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Soil microbial residue dynamics after 3-year elevated O3 exposure are plant species-specific

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Abstract

Background and aims

Rising ozone (O3) concentrations poses a great threat to crop growth and ecosystem carbon storage, but the underlying mechanism remains unclear. Identifying the impact of elevated O3 on soil microbial residues may advance our knowledge of microbial-mediated soil organic matter (SOM) turnover. In this paper, we aimed to investigate the effects of elevated O3 on the accumulation of amino sugars in the soil of the two wheat cultivars (Tritcium aestivum L.) with different ozone-tolerances.

Methods

Using the O3-Free Air Concentration Enrichment technique, we investigated the response of amino sugars to elevated O3 in a soil planted with two wheat cultivars of different ozone-tolerance [ozone-sensitive Yannong 19 (Y19) and ozone-tolerant Yangmai 16 (Y16)]. This study was conducted during the wheat growing season (jointing stage and ripening stage) of 2010 after exposure to elevated O3 for 3 years. Soil amino sugars were measured by gas chromatography technique.

Results

After exposure to elevated O3, the contents of total amino sugars decreased at the wheat jointing stage, and increased at the wheat ripening stage in the Y16 cultivar. In contrast, no significant effect of elevated O3 was found in the Y19 cultivar. The Glucosamine/Galactosamine and fungal carbon/bacterial carbon ratios decreased under elevated O3. The findings indicated that elevated O3 altered the microbial process of SOM turnover and bacteria contributed more to SOM cycling than fungi under elevated O3 conditions.

Conclusions

The effect of elevated O3 on the SOM turnover was wheat cultivar-specific. Thus, belowground processes of SOM turnover should be considered when selecting a tolerant wheat cultivar under elevated O3 regimes from a view of long-term ecosystem stability.

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References

  • Amelung W (2001) Methods using amino sugars as markers for microbial residues in soil. In: Lal R, Kimble JM, Follett RF, Stewart BA (eds) Assessment methods for soil carbon. Lewis Publishers, Boca Raton, pp 233–272

    Google Scholar 

  • Andersen CP (2003) Source-sink balance and carbon allocation below ground in plants exposed to ozone. New Phytol 157:213–228. doi:10.1046/j.1469-8137.2003.00674.x

    Article  CAS  Google Scholar 

  • Biswas DK, Xu H, Li YG, Sun JZ, Wang XZ, Han XG, Jiang GM (2008) Genotypic differences in leaf biochemical, physiological and growth responses to ozone in 20 winter wheat cultivars released over the past 60 years. Global Change Biol 14:46–59. doi:10.1111/j.1365-2486.2007.01477.x

    Google Scholar 

  • Brock TD, Madigan MT, Martinko JM, Parker J (1994) Biology of microorganisms, 7th edn. Prentice Hall, Englewood Cliffs

    Google Scholar 

  • Cao JL, Wang L, Zeng Q, Liang J, Tang HZ, Xie ZB, Liu G, Zhu JG, Kobayashi K (2009) Characteristics of photosynthesis in Wheat Cultivars with different sensitivities to ozone under O3-Free air concentration enrichment conditions. Acta Agron Sin 35:1500–1507

    CAS  Google Scholar 

  • Chander K, Joergensen RG (2001) Decomposition of 14C glucose in two soils with different amounts of heavy metal contamination. Soil Biol Biochem 33:1811–1816. doi:10.1016/S0038-0717(01)00108-0

    Article  CAS  Google Scholar 

  • Chantigny MH, Angers DA, Prévost D, Vézina LP, Chalifour FP (1997) Soil aggregation and fungal and bacterial biomass under annual and perennial cropping systems. Soil Sci Soc Am J 61:262–267

    Article  CAS  Google Scholar 

  • Chen Z, Wang XK, Feng ZZ, Xiao Q, Duan X (2009) Impact of elevated O3 on soil microbial community function under wheat crop. Water Air Soil Poll 198:189–198. doi:10.1007/s11270-008-9838-1

    Article  CAS  Google Scholar 

  • Chen Z, Wang X, Yao F, Zheng F, Feng Z (2010) Elevated ozone changed soil microbial community in a rice paddy. Soil Sci Soc Am J 74:829–837. doi:10.2136/sssaj2009.0258

    Article  CAS  Google Scholar 

  • Coyle JS, Dijkstra P, Doucett RR, Schwartz E, Hart SC, Hungate BA (2009) Relationships between C and N availability, substrate age, and natural abundance 13C and 15 N signatures of soil microbial biomass in a semiarid climate. Soil Biol Biochem 41:1605–1611. doi:10.1016/j.soilbio.2009.04.022

    Article  CAS  Google Scholar 

  • Dohrmann AB, Tebbe CC (2005) Effect of elevated tropospheric ozone on the structure of bacterial communities inhabiting the rhizosphere of herbaceous plants native to Germany. Appl Environ Microb 71:7750–7758. doi:10.1128/AEM.71.12.7750-7758.2005

    Article  CAS  Google Scholar 

  • Engelking B, Flessa H, Joergensen RG (2007) Shifts in amino sugar and ergosterol contents after addition of sucrose and cellulose to soil. Soil Biol Biochem 39:2111–2118. doi:10.1016/j.soilbio.2007.03.020

    Article  CAS  Google Scholar 

  • Esperschütz J, Pritsch K, Gattinger A, Welzl G, Haesler F, Buegger F, Winkler JB, Munch JC, Schloter M (2009) Influence of chronic ozone stress on carbon translocation pattern into rhizosphere microbial communities of beech trees (Fagus sylvatica L.) during a growing season. Plant Soil 323:85–95. doi:10.1007/s11104-009-0090-2

    Article  Google Scholar 

  • Feng ZZ, Kobayashi K (2009) Assessing the impacts of current and future concentrations of surface ozone on crop yield with meta-analysis. Atmos Environ 43:1510–1519. doi:10.1016/j.atmosenv.2008.11.033

    Article  CAS  Google Scholar 

  • Feng ZZ, Kobayashi K, Ainsworth EA (2008) Impact of elevated ozone concentration on growth, physiology, and yield of wheat (Triticum aestivum L.): A meta-analysis. Global Change Biol 14:2696–2708. doi:10.1111/j.1365-2486.2008.01673.x

    Google Scholar 

  • Feng ZZ, Pang J, Kobayashi K, Zhu JG, Ort DR (2011) Differential responses in two varieties of winter wheat to elevated ozone concentration under fully open-air field conditions. Global Change Biol 17:580–591. doi:10.1111/j.1365-2486.2010.02184.x

    Article  Google Scholar 

  • Glaser B, Turrión MB, Alef K (2004) Amino sugars and muramic acid-biomarkers for soil microbial community structure analysis. Soil Biol Biochem 36:399–407. doi:10.1016/j.soilbio.2003.10.013

    Article  CAS  Google Scholar 

  • He H, Zhang W, Zhang X, Xie H, Zhuang J (2011) Temporal responses of soil microorganisms to substrate addition as indicated by amino sugar differentiation. Soil Biol Biochem 43:1155–1161. doi:10.1016/j.soilbio.2011.02.002

    Article  CAS  Google Scholar 

  • Hofmockel KS, Zak DR, Moran KK, Jastrow JD (2011) Changes in forest soil organic matter pools after a decade of elevated CO2 and O3. Soil Biol Biochem 43:1518–1527. doi:10.1016/j.soilbio.2011.03.030

    Article  CAS  Google Scholar 

  • Kanerva T, Palojärvi A, Rämö K, Manninen S (2008) Changes in soil microbial community structure under elevated tropospheric O3 and CO2. Soil Biol Biochem 40:2502–2510. doi:10.1016/j.soilbio.2008.06.007

    Article  CAS  Google Scholar 

  • Karnosky DF, Skelly JM, Percy KE, Chappelka AH (2007) Perspectives regarding 50 years of research on effects of tropospheric ozone air pollution on US forests. Environ Pollut 147:489–506. doi:10.1016/j.envpol.2006.08.043

    Article  CAS  PubMed  Google Scholar 

  • Kögel-Knabner I (2002) The macromolecular organic composition of plant and microbial residues as inputs to soil organic matter. Soil Biol Biochem 34:139–162. doi:10.1016/S0038-0717(01)00158-4

    Article  Google Scholar 

  • Lauer F, Kösters R, du Preez CC, Amelung W (2011) Microbial residues as indicators of soil restoration in South African secondary pastures. Soil Biol Biochem 43:787–794. doi:10.1016/j.soilbio.2010.12.012

    Article  CAS  Google Scholar 

  • Li Q, Bao XL, Lu CY, Zhang XK, Zhu JG, Jiang Y, Liang WJ (2012) Soil microbial food web responses to free air ozone enrichment can depend on the ozone-tolerance of wheat cultivars. Soil Biol Biochem 47:27–35. doi:10.1016/j.soilbio.2011.12.012

    Article  CAS  Google Scholar 

  • Liang C, Balser TC (2008) Preferential sequestration of microbial carbon in subsoils of a glacial-landscape toposequence, Dane County, WI, USA. Geoderma 148:113–119. doi:10.1016/j.geoderma.2008.09.012

    Article  CAS  Google Scholar 

  • Liang C, Zhang X, Balser TC (2007a) Net microbial amino sugar accumulation process in soil as influenced by different plant material inputs. Biol Fert Soils 44:1–7. doi:10.1007/s00374-007-0170-5

    Article  CAS  Google Scholar 

  • Liang C, Zhang X, Rubert KF, Balser TC (2007b) Effect of plant materials on microbial transformation of amino sugars in three soil microcosms. Biol Fert Soils 43:631–639. doi:10.1007/s00374-006-0142-1

    Article  Google Scholar 

  • Liang C, Cheng G, Wixon DL, Balser TC (2011) An absorbing Markov Chain approach to understanding the microbial role in soil carbon stabilization. Biogeochemistry 106:303–309. doi:10.1007/s10533-010-9525-3

    Article  Google Scholar 

  • Loya WM, Pregitzer KS, Karberg NJ, King JS, Giardina CP (2003) Reduction of soil carbon formation by tropospheric ozone under increased carbon dioxide levels. Nature 425:705–707. doi:10.1038/nature02047

    Article  CAS  PubMed  Google Scholar 

  • Manninen S, Aaltonen H, Kanerva T, Rämö K, Palojärvi A (2010) Plant and soil microbial biomasses in Agrostis capillaris and Lathyrus pratensis monocultures exposed to elevated O3 and CO2 for three growing seasons. Soil Biol Biochem 42:1967–1975. doi:10.1016/j.soilbio.2010.07.017

    Article  CAS  Google Scholar 

  • McCrady JK, Andersen CP (2000) The effect of ozone on below-ground carbon allocation in wheat. Environ Pollut 107:465–472. doi:10.1016/S0269-7491(99)00122-0

    Article  CAS  PubMed  Google Scholar 

  • Morgan PB, Mies TA, Bollero GA, Nelson RL, Long SP (2006) Season-long elevation of ozone concentration to projected 2050 levels under fully open-air conditions substantially decreases the growth and production of soybean. New Phytol 170:333–343. doi:10.1111/j.1469-8137.2006.01679.x

    Article  PubMed  Google Scholar 

  • Parsons JW (1981) Chemistry and distribution of amino sugars in soils and soil organisms. In: Paul EA, Ladd JN (eds) Soil biochemistry, vol 5. Marcel Dekker, New York, pp 197–227

    Google Scholar 

  • Paul EA, Clark FE (1996) Soil Microbiology and Biochemistry, 2nd edn. Academic, San Diego

    Google Scholar 

  • Phillips RL, Zak DR, Holmes WE, White DC (2002) Microbial community composition and function beneath temperate trees exposed to elevated atmospheric carbon dioxide and ozone. Oecologia 131:236–244. doi:10.1007/s00442-002-0868-x

    Article  Google Scholar 

  • Pleijel H, Eriksen AB, Danielsson H, Bondesson N, Selldén G (2006) Differential ozone sensitivity in an old and a modern Swedish wheat cultivar–grain yield and quality, leaf chlorophyll and stomatal conductance. Environ Exp Bot 56:63–71. doi:10.1016/j.envexpbot.2005.01.004

    Article  CAS  Google Scholar 

  • Simpson RT, Frey SD, Six J, Thiet RK (2004) Preferential accumulation of microbial carbon in aggregate structures of no-tillage soils. Soil Sci Soc of Am J 68:1249–1255

    Article  CAS  Google Scholar 

  • Sitch S, Cox PM, Collins WJ, Huntingford C (2007) Indirect radiative forcing of climate change through ozone effects on the land-carbon sink. Nature 448:791–794. doi:10.1038/nature06059

    Article  CAS  PubMed  Google Scholar 

  • Talhelm AF, Pregitzer KS, Zak DR (2009) Species-specific responses to atmospheric carbon dioxide and tropospheric ozone mediate changes in soil carbon. Ecol Lett 12:1219–1228. doi:10.1111/j.1461-0248.2009.01380.x

    Article  PubMed  Google Scholar 

  • ter Braak CJF (1988) CANOCO–A FORTRAN program for canonical community ordination by (partial) (detrended) (canonical) correspondence analysis, principal components analysis and redundancy analysis (version2.1), Technical report LWA-88-02, Agricultural Mathematics Group, Wageningen

  • Turrión MB, Glaser B, Zech W (2002) Effects of deforestation on contents and distribution of amino sugars within particle-size fractions of mountain soils. Biol Fert Soils 35:49–53. doi:10.1007/s00374-001-0440-6

    Article  Google Scholar 

  • van Groenigen KJ, Six J, Harris D, van Kessel C (2007) Elevated CO2 does not favor a fungal decomposition pathway. Soil Biol Biochem 39:2168–2172. doi:10.1016/j.soilbio.2007.03.009

    Article  Google Scholar 

  • van Groenigen KJ, Bloem J, Bååth E, Boeckx P, Rousk J, Bodé S, Forristal D, Jones MB (2010) Abundance, production and stabilization of microbial biomass under conventional and reduced tillage. Soil Biol Biochem 42:48–55. doi:10.1016/j.soilbio.2009.09.023

    Article  Google Scholar 

  • Vance ED, Brookes PC, Jenkinson DS (1987) An extraction method for measuring soil microbial biomass-C. Soil Biol Biochem 19:703–707. doi:10.1016/0038-0717(87)90052-6

    Article  CAS  Google Scholar 

  • Vingarzan R (2004) A review of surface ozone background levels and trends. Atmos Environ 33:3431–3442. doi:10.1016/j.atmosenv.2004.03.030

    Article  Google Scholar 

  • Wardle DA, Bardgett RD, Klironomos JN, Setälä H, van der Putten WH, Wall DH (2004) Ecological linkages between aboveground and belowground biota. Science 304:1629–1633. doi:10.1126/science.1094875

    Article  CAS  PubMed  Google Scholar 

  • Wittig VE, Ainsworth EA, Long SP (2007) To what extent do current and projected increases in surface ozone affect photosynthesis and stomatal conductance of trees? A meta-analytic review of the last 3 decades of experiments. Plant Cell Environ 30:1150–1162. doi:10.1111/j.1365-3040.2007.01717.x

    Article  CAS  PubMed  Google Scholar 

  • Zhang X, Amelung W (1996) Gas chromatographic determination of muramic acid, glucosamine, mannosamine, and galactosamine in soils. Soil Biol Biochem 28:1201–1206. doi:10.1016/0038-0717(96)00117-4

    Article  CAS  Google Scholar 

  • Zhang X, Amelung W, Yuan Y, Zech W (1998) Amino sugar signature of particle size fractions in soils of the native prairie as affected by climate. Soil Sci 163:220–229. doi:10.1097/00010694-199803000-00007

    Article  CAS  Google Scholar 

  • Zhang X, Amelung W, Yuan Y, Zech W, Samson-Liebig S, Brown L, Zech W (1999) Land-use effects on amino sugars in particle-size fractions of an Argiudoll. Appl Soil Ecol 11:271–275. doi:10.1007/s00374-001-0440-6

    Article  Google Scholar 

  • Zhu XK, Feng ZZ, Sun TF, Liu XC, Tang HY, Zhu JG, Guo WS, Kabayashi K (2011) Effects of elevated ozone concentration on yield of four Chinese cultivars of winter wheat under fully open-air field conditions. Global Change Biol 17:2697–2706. doi:10.1111/j.1365-2486.2011.02400.x

    Article  Google Scholar 

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Acknowledgments

The authors are grateful to Prof. Xinkai Zhu in Yangzhou University for supplying different wheat cultivars. We thank Professor Philip Brookes of Rothamsted Research for his great help in the revision of our manuscript. We also thank the anonymous reviewers for their insightful reviews of the manuscript. This research was supported by the Natural Science Foundation of China (Grant No. 41071161, 41130524, 31270487 and 41101242), the International S & T Cooperation Program of China (Grant No. 2009DFA31110), the Knowledge Innovation Program of Chinese Academy of Sciences (Grant No. KZCX2-EW-414), and the Global Environment Research Fund by the Ministry of the Environment, Japan (Grant No. C-062).

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Authors and Affiliations

  1. State Key Laboratory of Forest and Soil Ecology, Institute of Applied Ecology, Chinese Academy of Sciences, Shenyang, 110164, China

    Wei Zhang, Hongbo He, Qi Li, Caiyan Lu & Xudong Zhang

  2. National Field Observation and Research Station of Shenyang Agroecosystems, Chinese Academy of Sciences, Shenyang, 110016, China

    Xudong Zhang

  3. State Key Laboratory of Soil and Sustainable Agriculture, Institute of Soil Science, Chinese Academy of Sciences, Nanjing, 210008, China

    Jianguo Zhu

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  1. Wei Zhang
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  2. Hongbo He
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  3. Qi Li
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Correspondence to Hongbo He or Xudong Zhang.

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Zhang, W., He, H., Li, Q. et al. Soil microbial residue dynamics after 3-year elevated O3 exposure are plant species-specific. Plant Soil 376, 139–149 (2014). https://doi.org/10.1007/s11104-013-1973-9

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