Plant roots and species moderate the salinity effect on microbial respiration, biomass, and enzyme activities in a sandy clay soil

Original Paper
  • 20 Downloads

Abstract

The aim of this study was to determine the effects of plant absence or presence on microbial properties and enzyme activities at different levels of salinity in a sandy clay soil. The treatments involved five salinity levels—0.5 (control), 2.5, 5, 7.5, and 10 dS m−1 which were prepared using a mixture of chloride salts—and three soil environments (unplanted soil, and soils planted with either wheat or clover) under greenhouse conditions. Each treatment was replicated three times. At the end of the experiment, soil microbial respiration, substrate-induced respiration (SIR), microbial biomass C (MBC), and enzyme activities were determined after plant harvest. Increasing salinity decreased soil microbial properties and enzyme activities, but increased the metabolic quotient (qCO2) in both unplanted and planted soils. Most microbial properties of planted soils were greater than those of unplanted soils at low to moderate salinity levels, depending upon plant species. There was a small or no difference in soil properties between the unplanted and planted treatments at the highest salinity level, indicating that the indirect effects of plant presence might be less important due to significant reduction of plant growth. The lowered microbial activity and biomass, and enzyme activities were due to the reduction of root activity and biomass in salinized soils. The lower values of qCO2 in planted than unplanted soils support the positive influence of plant root and its exudates on soil microbial activity and biomass in saline soils. Nonetheless, the role of plants in alleviating salinity influence on soil microbial activities decreases at high salinity levels and depends on plant type. In conclusion, cultivation and growing plant in abandoned saline environments with moderate salinity would improve soil microbial properties and functions by reducing salinity effect, in particular planting moderately tolerant crops. This helps to maintain or increase the fertility and quality of abandoned saline soils in arid regions.

Keywords

Enzyme activity Microbial indicators Root effects Plant type Salinity stress 

Notes

Acknowledgements

The authors express their thanks to Shahrekord University for the financial support of the study reported in this paper. They also thank the Editor-in-Chief and three anonymous reviewers for their valuable and critical comments on an earlier draft of the manuscript.

Supplementary material

374_2018_1277_MOESM1_ESM.doc (152 kb)
ESM 1 (DOC 152 kb)

References

  1. Akhter J, Mahmood K, Malik KA, Ahmed S, Murray R (2003) Amelioration of a saline sodic soil through cultivation of a salt-tolerant grass Leptochloa fusca. Environ Conserv 30:168–174CrossRefGoogle Scholar
  2. Akhter J, Murray R, Mahmood K, Malik KA, Ahmed S (2004) Improvement of degraded physical properties of a saline-sodic soil by reclamation with kallar grass (Leptochloa fusca). Plant Soil 258:207–216CrossRefGoogle Scholar
  3. Alef K, Nannipieri P (1995) Methods in applied soil microbiology and biochemistry. Academic Press, LondonGoogle Scholar
  4. Anderson TH, Domsch KH (1993) The metabolic quotient for CO2 (qCO2) as a specific activity parameter to assess the effects of environmental conditions, such as pH, on the microbial biomass of forest soils. Soil Biol Biochem 25:393–395CrossRefGoogle Scholar
  5. Anderson TH, Domsch KH (2010) Soil microbial biomass: the eco-physiological approach. Soil Biol Biochem 42:2039–2043CrossRefGoogle Scholar
  6. Anderson JM, Ingram JSI (1993) Tropical soil biology and fertility. A handbook of methods, OxfordGoogle Scholar
  7. Cheng W (2009) Rhizosphere priming effect: its functional relationships with microbial turnover, evapotranspiration, and C–N budgets. Soil Biol Biochem 41:1795–1801CrossRefGoogle Scholar
  8. Cheng W, Kuzyakov Y (2005) Root effects on soil organic matter decomposition. In: Zobel RW, Wright SF (eds) Roots and soil management: interactions between roots and the soil, agronomy monograph no. 48. American Society of Agronomy, Madison, pp 119–143Google Scholar
  9. Delmo-Organo N, Delfine EF, Gregorio GB, lantican NB, Simbahan JF, Paterno E (2017) Combined effects of salinity, rice variety and rice growth stage on the diversity of bacterial communities associated with rice (Oryza sativa L.). J Inter Soc Southeast Asian Agric Sci 23:134–145Google Scholar
  10. Dijkstra FA, Bader NE, Johnson DW, Cheng W (2009) Does accelerated soil organic matter decomposition in the presence of plants increase plant N availability? Soil Biol Biochem 41:1080–1087CrossRefGoogle Scholar
  11. Egamberdieva D, Renella G, Wirth S, Islam R (2010) Secondary salinity effects on soil microbial biomass. Biol Fertil Soils 46:445–449CrossRefGoogle Scholar
  12. Emadodin I, Narita D, Bork HR (2012) Soil degradation and agricultural sustainability: an overview from Iran. Environ Dev Sustain 14:611–625CrossRefGoogle Scholar
  13. Epelde L, Mijangos I, Becerril JM, Garbisu C (2009) Soil microbial community as bioindicator of the recovery of soil functioning derived from metal phytoextraction with sorghum. Soil Biol Biochem 41:1788–1794CrossRefGoogle Scholar
  14. Futamata H, Sakai M, Ozawa H, Urashima Y, Sueguchi T, Matsuguchi T (1998) Chemotactic response to amino acid of Fluorescent pseudomonads isolated from spinach roots grown in soil with different salinity levels. J Plant Nutr Soil Sci 44:1–7CrossRefGoogle Scholar
  15. García C, Hernández T (1996) Influence of salinity on the biological and biochemical activity of a calciorthird soil. Plant Soil 178:255–263CrossRefGoogle Scholar
  16. Garcia C, Roldan A, Hernandez T (2005) Ability of different plant species to promote microbiological processes in semiarid soil. Geoderma 124:193–202CrossRefGoogle Scholar
  17. Ghollarata M, Raiesi F (2007) The adverse effects of soil salinization on the growth of Trifolium alexandrinum L. and associated microbial and biochemical properties in a soil from Iran. Soil Biol Biochem 39:1699–1702CrossRefGoogle Scholar
  18. Gianfreda L, Ruggiero P (2006) Enzyme activities in soil. In: Nannipieri P, Smalla K (Eds.) Nucleic acids and proteins in soil. Soil Biology, Volume 8, Springer-Verlag Berlin Heidelberg, pp 257–311Google Scholar
  19. Hasbullah H, Marschner P (2015) Residue properties influence the impact of salinity on soil respiration. Biol Fertil Soils 51:99–111CrossRefGoogle Scholar
  20. Hernández-Allica J, Becerril JM, Zárate O, Garbisu C (2006) Assessment of the efficiency of a metal phytoextraction process with biological indicators of soil health. Plant Soil 281:147–158CrossRefGoogle Scholar
  21. Hu YC, Schmidhalter U (2005) Drought and salinity: a comparison of their effects on mineral nutrition of plants. J Plant Nutr Soil Sci 168:541–549CrossRefGoogle Scholar
  22. Irshad M, Honna T, Yamamoto S, Eneji AE, Yamasaki N (2005) Nitrogen mineralization under saline conditions. Commun Soil Sci Plant Anal 36:1681–1689CrossRefGoogle Scholar
  23. Iwaoka C, Imada S, Taniguchi T, Du S, Tamanaka N, Tateno R (2017) The impacts of soil fertility and salinity on soil nitrogen dynamics mediated by the soil microbial community beneath the halophytic shrub tamarisk. Microb Ecol.  https://doi.org/10.1007/s00248-017-1090-z
  24. Jafari-Vafa H, Raiesi R, Hosseinpur A (2016) Sewage sludge application strongly modifies earthworm impact on microbial and biochemical attributes in a semi-arid calcareous soil from Iran. Appl Soil Ecol 100:45–56CrossRefGoogle Scholar
  25. Jiang J, Wu L, Li N, Luo Y, Liu L, Zhao Q, Zhang L, Christie P (2010) Effects of multiple heavy metal contamination and repeated phytoextraction by Sedum plumbizincicola on soil microbial properties. Eur J Soil Biol 46:18–26CrossRefGoogle Scholar
  26. Joergensen RG (1995) Microbial biomass: the fumigation-incubation method. In: Alef K, Nannipieri P (eds) Methods in applied soil microbiology and biochemistry. Academic Press, London, pp 375–381CrossRefGoogle Scholar
  27. Johnson DA, Rumbaugh MD, Asay KH (1981) Plant improvement for semi-arid rangelands: possibilities for drought resistance and nitrogen fixation. Plant Soil 58:279–303CrossRefGoogle Scholar
  28. Lu H, Li Z, Fu S, Méndez A, Gascó G, Paz-Ferreiro J (2015) Combining phytoextraction and biochar addition improves soil biochemical properties in a soil contaminated with Cd. Chemosphere 119:209–216CrossRefPubMedGoogle Scholar
  29. Luna-Guido ML, Beltrán-Hernández RI, Dendooven L (2001) Dynamics of 14C-labelled glucose in alkaline saline soil. Soil Biol Biochem 33:707–719CrossRefGoogle Scholar
  30. Luo G, Ling N, Nannipieri P, Chen H, Raza W, Wang M, Guo S, Shen G (2017) Long-term fertilisation regimes affect the composition of the alkaline phosphomonoesterase encoding microbial community of a vertisol and its derivative soil fractions. Biol Fertil Soils 53:375–388CrossRefGoogle Scholar
  31. Nannipieri P, Ascher J, Ceccherini M, Landi L, Pietramellara G, Renella G (2003) Microbial diversity and soil functions. Eur J Soil Sci 54:655–670CrossRefGoogle Scholar
  32. Nannipieri P, Giagnoni L, Renella G, Puglisi E, Ceccanti B, Masciandaro G, Fornasier F, Moscatelli MC, Marinari S (2012) Soil enzymology: classical and molecular approaches. Biol Fertil Soils 48:743–762CrossRefGoogle Scholar
  33. Nannipieri P, Trasar-Cepeda C, Dick RP (2018) Soil enzyme activity: a brief history and biochemistry as a basis for appropriate interpretations and meta-analysis. Biol Fertil Soils 54:11–19CrossRefGoogle Scholar
  34. Neergaard A, Gorissen A (2004) Carbon allocation to roots, rhizodeposits and soil after pulse labelling: a comparison of white clover (Trifolium repens L.) and perennial ryegrass (Lolium perenne L.). Biol Fertil Soils 39:228–234CrossRefGoogle Scholar
  35. Nie M, Zhang XD, Wang JG, Jiang LF, Yang J, Quan ZX, Cui XH, Fang CM, Li B (2009) Rhizosphere effects on soil bacterial abundance and diversity in the Yellow River deltaic ecosystem as influenced by petroleum contamination and soil salinization. Soil Biol Biochem 41:2535–2542CrossRefGoogle Scholar
  36. Okur N, Cengel M, Gocmez S (2002) Influence of salinity on microbial respiration and enzyme activity of soils. Proc Int Symp Tech Control Salination Hortic Prod (573):198–194Google Scholar
  37. Pathak H, Rao DLN (1998) Carbon and nitrogen mineralization from added organic matter in saline and alkali soils. Soil Biol Biochem 30:695–702CrossRefGoogle Scholar
  38. Pessarakli M (2011) Handbook of plant and crop stress (3rd Ed). CRC Press, Taylor & Francis Group, Boca RatonGoogle Scholar
  39. Raiesi F (2006) Carbon and N mineralization as affected by soil cultivation and crop residue in a calcareous wetland ecosystem in Central Iran. Agric Ecosyst Environ 112:13–20CrossRefGoogle Scholar
  40. Rao DLN, Pathak H (1996) Ameliorative influence of organic matter on biological activity of salt affected soils. Arid Soil Res Rehab 10:311–319CrossRefGoogle Scholar
  41. Rasul G, Appuhn A, Müller T, Joergensen RG (2006) Salinity-induced changes in the microbial use of sugarcane filter cake added to soil. Appl Soil Ecol 31:1–10CrossRefGoogle Scholar
  42. Rath KM, Rousk J (2015) Salt effects on the soil microbial decomposer community and their role in organic carbon cycling: a review. Soil Biol Biochem 81:108–123CrossRefGoogle Scholar
  43. Rietz DN, Haynes RJ (2003) Effects of irrigation-induced salinity and sodicity on soil microbial activity. Soil Biol Biochem 35:845–854CrossRefGoogle Scholar
  44. Sacchi GA, Abruzzese A, Lucchini G, Fiorani F, Cocucci S (2000) Efflux and active re-absorption of glucose in roots of cotton plants grown under saline conditions. Plant Soil 220:1–11CrossRefGoogle Scholar
  45. Sanaullah M, Blagodatskaya E, Chabbi A, Rumpel C, Kuzyakov Y (2011) Drought effects on microbial biomass and enzyme activities in the rhizosphere of grasses depend on plant community composition. Appl Soil Ecol 48:38–44CrossRefGoogle Scholar
  46. Sardinha MT, Muller H, Schmeisky R, Joergensen RG (2003) Microbial performance in soils along a salinity gradient under acidic conditions. Appl Soil Ecol 23:237–244CrossRefGoogle Scholar
  47. Setia R, Marschner P (2013) Carbon mineralization in saline soils as affected by residue composition and water potential. Biol Fertil Soils 49:71–77CrossRefGoogle Scholar
  48. Setia R, Marschner P, Baldock J, Chittleborough D, Smith P, Smith J (2011) Salinity effects on carbon mineralization in soils of varying texture. Soil Biol Biochem 43:1908–1916CrossRefGoogle Scholar
  49. Six J, Frey SD, Thiet RK, Batten KM (2006) Bacterial and fungal contributions to carbon sequestration in agroecosystems. Soil Sci Soc Am J 70:555–569CrossRefGoogle Scholar
  50. Sparling GP (1997) Soil microbial biomass, activity and nutrient cycling as indicators of soil health. In: Pankhurst CE, Doube BM, Gupta VVSR (eds) Biological indicators of soil health. CAB, Wallingford, pp 97–119Google Scholar
  51. Tripathi S, Kumari S, Chakraborty A, Gupta A, Chakrabarti K, Bandyapadhyay BK (2006) Microbial biomass and its activities in salt-affected coastal soils. Biol Fertil Soils 42:273–277CrossRefGoogle Scholar
  52. Wallenstein MD, Weintraub MN (2008) Emerging tools for measuring and modeling the in situ activity of soil extracellular enzymes. Soil Biol Biochem 40:2098–2106CrossRefGoogle Scholar
  53. Wang M, Li E, Liu C, Jousset A, Salles JF (2017) Functionality of root-associated bacteria along a salt marsh primary succession. Front Microbiol 8.  https://doi.org/10.3389/fmicb.2017.02102
  54. Wardle DA, Ghani A (1995) A critique of the microbial quotient (qCO2) as a bio-indicator of disturbance and ecosystem development. Soil Biol Biochemi 27:1601–1610CrossRefGoogle Scholar
  55. Wardle DA, Bardgett RD, Klironomos JN, Setälä H, van der Putten WH, Wall DH (2004) Ecological linkages between aboveground and belowground biota. Science 304:1629–1633CrossRefPubMedGoogle Scholar
  56. Wichern J, Wichern F, Joergensen RG (2006) Impact of salinity on soil microbial communities and the decomposition of maize in acidic soils. Geoderma 137:100–108CrossRefGoogle Scholar
  57. Wong VNL, Dalal RC, Greene RSB (2008) Salinity and sodicity effects on respiration and microbial biomass of soil. Biol Fertil Soils 44:943–953CrossRefGoogle Scholar
  58. Yan N, Petra Marschner P (2012) Response of microbial activity and biomass to increasing salinity depends on the final salinity, not the original salinity. Soil Biol Biochem 53:50–55CrossRefGoogle Scholar
  59. Yuan BC, Li ZZ, Liu H, Gao M, Zhang YY (2007) Microbial biomass and activity in salt affected soils under arid conditions. Appl Soil Ecol 35:319–328CrossRefGoogle Scholar
  60. Zhang CB, Wang J, Liu W, Zhu S, Ge H, Chang S, Chang J, Ge Y (2010) Effects of plant diversity on microbial biomass and community metabolic profiles in a full-scale constructed wetland. Ecol Eng 36:62–68CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Department of Soil Science and Engineering, Faculty of AgricultureShahrekord UniversityShahrekordIran

Personalised recommendations