Ectomycorrhizal fungi inoculation alleviates simulated acid rain effects on soil ammonia oxidizers and denitrifiers in Masson pine forest

Acid rain can cause severe effects on soil biota and nutrient biogeochemical cycles in the forest ecosystem, but how plant-symbiotic ectomycorrhizal fungi will modulate the effects remains unknown. Here, we conducted a full factorial field experiment in a Masson pine forest by simultaneously controlling the acidity of the simulated rain (pH 5.6 vs. pH 3.5) and the ectomycorrhizal fungi Pisolithus tinctorius inoculation (non-inoculation vs. inoculation), to investigate the effects on ammonia oxidizers and denitrifiers. After 10 months, compared with the control (rain pH 5.6, and non-inoculation), simulated acid rain (pH 3.5) reduced soil nutrient content, decreased archaeal amoA gene abundance and inhibited denitrification enzyme activity. Also, simulated acid rain altered the community compositions of all the examined functional genes (archaeal amoA, bacterial amoA, nirK, nirS and nosZ). However, inoculation with ectomycorrhizal fungi under acid rain stress recovered soil nutrient content, archaeal amoA gene abundance and denitrification enzyme activity to levels comparable to the control, suggesting that ectomycorrhizal fungi inoculation ameliorates simulated acid rain effects. Taken together, ectomycorrhizal fungi inoculation - potentially through improving soil substrate availability - could alleviate the deleterious effects of acid rain on nitrogen cycling microbes in forest soils.

[1]  ammonia oxidation , 2020, Catalysis from A to Z.

[2]  A. Ekblad,et al.  Contrasting effects of ectomycorrhizal fungi on early and late stage decomposition in a boreal forest , 2018, The ISME Journal.

[3]  T. Whitham,et al.  Tree genetics defines fungal partner communities that may confer drought tolerance , 2017, Proceedings of the National Academy of Sciences.

[4]  Ji‐Zheng He,et al.  Time-dependent shifts in populations and activity of bacterial and archaeal ammonia oxidizers in response to liming in acidic soils , 2017 .

[5]  A. Vizzini,et al.  A nonnative and a native fungal plant pathogen similarly stimulate ectomycorrhizal development but are perceived differently by a fungal symbiont. , 2017, The New phytologist.

[6]  Ji‐Zheng He,et al.  Effects of dicyandiamide and acetylene on N2O emissions and ammonia oxidizers in a fluvo-aquic soil applied with urea , 2016, Environmental Science and Pollution Research.

[7]  Tao Zhang,et al.  Primary Succession of Nitrogen Cycling Microbial Communities Along the Deglaciated Forelands of Tianshan Mountain, China , 2016, Front. Microbiol..

[8]  Yuan Ge,et al.  Long-Term Effects of Multiwalled Carbon Nanotubes and Graphene on Microbial Communities in Dry Soil. , 2016, Environmental science & technology.

[9]  J. Barrett,et al.  Substrate availability drives spatial patterns in richness of ammonia-oxidizing bacteria and archaea in temperate forest soils , 2016 .

[10]  Deli Chen,et al.  Microbial regulation of terrestrial nitrous oxide formation: understanding the biological pathways for prediction of emission rates. , 2015, FEMS microbiology reviews.

[11]  Y. Ouyang,et al.  Effects of simulated acid rain on microbial characteristics in a lateritic red soil , 2015, Environmental Science and Pollution Research.

[12]  B. Singh,et al.  Water addition regulates the metabolic activity of ammonia oxidizers responding to environmental perturbations in dry subhumid ecosystems. , 2015, Environmental microbiology.

[13]  Zhan Chen,et al.  Impact of simulated acid rain on soil microbial community function in Masson pine seedlings , 2014 .

[14]  D. Stahl,et al.  Marine ammonia-oxidizing archaeal isolates display obligate mixotrophy and wide ecotypic variation , 2014, Proceedings of the National Academy of Sciences.

[15]  C. Prescott,et al.  Microbial functional genes involved in nitrogen fixation, nitrification and denitrification in forest ecosystems , 2014 .

[16]  C. Fang,et al.  Community size and composition of ammonia oxidizers and denitrifiers in an alluvial intertidal wetland ecosystem , 2014, Front. Microbiol..

[17]  S. Wan,et al.  Abundance and community structure of ammonia-oxidizing Archaea and Bacteria in response to fertilization and mowing in a temperate steppe in Inner Mongolia. , 2014, FEMS microbiology ecology.

[18]  Juan Chen,et al.  Comparative Proteomic Analysis of Differential Responses of Pinus massoniana and Taxus wallichiana var. mairei to Simulated Acid Rain , 2014, International journal of molecular sciences.

[19]  Haibo Li,et al.  Identification of fungal genes involved in the preinfection events between ectomycorrhizal association (Pisolithus tinctorius and Pinus massoniana) , 2014, Mycological Progress.

[20]  M. S. Pais,et al.  Ectomycorrhizal inoculation with Pisolithus tinctorius increases the performance of Quercus suber L. (cork oak) nursery and field seedlings , 2013, New Forests.

[21]  C. Troein,et al.  Carbon availability triggers the decomposition of plant litter and assimilation of nitrogen by an ectomycorrhizal fungus , 2013, The ISME Journal.

[22]  A. Ekblad,et al.  Growth of ectomycorrhizal fungal mycelium along a Norway spruce forest nitrogen deposition gradient and its effect on nitrogen leakage , 2013 .

[23]  Yong-guan Zhu,et al.  Effect of long-term wastewater irrigation on potential denitrification and denitrifying communities in soils at the watershed scale. , 2013, Environmental science & technology.

[24]  Ji‐Zheng He,et al.  Current insights into the autotrophic thaumarchaeal ammonia oxidation in acidic soils , 2012 .

[25]  Mary Firestone,et al.  Abundance of microbial genes associated with nitrogen cycling as indices of biogeochemical process rates across a vegetation gradient in Alaska. , 2012, Environmental microbiology.

[26]  Jianghong,et al.  Impacts of enhanced nitrogen deposition and soil acidification on biomass production and nitrogen leaching in Chinese fir plantations , 2012 .

[27]  Ji‐Zheng He,et al.  Ammonia-oxidizing archaea have more important role than ammonia-oxidizing bacteria in ammonia oxidation of strongly acidic soils , 2011, The ISME Journal.

[28]  Zhengqin Xiong,et al.  Autotrophic growth of nitrifying community in an agricultural soil , 2011, The ISME Journal.

[29]  S. Recous,et al.  Soil environmental conditions rather than denitrifier abundance and diversity drive potential denitrification after changes in land uses , 2011 .

[30]  Andreas Richter,et al.  Nitrososphaera viennensis, an ammonia oxidizing archaeon from soil , 2011, Proceedings of the National Academy of Sciences.

[31]  J. Prosser,et al.  Ammonia concentration determines differential growth of ammonia-oxidising archaea and bacteria in soil microcosms , 2011, The ISME Journal.

[32]  J. Prosser,et al.  Archaea rather than bacteria control nitrification in two agricultural acidic soils. , 2010, FEMS microbiology ecology.

[33]  D. Malakoff.  Air pollution. Taking the sting out of acid rain. , 2010, Science.

[34]  D. Gleeson,et al.  Response of ammonia oxidizing archaea and bacteria to changing water filled pore space , 2010 .

[35]  D. Arrouays,et al.  Determinants of the distribution of nitrogen-cycling microbial communities at the landscape scale , 2010, The ISME Journal.

[36]  Xingjun Tian,et al.  Effect of simulated acid rain on the litter decomposition of Quercus acutissima and Pinus massoniana in forest soil microcosms and the relationship with soil enzyme activities. , 2010, The Science of the total environment.

[37]  L. Bakken,et al.  Denitrification gene pools, transcription and kinetics of NO, N2O and N2 production as affected by soil pH. , 2010, FEMS microbiology ecology.

[38]  S. Zechmeister-Boltenstern,et al.  Nitrifiers and denitrifiers respond rapidly to changed moisture and increasing temperature in a pristine forest soil. , 2010, FEMS microbiology ecology.

[39]  William A. Walters,et al.  QIIME allows analysis of high-throughput community sequencing data , 2010, Nature Methods.

[40]  P. Courty,et al.  The role of ectomycorrhizal communities in forest ecosystem processes: new perspectives and emerging concepts. , 2010 .

[41]  X. Le Roux,et al.  Community niche predicts the functioning of denitrifying bacterial assemblages. , 2009, Ecology.

[42]  D. Stahl,et al.  Ammonia oxidation kinetics determine niche separation of nitrifying Archaea and Bacteria , 2009, Nature.

[43]  Maureen O’Callaghan,et al.  Nitrification driven by bacteria and not archaea in nitrogen-rich grassland soils , 2009 .

[44]  R. Conrad,et al.  Bacteria rather than Archaea dominate microbial ammonia oxidation in an agricultural soil. , 2009, Environmental microbiology.

[45]  C. Schleper,et al.  The influence of soil pH on the diversity, abundance and transcriptional activity of ammonia oxidizing archaea and bacteria. , 2008, Environmental microbiology.

[46]  Guoyi Zhou,et al.  Effect of Simulated Acid Rain on Potential Carbon and Nitrogen Mineralization in Forest Soils , 2008 .

[47]  Karen L. Adair,et al.  Evidence that Ammonia-Oxidizing Archaea are More Abundant than Ammonia-Oxidizing Bacteria in Semiarid Soils of Northern Arizona, USA , 2008, Microbial Ecology.

[48]  Ming-Gang Xu,et al.  Quantitative analyses of the abundance and composition of ammonia-oxidizing bacteria and ammonia-oxidizing archaea of a Chinese upland red soil under long-term fertilization practices. , 2007, Environmental microbiology.

[49]  Y. Ouyang,et al.  Impacts of simulated acid rain on cation leaching from the Latosol in south China. , 2007, Chemosphere.

[50]  S. Trumbore,et al.  Spatial separation of litter decomposition and mycorrhizal nitrogen uptake in a boreal forest. , 2007, The New phytologist.

[51]  G. Huang,et al.  Seasonal ionic exchange in two-layer canopies and total deposition in a subtropical evergreen mixed forest in central-south China , 2006 .

[52]  C. Schleper,et al.  Ammonia-oxidising Crenarchaeota: important players in the nitrogen cycle? , 2006, Trends in microbiology.

[53]  T. Huntington.  Available Water Capacity and Soil Organic Matter , 2005 .

[54]  M. Könneke,et al.  Isolation of an autotrophic ammonia-oxidizing marine archaeon , 2005, Nature.

[55]  M. Salkinoja-Salonen,et al.  Activity, diversity and population size of ammonia-oxidising bacteria in oil-contaminated landfarming soil. , 2005, FEMS microbiology letters.

[56]  Sara Hallin,et al.  Reassessing PCR primers targeting nirS, nirK and nosZ genes for community surveys of denitrifying bacteria with DGGE. , 2004, FEMS microbiology ecology.

[57]  H. Wallander,et al.  The production of ectomycorrhizal mycelium in forests: Relation between forest nutrient status and local mineral sources , 2003, Plant and Soil.

[58]  M. Schulz,et al.  The global distribution of acidifying wet deposition. , 2002, Environmental Science and Technology.

[59]  G. Likens,et al.  Mycorrhizal weathering of apatite as an important calcium source in base-poor forest ecosystems , 2002, Nature.

[60]  A. Stachurski,et al.  Atmospheric deposition and ionic interactions within a beech canopy in the Karkonosze Mountains. , 2002, Environmental pollution.

[61]  Jizhong Zhou,et al.  Nitrite Reductase Genes (nirK andnirS) as Functional Markers To Investigate Diversity of Denitrifying Bacteria in Pacific Northwest Marine Sediment Communities , 2000, Applied and Environmental Microbiology.

[62]  W. Zumft.  Cell biology and molecular basis of denitrification. , 1997, Microbiology and molecular biology reviews : MMBR.

[63]  F. Schinner,et al.  Methods in Soil Biology. , 1997 .

[64]  J. Graham,et al.  Functioning of mycorrhizal associations along the mutualism–parasitism continuum* , 1997 .

[65]  M. Firestone,et al.  Mechanisms for soil moisture effects on activity of nitrifying bacteria , 1995, Applied and environmental microbiology.

[66]  G. Lovett,et al.  Atmospheric Deposition and Canopy Interactions of Major Ions in a Forest , 1986, Science.

[67]  P. M. Kelly,et al.  Effects on climate , 1980, Nature.

[68]  Yaying Li,et al.  Nitrification and nitrifiers in acidic soils , 2018 .

[69]  Zen H. Lu,et al.  Comparative Proteomic Analysis , 2018 .

[70]  Jiaen Zhang,et al.  Effects of simulated acid rain on soil fauna community composition and their ecological niches. , 2017, Environmental pollution.

[71]  Levente Bodrossy,et al.  Effects of climate warming and elevated CO2 on autotrophic nitrification and nitrifiers in dryland ecosystems , 2016 .

[72]  W. Shen,et al.  Atmospheric deposition and canopy exchange of anions and cations in two plantation forests under acid rain influence , 2013 .

[73]  K. Futai,et al.  Ectomycorrhizae and Their Importance in Forest Ecosystems , 2008 .

[74]  J. Zwiazek,et al.  Ectomycorrhizas increase apoplastic water transport and root hydraulic conductivity in Ulmus americana seedlings , 2002 .

[75]  F. Dentener,et al.  Forest ecosystems and the changing patterns of nitrogen input and acid deposition today and in the future based on a scenario , 2001, Environmental science and pollution research international.

[76]  S. Hamburg,et al.  Base cation leaching from the canopy of a subtropical rainforest in northeastern Taiwan , 2001 .

[77]  Rattan Lal,et al.  Soil processes and the carbon cycle. , 1998 .

[78]  Y. Benjamini,et al.  Controlling the false discovery rate: a practical and powerful approach to multiple testing , 1995 .

[79]  J. Tiedje,et al.  Phases of denitrification following oxygen depletion in soil , 1979 .