abstract
Elemental S oxidation in soil is a microbially mediated process and is hypothesised to be influenced by changes to soil chemical properties such as acidity and ionic strength, which may arise from co-granulation with macronutrients or elemental S oxidation itself. Soil incubation was conducted with a sandy soil from South Australia to assess the effect of acidification and increased ionic strength on bacterial abundance and community composition and on elemental S oxidation during a 14-week incubation at 25 °C and 70% field capacity. Prior to incubation, the soil was treated with HNO3 to bring the pH to 6.7–4.4 or with KH2PO4 to increase the ionic strength by 0–0.7 M. Elemental S was applied at 200 mg kg−1 air-dried soil. Acidification or increased ionic strength had no or little effect on elemental S oxidation but decreased the abundances of 16S ribosomal deoxyribonucleic acid (rRNA) and soxB genes and changed the bacterial community composition. A second experiment with two other soils also showed that acidification did not, or only slightly, decreased elemental S oxidation, even though acidification strongly reduced 16S rRNA and soxB gene abundances in one of the soils. This study suggests that shifts in bacterial population brought about by temporary changes in pH and ionic strength, as may occur around fertiliser granules, have no or little effect on elemental S oxidation, indicating that the S-oxidising bacterial community in these agricultural soils contains functionally redundant taxa, which responded to changing conditions.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Adamczyk-Winiarska Z, Król M, Kobus J (1975) Microbial oxidation of elemental sulphur in brown soil. Plant Soil 43:95–100. doi:10.1007/BF01928478
Allison SD, Martiny JBH (2008) Resistance, resilience and redundancy in microbial communities. PNAS 105:11512–11519. doi:10.1073/pnas.0801925105
Anandham R, Indiragandhi P, Madhaiyan M (2008) Chemolithoautotrophic oxidation of thiosulfate and phylogenetic distribution of sulfur oxidation gene (soxB) in rhizobacteria isolated from crop plants. Res Microbiol 159:579–589. doi:10.1016/j.resmic.2008.08.007
Anderson MJ (2001) A new method for non-parametric multivariate analysis of variance. Austral Ecol 26:32–46. doi:10.1046/j.1442-9993.2001.01070.x
Clarke KR, Ainsworth M (1993) A method of linking multivariate community structure to environmental variables. Mar Ecol Prog Ser 92:205–219. doi:10.3354/meps092205
Donn MJ, Menzies NW (2005) Simulated rainwater effects on anion exchange capacity and nitrate retention in Ferrosols. Soil Res 43:33–42. doi:10.1071/SR04015 Source: OAI
Edwards U, Rogall T, Blöcker H, Emde M, Böttger EC (1989) Isolation and direct complete nucleotide determination of entire genes. Characterization of a gene coding for 16S ribosomal RNA. Nucleic Acids Res 17:7843–7853. doi:10.1093/nar/17.19.7843
Fierer N, Leff JW, Adams BJ, Nielsen UN, Bates ST, Lauber CL, Owens S, Gilbert JA, Wall DH, Caporaso JG (2012) Cross-biome metagenomic analyses of soil microbial communities and their functional attributes. PNAS 109:21390–21395. doi:10.1073/pnas.1215210110
Franklin RB, Mills AL (2006) Structural and functional responses of a sewage microbial community to dilution-induced reductions in diversity. Microb Ecol 52:280–288. doi:10.1007/s00248-006-9033-0
Galinski EA, Trüper HG (1994) Microbial behaviour in salt-stressed ecosystems. FEMS Microbiol Rev 15:95–108. doi:10.1111/j.1574-697 6. 1994.tb00128.x
Grayston SJ, Wainwright M (1988) Sulphur oxidation by soil fungi including some species of mycorrhizae and wood-rotting basidiomycetes. FEMS Microbiol Lett 53:1–8. doi:10.1111/j.1574-6968.1988.tb02641.x
Gupta VVSR, Kroker SK, Hicks M, Davoren CW, Descheemaeker K, Llewellyn RS (2014) Nitrogen cycling in summer active perennial grass systems in South Australia: non-symbiotic nitrogen fixation. Crop Pasture Sci 65:1044–1056. doi:10.1071/CP14109
Ibekwe AM, Poss JA, Grattan SR, Grieve CM, Suarez D (2010) Bacterial diversity in cucumber (Cucumis sativus) rhizosphere in response to salinity, soil pH, and boron. Soil Biol Biochem 42:567–575. doi:10.1016/j.soilbio.2009.11.033
Janzen HH, Bettany JR (1987) Measurement of sulfur oxidation in soils. Soil Sci 143:444–452. doi:10.1097/00010694-198706000-00008
Kemmitt SJ, Wright D, Goulding KWT, Jones DL (2006) pH regulation of carbon and nitrogen dynamics in two agricultural soils. Soil Biol Biochem 38:898–911. doi:10.1016/j.soilbio.2005.08.006
Lawrence JR, Germida JJ (1988) Relationship between microbial biomass and elemental sulfur oxidation in agricultural soils. Soil Sci Soc Am J 52:672–677. doi:10.2136/sssaj1988.03615995005200030014x
Lee A, Watkinson JH, Orbell G, Bagyaraj J, Lauren DR (1987) Factors influencing dissolution of phosphate rock and oxidation of elemental sulphur in some New Zealand soils. New Zeal J Agr Res 30:373–385. doi:10.1080/00288233.1987.10421898
Lehman RM, Acosta-Martinez V, Buyer JS, Cambardella CA, Collins HP, Ducey TF, Halvorson JJ, Jin VL, Johnson JMF, Kremer RJ, Lundgren JG, Manter DK, Maul JE, Smith JL, Stott DE (2015) Soil biology for resilient, healthy soil. J Soil Water Conserv 70:12A–18A. doi:10.2489/jswc.70.1.12A
Lettl A, Langkramer O, Lochman V (1981) Dynamics of oxidation of inorganic sulphur compounds in upper soil horizons of spruce forests. Folia Microbiol 26:24–28. doi:10.1007/BF02927219
Li P, Caldwell AC (1966) The oxidation of elemental sulfur in soil. Soil Sci Soc Am J 30:370–372. doi:10.2136/sssaj1966.03615995003000030021x
Marschner P, Kandeler E, Marschner B (2003) Structure and function of the soil microbial community in a long-term fertilizer experiment. Soil Biol Biochem 35:453–461. doi:10.1016/S0038-0717(02)00297-3
Nannipieri P, Ascher J, Ceccherini MT, Landi L, Pietramellara G, Renella G (2003) Microbial diversity and soil functions. Eur J Soil Sci 54:655–670. doi:10.1046/j.1351-0754.2003.0556.x
Nor YM, Tabatabai MA (1977) Oxidation of elemental sulfur in soils. Soil Sci Soc Am J 41:736–741. doi:10.2136/sssaj1977.03615995004100040025x
Ollivier J, Wanat N, Austruy A, Hitmi A, Joussein E, Welzl G, Munch JC, Schloter M (2012) Abundance and diversity of ammonia-oxidizing prokaryotes in the root–rhizosphere complex of Miscanthus giganteus grown in heavy metal-contaminated soils. Microb Ecol 64:1038–1046. doi:10.1007/s00248-012-0078-y
Petersen DG, Blazewicz SJ, Firestone M, Herman DJ, Turetsky M, Waldrop M (2012) Abundance of microbial genes associated with nitrogen cycling as indices of biogeochemical process rates across a vegetation gradient in Alaska. Environ Microbiol 14:993–1008. doi:10.1111/j.1462-2920.2011.02679.x
Petri R, Podgorsek L, Imhoff JF (2001) Phylogeny and distribution of the soxB gene among thiosulfate-oxidizing bacteria. FEMS Microbiol Lett 197:171–178. doi:10.1111/j.1574-6968.2001.tb10600.x
Prevost-Boure NC, Christen R, Dequiedt S, Mougel C, Lelievre M, Jolivet C, Shahbazkia HR, Guillou L, Arrouays D, Ranjard L (2011) Validation and application of a PCR primer set to quantify fungal communities in the soil environment by real-time quantitative PCR. PLoS One 6:1–13
Rothbaum H, Groom P (1961) Fire hazards in the use of fertilisers containing elemental sulphur. New Zealand J Sci 4:476–488
Rousk J, Baath E, Brookes PC, Lauber CL, Lozupone C, Caporaso JG, Knight R, Fierer N (2010) Soil bacterial and fungal communities across a pH gradient in an arable soil. ISME J 4:1340–1351. doi:10.1038/ismej.2010.58
Sample EC, Soper RJ, Racz GJ (1980) Reactions of phosphate fertilizers in soils. In: Khasawneh FE, Sample EC, Kamprath EJ (eds) The role of phosphorus in agriculture. American Society of Agronomy, Crop Science Society of America Soil Science Society of America, Madison, pp. 263–310
Shannon CE, Weaver W (1948) A mathematical theory of communication. Bell Syst Tech J 27:379–423. doi:10.1002/j.1538-7305.1948.tb01338.x
Suzuki I, Lee D, Mackay B, Harahuc L, Oh JK (1999) Effect of various ions, pH, and osmotic pressure on oxidation of elemental sulfur by Thiobacillus thiooxidans. Appl Environ Microb 65:5163–5168
Tan Y, Bond WJ, Rovira AD, Brisbane PG, Griffin DM (1991) Movement through soil of a biological control agent, Pseudomonas fluorescens. Soil Biol Biochem 23:821–825. doi:10.1016/0038-0717(91)90092-X
Tan Y, Bond WJ, Griffin DM (1992) Transport of bacteria during unsteady unsaturated soil water flow. Soil Sci Soc Am J 56:1331–1340. doi:10.2136/sssaj1992.03615995005600050001x
Tourna M, Maclean P, Condron L, O’Callaghan M, Wakelin SA (2014) Links between sulphur oxidation and sulphur-oxidising bacteria abundance and diversity in soil microcosms based on soxB functional gene analysis. FEMS Microbiol Ecol 88:538–549. doi:10.1111/1574-6941.12323
Wertz S, Degrange V, Prosser JI, Poly F, Commeaux C, Guillaumaud N, Le Roux X (2007) Decline of soil microbial diversity does not influence the resistance and resilience of key soil microbial functional groups following a model disturbance. Environ Microbiol 9:2211–2219. doi:10.1111/j.1462-2920.2007.01335.x
Xia FF, Su Y, Wei XM, He YH, Wu ZC, Ghulam A, He R (2014) Diversity and activity of sulphur-oxidizing bacteria and sulphate-reducing bacteria in landfill cover soils. Lett Appl Microbiol 59:26–34. doi:10.1111/lam.12240
Zhao C, Degryse F, Gupta VVSR, McLaughlin MJ (2015) Elemental sulfur oxidation in Australian cropping soils. Soil Sci Soc Am J 79:89–96. doi:10.2136/sssaj 201 4.08.0314
Zhao C, Degryse F, Gupta VVSR, McLaughlin MJ (2016a) Low effective surface area explains slow oxidation of co-granulated elemental sulfur. Soil Sci Soc Am J 80:911–918. doi:10.2136/sssaj2015.09.0215
Zhao C, Gupta VVSR, Degryse F, McLaughlin MJ (2016b). Abundance and diversity of S-oxidising bacteria and their role in elemental sulphur oxidation in Australian cropping soils. Biol Fertil Soils. doi:10.1007/s00374-016-1162-0
Acknowledgements
The authors would like to acknowledge the China Scholarship Council for providing the scholarship and Mosaic Company for support. We would also like to thank Marcus Hicks for his assistance with TRFLP analysis and Bogumila Tomczak, Colin Rivers and Ashleigh Broadbent for their assistances with chemical analysis.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Zhao, C., Gupta, V.V.S.R., Degryse, F. et al. Effects of pH and ionic strength on elemental sulphur oxidation in soil. Biol Fertil Soils 53, 247–256 (2017). https://doi.org/10.1007/s00374-016-1170-0
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00374-016-1170-0