The interactive effects of elevated ozone and wheat cultivars on soil microbial community composition and metabolic diversity.

Abstract Human-induced global changes have important impacts on terrestrial ecosystems. Although aboveground influences of elevated ozone have been widely studied, relatively little attention has been paid to the belowground subsystem, nevertheless it is critical to study belowground effects in determining the long-term consequences of ozone exposure to ecosystems. Here, we investigated the effects of elevated ozone on soil microbial community structure and functional diversity using the free-air ozone enrichment platform (FAOE). We detected that soil fungal phospholipid fatty acid and the fungal/bacterial ratio were significantly ower under elevated ozone than under ambient ozone at the wheat ripening stage. Through determining soil microbial metabolic diversity as evaluated by variations in the microbial utilization rates of different carbon sources among different wheat cultivars, we found that soil microbial communities inhabiting the rhizosphere of ozone-tolerant cultivars preferred to consume easily degradable carbon sources, while more complex carbon sources were preferably utilized by those associated with ozone-sensitive cultivars. These changes may in turn promote (ozone-tolerant wheat cultivars)/inhibit (ozone-sensitive wheat cultivars) plant growth through alterations in nutrient availability and resource distribution.

[1]  Jaap Bloem,et al.  Microbiological methods for assessing soil quality , 2005 .

[2]  Xiaoke Zhang,et al.  Soil microbial food web responses to free-air ozone enrichment can depend on the ozone-tolerance of wheat cultivars , 2012 .

[3]  J. McCrady,et al.  The effect of ozone on below-ground carbon allocation in wheat. , 2000, Environmental pollution.

[4]  S. Krupa,et al.  The ozone component of global change: potential effects on agricultural and horticultural plant yield, product quality and interactions with invasive species. , 2009, Journal of integrative plant biology.

[5]  D. Hirst,et al.  Use of rhizosphere carbon sources in sole carbon source tests to discriminate soil microbial communities , 1997 .

[6]  D. K. Biswas,et al.  Genotypic differences in leaf biochemical, physiological and growth responses to ozone in 20 winter wheat cultivars released over the past 60 years , 2007 .

[7]  Abdul Malik,et al.  Environmental Protection Strategies for Sustainable Development , 2012 .

[8]  E. Bååth,et al.  The use of phospholipid fatty acid analysis to estimate bacterial and fungal biomass in soil , 1996, Biology and Fertility of Soils.

[9]  Håkan Pleijel,et al.  A stomatal ozone flux-response relationship to assess ozone-induced yield loss of winter wheat in subtropical China. , 2012, Environmental pollution.

[10]  E. Ainsworth,et al.  Impact of elevated ozone concentration on growth, physiology, and yield of wheat (Triticum aestivum L.): a meta‐analysis , 2008 .

[11]  P. Lemanceau,et al.  Going back to the roots: the microbial ecology of the rhizosphere , 2013, Nature Reviews Microbiology.

[12]  C. Andersen Source-sink balance and carbon allocation below ground in plants exposed to ozone. , 2003, The New phytologist.

[13]  C.J.F. ter Braak,et al.  CANOCO - a FORTRAN program for canonical community ordination by [partial] [etrended] [canonical] correspondence analysis, principal components analysis and redundancy analysis (version 2.1) , 1988 .

[14]  B. Hungate,et al.  Relationships between C and N availability, substrate age, and natural abundance 13C and 15N signatures of soil microbial biomass in a semiarid climate , 2009 .

[15]  D. Bossio,et al.  Determinants of Soil Microbial Communities: Effects of Agricultural Management, Season, and Soil Type on Phospholipid Fatty Acid Profiles , 1998, Microbial Ecology.

[16]  A. Edwards,et al.  Rock fragments in soil support a different microbial community from the fine earth , 2004 .

[17]  P. Brookes,et al.  AN EXTRACTION METHOD FOR MEASURING SOIL MICROBIAL BIOMASS C , 1987 .

[18]  D. Grantz,et al.  O3 impacts on plant development: a meta-analysis of root/shoot allocation and growth. , 2006, Plant, cell & environment.

[19]  Jianguo Zhu,et al.  Effects of elevated ozone concentration on yield of four Chinese cultivars of winter wheat under fully open‐air field conditions , 2011 .

[20]  Zhaozhong Feng,et al.  Assessing the impacts of current and future concentrations of surface ozone on crop yield with meta-analysis , 2009 .

[21]  R Core Team,et al.  R: A language and environment for statistical computing. , 2014 .

[22]  D. Ort,et al.  Differential responses in two varieties of winter wheat to elevated ozone concentration under fully open‐air field conditions , 2011 .

[23]  A. Palojärvi,et al.  Plant and soil microbial biomasses in Agrostis capillaris and Lathyrus pratensis monocultures exposed to elevated O3 and CO2 for three growing seasons , 2010 .

[24]  A. Palojärvi,et al.  Changes in soil microbial community structure under elevated tropospheric O3 and CO2 , 2008 .

[25]  Gang Liu,et al.  A system for free-air ozone concentration elevation with rice and wheat: Control performance and ozone exposure regime , 2011 .

[26]  R. Artz,et al.  Assessing CLPPs using MicroResp™ , 2007 .

[27]  A. Benedetti,et al.  Phospholipid fatty acid (PLFA) analyses. , 2005 .

[28]  P. Legendre,et al.  Variation partitioning of species data matrices: estimation and comparison of fractions. , 2006, Ecology.

[29]  Chonggang Xu,et al.  Residue incorporation and N fertilization affect the response of soil nematodes to the elevated CO2 in a Chinese wheat field , 2009 .

[30]  Harry Harmens,et al.  Evidence of widespread effects of ozone on crops and (semi‐)natural vegetation in Europe (1990–2006) in relation to AOT40‐ and flux‐based risk maps , 2011 .

[31]  Denise L Mauzerall,et al.  Increasing global agricultural production by reducing ozone damages via methane emission controls and ozone-resistant cultivar selection , 2013, Global change biology.

[32]  G. Gleixner,et al.  Soil organic matter in soil depth profiles: Distinct carbon preferences of microbial groups during carbon transformation , 2008 .

[33]  Gang Liu,et al.  Characteristics of Photosynthesis in Wheat Cultivars with Different Sensitivi-ties to Ozone under O 3 -Free Air Concentration Enrichment Conditions: Characteristics of Photosynthesis in Wheat Cultivars with Different Sensitivi-ties to Ozone under O 3 -Free Air Concentration Enrichment Conditions , 2009 .

[34]  J. Potts,et al.  A Rapid Microtiter Plate Method To Measure Carbon Dioxide Evolved from Carbon Substrate Amendments so as To Determine the Physiological Profiles of Soil Microbial Communities by Using Whole Soil , 2003, Applied and Environmental Microbiology.

[35]  M. V. D. van der Heijden,et al.  The unseen majority: soil microbes as drivers of plant diversity and productivity in terrestrial ecosystems. , 2008, Ecology letters.

[36]  M. Rowell Colorimetric method for CO2 measurement in soils , 1995 .

[37]  Pierre Legendre,et al.  DISTANCE‐BASED REDUNDANCY ANALYSIS: TESTING MULTISPECIES RESPONSES IN MULTIFACTORIAL ECOLOGICAL EXPERIMENTS , 1999 .

[38]  S. B. Agrawal,et al.  Elevated ozone and two modern wheat cultivars: An assessment of dose dependent sensitivity with respect to growth, reproductive and yield parameters , 2010 .

[39]  K. Kobayashi,et al.  Characteristics of Photosynthesis in Wheat Cultivars with Different Sensitivities to Ozone Under O3-Free Air Concentration Enrichment Conditions , 2009 .

[40]  E. Bååth,et al.  Comparison of soil fungal/bacterial ratios in a pH gradient using physiological and PLFA-based techniques , 2003 .

[41]  J. Six,et al.  The distribution of nematodes and soil microbial communities across soil aggregate fractions and farm management systems , 2011 .

[42]  Jianguo Zhu,et al.  Soil microbial residue dynamics after 3-year elevated O3 exposure are plant species-specific , 2014, Plant and Soil.

[43]  K. Burkey,et al.  Crop responses to ozone: uptake, modes of action, carbon assimilation and partitioning , 2005 .

[44]  W. J. Dyer,et al.  A rapid method of total lipid extraction and purification. , 1959, Canadian journal of biochemistry and physiology.

[45]  J. Six,et al.  Bacterial and Fungal Contributions to Carbon Sequestration in Agroecosystems , 2006 .

[46]  Luc Abbadie,et al.  Carbon input to soil may decrease soil carbon content , 2004 .

[47]  K. Domsch,et al.  A physiological method for the quantitative measurement of microbial biomass in soils , 1978 .

[48]  Y. Steinberger,et al.  Soil microbial metabolic profiles in two geomorphological units in a semistable sand-dune ecosystem , 2012 .