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Soil, land care and environmental research
RESEARCH ARTICLE

Effects of addition of nitrogen on soil fungal and bacterial biomass and carbon utilisation efficiency in a city lawn soil

Xinyu Jiang A C , Lixiang Cao B and Renduo Zhang A C

A Guangdong Provincial Key Laboratory of Environmental Pollution Control and Remediation Technology, School of Environmental Science and Engineering, Sun Yat-sen University, Guangzhou 510275, China.

B School of Life Science, Sun Yat-sen University, Guangzhou 510275, China.

C Corresponding authors. Email: zhangrd@mail.sysu.edu.cn; XIN.YU.JIANG1@gmail.com

Soil Research 52(1) 97-105 http://dx.doi.org/10.1071/SR13210
Submitted: 2 May 2013  Accepted: 23 September 2013   Published: 5 February 2014

Abstract

The aim of this study was to investigate the effects of nitrogen (N) addition on soil microbial (fungal and bacterial) biomass and carbon utilisation efficiency (CUE) in a city lawn soil. A field experiment was conducted with three N treatments (kg N ha–1 year–1): the control (0), low-N (100), and high-N (200). Soil biogeochemical properties including pH, C : N, CUE, microbial biomass C (MBC), fungal and bacterial biomass, microbial C uptake rates, and soil respiration (SR) rates were determined during a 500-day experiment. The low- and high-N treatments significantly decreased soil pH, MBC, and CUE. Available N and soil acidification caused a decline in soil MBC. Soil acidification was not beneficial for microbial biomass growth, especially for bacteria. The treatments with N changed soil biomass from bacterial-dominant to fungal-dominant.

The results also showed that the CUE of bacterial-dominant soil was higher than that of fungal-dominant soil, which is contrary to previous studies. However, SR did not increase with decreased CUE under N treatments, because the addition of N limited soil microbial C uptake rates and significantly decreased soil microbial biomass. The CUE showed a negative correlation with soil temperature for the control treatment but not for the N treatments, which suggested that added N played a more important role in CUE than did soil temperature. Our results showed that addition of further N significantly alters soil biogeochemical properties, alters the ratio of bacteria to fungi, and decreases microbial carbon utilisation, which should provide important information for model-based prediction of soil C-cycling.

Additional keywords: carbon utilisation efficiency, microbial biomass, N treatment, soil acidification, soil carbon, soil respiration.


References

Aciego Pietri JC, Brookes PC (2009) Substrate inputs and pH as factors controlling microbial biomass, activity and community structure in an arable soil. Soil Biology & Biochemistry 41, 1396–1405.
Substrate inputs and pH as factors controlling microbial biomass, activity and community structure in an arable soil.CrossRef | 1:CAS:528:DC%2BD1MXnt1Oltb0%3D&md5=2e3cdb3c820e065a5ba2ab040eb74c39CAS | open url image1

Allison SD, Wallenstein MD, Bradford MA (2010) Soil-carbon response to warming dependent on microbial physiology. Nature Geoscience 3, 336–340.
Soil-carbon response to warming dependent on microbial physiology.CrossRef | 1:CAS:528:DC%2BC3cXlsFSksLY%3D&md5=20ec5aece56b89588c41f879e9d82bddCAS | open url image1

Bardgett RD, McAlister E (1999) The measurement of soil fungal: bacterial biomass ratios as an indicator of ecosystem self-regulation in temperate meadow grasslands. Biology and Fertility of Soils 29, 282–290.
The measurement of soil fungal: bacterial biomass ratios as an indicator of ecosystem self-regulation in temperate meadow grasslands.CrossRef | open url image1

Bardgett RD, Lovell RD, Hobbs PJ, Jarvis SC (1999) Seasonal changes in soil microbial communities along a fertility gradient of temperate grasslands. Soil Biology & Biochemistry 31, 1021–1030.
Seasonal changes in soil microbial communities along a fertility gradient of temperate grasslands.CrossRef | 1:CAS:528:DyaK1MXjsFCnu7w%3D&md5=d3a957d2a013892cc72ca314a2cbea2eCAS | open url image1

Bell JM, Smith JL, Bailey VL, Bolton H (2003) Priming effect and C storage in semi-arid no-till spring crop rotations. Biology and Fertility of Soils 37, 237–244.

Bi J, Zhang NL, Liang Y, Yang HJ, Ma KP (2012) Interactive effects of water and nitrogen addition on soil microbial communities in a semiarid steppe. Journal of Plant Ecology 5, 320–329.
Interactive effects of water and nitrogen addition on soil microbial communities in a semiarid steppe.CrossRef | open url image1

Boberg J, Finlay RD, Stenlid J, Nasholm T, Lindahl BD (2008) Glucose and ammonium additions affect needle decomposition and carbon allocation by the litter degrading fungus Mycena epipterygia. Soil Biology & Biochemistry 40, 995–999.
Glucose and ammonium additions affect needle decomposition and carbon allocation by the litter degrading fungus Mycena epipterygia.CrossRef | 1:CAS:528:DC%2BD1cXhslGqtbw%3D&md5=d2c876c55d1ccefa25538788f63c34ccCAS | open url image1

Bossuyt H, Denef K, Six J, Frey SD, Merckx R, Paustian K (2001) Influence of microbial populations and residue quality on aggregate stability. Applied Soil Ecology 16, 195–208.
Influence of microbial populations and residue quality on aggregate stability.CrossRef | open url image1

Bottomley PJ (1994) Light microscopic methods for studying soil microorganisms. In ‘Methods of soil analysis. Part 2. Microbiological and biochemical properties’. (Ed. RW Weaver) pp. 81–105. (Soil Science Society of America: Madison, WI)

Bowden RD, Davidson E, Savage K, Arabia C, Steudler P (2004) Chronic nitrogen additions reduce total soil respiration and microbial respiration in temperate forest soils at the Harvard Forest. Forest Ecology and Management 196, 43–56.
Chronic nitrogen additions reduce total soil respiration and microbial respiration in temperate forest soils at the Harvard Forest.CrossRef | open url image1

Boyle D (1998) Nutritional factors limiting the growth of Lentinula edodes and other white-rot fungi in wood. Soil Biology & Biochemistry 30, 817–823.
Nutritional factors limiting the growth of Lentinula edodes and other white-rot fungi in wood.CrossRef | 1:CAS:528:DyaK1cXjsFylurY%3D&md5=2e60969488db172c110dda488997a011CAS | open url image1

Brink RH, Dubach P, Lynch DL (1960) Measurement of carbohydrate in soil hydrolyzates with anthrone. Soil Science 89, 157–166.
Measurement of carbohydrate in soil hydrolyzates with anthrone.CrossRef | 1:CAS:528:DyaF3MXhsFSgtg%3D%3D&md5=a45bf4ca902c22e6f134af28dce68d53CAS | open url image1

Busse MD, Sanchez FG, Ratcliff AW, Butnor JR, Carter EA, Powers RE (2009) Soil carbon sequestration and changes in fungal and bacterial biomass following incorporation of forest residues. Soil Biology & Biochemistry 41, 220–227.
Soil carbon sequestration and changes in fungal and bacterial biomass following incorporation of forest residues.CrossRef | 1:CAS:528:DC%2BD1MXotV2isw%3D%3D&md5=2dc3444e67438942e210ad98103ee55eCAS | open url image1

Compton JE, Watrud LS, Porteous LA, DeGrood S (2004) Response of soil microbial biomass and community composition to chronic nitrogen additions at Harvard forest. Forest Ecology and Management 196, 143–158.
Response of soil microbial biomass and community composition to chronic nitrogen additions at Harvard forest.CrossRef | open url image1

Dalal RC, Mayer RJ (1986) Long term trends in fertility of soils under continuous cultivation and cereal cropping in southern Queensland. II. Total organic carbon and its rate of loss from the soil profile. Soil Research 24, 281–292.
Long term trends in fertility of soils under continuous cultivation and cereal cropping in southern Queensland. II. Total organic carbon and its rate of loss from the soil profile.CrossRef | 1:CAS:528:DyaL28XkvFKmsLw%3D&md5=0e8cc56dee57a5b989b47a587da88fd4CAS | open url image1

Devêvre OC, Horwáth WR (2000) Decomposition of rice straw and microbial carbon use efficiency under different soil temperatures and moistures. Soil Biology & Biochemistry 32, 1773–1785.
Decomposition of rice straw and microbial carbon use efficiency under different soil temperatures and moistures.CrossRef | open url image1

Fang Y, Xun F, Bai WM, Zhang WH, Li LH (2012) Long-term nitrogen addition leads to loss of species richness due to litter accumulation and soil acidification in a temperate steppe. PLoS ONE.
Long-term nitrogen addition leads to loss of species richness due to litter accumulation and soil acidification in a temperate steppe.CrossRef | 23166811PubMed | open url image1

Follett RF, Paul EA, Pruessner EG (2007) Soil carbon dynamics during a long-term incubation study involving 13C and 14C measurements. Soil Science 172, 189–208.
Soil carbon dynamics during a long-term incubation study involving 13C and 14C measurements.CrossRef | 1:CAS:528:DC%2BD2sXkt1KrtL0%3D&md5=e082c3979bc2bd89d3875a9350a586a4CAS | open url image1

Frey SD, Gupta VVSR, Elliott ET, Paustian K (2001) Protozoan grazing affects estimates of carbon utilization efficiency of the soil microbial community. Soil Biology & Biochemistry 33, 1759–1768.
Protozoan grazing affects estimates of carbon utilization efficiency of the soil microbial community.CrossRef | 1:CAS:528:DC%2BD3MXotFOlu74%3D&md5=65bf7d769ea827a1c2e9241786862291CAS | open url image1

Groffman PM, Pouyat RV (2009) Methane uptake in urban forests and lawns. Environmental Science & Technology 43, 5229–5235.
Methane uptake in urban forests and lawns.CrossRef | 1:CAS:528:DC%2BD1MXmvFWqsL4%3D&md5=4b86ec9e969dd6442776a371fdc52cd5CAS | open url image1

Groffman PM, Williams CO, Pouyat RV, Band LE, Yesilonis ID (2009) Nitrate leaching and nitrous oxide flux in urban forests and grasslands. Journal of Environmental Quality 38, 1848–1860.
Nitrate leaching and nitrous oxide flux in urban forests and grasslands.CrossRef | 1:CAS:528:DC%2BD1MXhtFCjsrfI&md5=fe458bf6deff16b43d8500844b445676CAS | 19643750PubMed | open url image1

Hamer U, Potthast K, Makeschin F (2009) Urea fertilisation affected soil organic matter dynamics and microbial community structure in pasture soils of Southern Ecuador. Applied Soil Ecology 43, 226–233.
Urea fertilisation affected soil organic matter dynamics and microbial community structure in pasture soils of Southern Ecuador.CrossRef | open url image1

Hobbie SE (2000) Interactions between lignin and soil nitrogen availability during leaf litter decomposition in a Hawaiian montane forest. Ecosystems 3, 484–494.
Interactions between lignin and soil nitrogen availability during leaf litter decomposition in a Hawaiian montane forest.CrossRef | 1:CAS:528:DC%2BD3cXovFWgt7s%3D&md5=dabe21737f34d0eeda6f98edd99ac49bCAS | open url image1

Hobbie SE, Gough L (2004) Litter decomposition in moist acidic and non-acidic tundra with different glacial histories. Oecologia 140, 113–124.
Litter decomposition in moist acidic and non-acidic tundra with different glacial histories.CrossRef | 15164284PubMed | open url image1

Hobbie SE, Nadelhoffer KJ, Högberg P (2002) A synthesis: the role of nutrients as constraints on carbon balances in boreal and arctic regions. Plant and Soil 242, 163–170.
A synthesis: the role of nutrients as constraints on carbon balances in boreal and arctic regions.CrossRef | 1:CAS:528:DC%2BD38XlvFWjsr4%3D&md5=1490d2b25b3359326cf6c402b73d5b56CAS | open url image1

Ingham ER, Klein DA (1984) Soil fungi: relationships between hyphal activity and staining with fluorescein diacetate. Soil Biology & Biochemistry 16, 273–278.
Soil fungi: relationships between hyphal activity and staining with fluorescein diacetate.CrossRef | 1:CAS:528:DyaL2cXls1Krt7o%3D&md5=968559391f80049b2f05db45361e3669CAS | open url image1

Jim CY, Chen WY (2006) Perception and attitude of residents toward urban green spaces in Guangzhou (China). Environmental Management 38, 338–349.
Perception and attitude of residents toward urban green spaces in Guangzhou (China).CrossRef | 1:STN:280:DC%2BD28vkvFGnsg%3D%3D&md5=41697e82f0cfa098027c088e7eb1e01eCAS | 16752045PubMed | open url image1

Johnson D, Leake JR, Lee JA, Campbell CD (1998) Changes in soil microbial biomass and microbial activities in response to 7 years simulated pollutant nitrogen deposition on a heathland and two grasslands. Environmental Pollution 103, 239–250.
Changes in soil microbial biomass and microbial activities in response to 7 years simulated pollutant nitrogen deposition on a heathland and two grasslands.CrossRef | 1:CAS:528:DyaK1cXotVWqtL0%3D&md5=99cd1bba3800e7ad5df0756ebad587fcCAS | open url image1

Katharina MK, Edward KH, Wolfgang W, Ute S, Ieda H, Gunther E, Sandra B, Joseph S, Katja S, Andreas R, Sophie ZB (2010) The effect of resource quantity and resource stoichiometry on microbial carbon-use-efficiency. FEMS Microbiology Ecology 73, 430–440.

Keiblinger KM, Hall EK, Wanek W, Szukics U, Hämmerle I, Ellersdorfer G, Böck S, Strauss J, Sterflinger K, Richter A, Zechmeister-Boltenstern S (2010) The effect of resource quantity and resource stoichiometry on microbial carbon-use efficiency. FEMS Microbiology Ecology 73, 430–440.

Krusche AV, De Camargo PB, Cerri CE, Ballester MV, Lara LBLS, Victoria RL, Martinelli LA (2003) Acid rain and nitrogen deposition in a sub-tropical watershed (Piracicaba): ecosystem consequences. Environmental Pollution 121, 389–399.
Acid rain and nitrogen deposition in a sub-tropical watershed (Piracicaba): ecosystem consequences.CrossRef | 1:CAS:528:DC%2BD38XptlWjsLY%3D&md5=226ec8cd7ef409beed0ef8ea7c619c98CAS | 12685767PubMed | open url image1

Li LJ, Zeng DH, Yu ZY, Fan ZP, Mao R (2010) Soil microbial properties under N and P additions in a semi-arid, sandy grassland. Biology and Fertility of Soils 46, 653–658.
Soil microbial properties under N and P additions in a semi-arid, sandy grassland.CrossRef | 1:CAS:528:DC%2BC3cXoslyktrY%3D&md5=81d1d115fc0fa61fb36064645c85f84fCAS | open url image1

Lin Z, Zhang R, Tang J, Zhang J (2011) Effects of high soil water content and temperature on soil respiration. Soil Science 176, 150–155.
Effects of high soil water content and temperature on soil respiration.CrossRef | 1:CAS:528:DC%2BC3MXis1yjsbY%3D&md5=ba58036ccbf1ae738513817772968bf5CAS | open url image1

López-Urrutia A, Morán XAG (2007) Resource limitation of bacterial production distorts the temperature dependence of oceanic carbon cycling. Ecology 88, 817–822.
Resource limitation of bacterial production distorts the temperature dependence of oceanic carbon cycling.CrossRef | 17536698PubMed | open url image1

Lu XK, Mo JM, Gundersern P, Zhu WX, Zhou GY, Li DJ, Zhang X (2009) Effect of simulated N deposition on soil exchangeable cations in three forest types of subtropical China. Pedosphere 19, 189–198.
Effect of simulated N deposition on soil exchangeable cations in three forest types of subtropical China.CrossRef | 1:CAS:528:DC%2BD1MXkvFCltb4%3D&md5=cf87cde660dd65c4ea018ac55cce298eCAS | open url image1

Magid J, Kjaergaard GA, Kuikman PJ (1999) Drying and rewetting of a loamy sand soil did not increase turnover of native organic matter, but retarded the decomposition of added 14C-labelled plant material. Soil Biology & Biochemistry 31, 595–602.
Drying and rewetting of a loamy sand soil did not increase turnover of native organic matter, but retarded the decomposition of added 14C-labelled plant material.CrossRef | 1:CAS:528:DyaK1MXitlansbk%3D&md5=280b6c94f1309aef9c0c049fe84e463dCAS | open url image1

Magill AH, Aber JD, Hendricks JJ, Bowden RD, Melillo JM, Steudler PA (1997) Biogeochemical response of forest ecosystems to simulated chronic nitrogen deposition. Ecological Applications 7, 402–415.
Biogeochemical response of forest ecosystems to simulated chronic nitrogen deposition.CrossRef | open url image1

Micks P, Aber JD, Boone RD, Davidson EA (2004) Short-term soil respiration and nitrogen immobilization response to nitrogen applications in control and nitrogen-enriched temperate forests. Forest Ecology and Management 196, 57–70.
Short-term soil respiration and nitrogen immobilization response to nitrogen applications in control and nitrogen-enriched temperate forests.CrossRef | open url image1

Mo JM, Zhang W, Zhu WX, Fang YT, Li DJ, Zhao P (2007) Response of soil respiration to simulated N deposition in a disturbed and a rehabilitated tropical forest in southern China. Plant and Soil 296, 125–135.
Response of soil respiration to simulated N deposition in a disturbed and a rehabilitated tropical forest in southern China.CrossRef | 1:CAS:528:DC%2BD2sXnsFejsrc%3D&md5=cc8d2a06431af58fceb980f29d734a26CAS | open url image1

Nilsson LO, Wallander H, Gundersen P (2012) Changes in microbial activities and biomasses over a forest floor gradient in C-to-N ratio. Plant and Soil 355, 75–86.
Changes in microbial activities and biomasses over a forest floor gradient in C-to-N ratio.CrossRef | 1:CAS:528:DC%2BC38Xns1eks7Y%3D&md5=c6d7d3b51dd8c899887f4d8fbf8229d1CAS | open url image1

Parton WJ, Schimel DS, Cole CV, Ojima DS (1987) Analysis of factors controlling soil organic matter levels in Great Plains grasslands. Soil Science Society of America Journal 51, 1173–1179.
Analysis of factors controlling soil organic matter levels in Great Plains grasslands.CrossRef | 1:CAS:528:DyaL2sXmtlGnsbw%3D&md5=83adee9d531a52b4c726cce830d3407cCAS | open url image1

Rousk J, Bååth E (2007) Fungal and bacterial growth in soil with plant materials of different C/N ratios. FEMS Microbiology Ecology 62, 258–267.
Fungal and bacterial growth in soil with plant materials of different C/N ratios.CrossRef | 1:CAS:528:DC%2BD2sXhsValtr7I&md5=7be35778c24cc413772c807c975a0e6cCAS | 17991019PubMed | open url image1

Rousk J, Demoling LA, Bahr A, Bååth E (2008) Examining the fungal and bacterial niche overlap using selective inhibitors in soil. FEMS Microbiology Ecology 63, 350–358.
Examining the fungal and bacterial niche overlap using selective inhibitors in soil.CrossRef | 1:CAS:528:DC%2BD1cXivFeqs7w%3D&md5=238cf208a867f049ee3518dc396322b9CAS | 18205814PubMed | open url image1

Rousk J, Brookes PC, Bååth E (2009) Contrasting soil pH effects on fungal and bacterial growth suggest functional redundancy in carbon mineralization. Applied and Environmental Microbiology 75, 1589–1596.
Contrasting soil pH effects on fungal and bacterial growth suggest functional redundancy in carbon mineralization.CrossRef | 1:CAS:528:DC%2BD1MXjsFKgsLo%3D&md5=90c606e8fe28332ea97e73b1cc889256CAS | 19151179PubMed | open url image1

Schimel JP, Gulledge JM, Clein-Curley JS, Lindstrom JE, Braddock JF (1999) Moisture effects on microbial activity and community structure in decomposing birch litter in the Alaskan taiga. Soil Biology & Biochemistry 31, 831–838.
Moisture effects on microbial activity and community structure in decomposing birch litter in the Alaskan taiga.CrossRef | 1:CAS:528:DyaK1MXjtFSrsL4%3D&md5=c864454d0c297a2ba93b9180f4e73f9bCAS | open url image1

Söderström BE (1977) Vital staining of fungi in pure cultures and in soil with fluorescein diacetate. Soil Biology & Biochemistry 9, 59–63.
Vital staining of fungi in pure cultures and in soil with fluorescein diacetate.CrossRef | open url image1

Steinweg JM, Plante AF, Conant RT, Paula EA, Tanaka DL (2008) Patterns of substrate utilization during long-term incubations at different temperatures. Soil Biology & Biochemistry 40, 2722–2728.
Patterns of substrate utilization during long-term incubations at different temperatures.CrossRef | 1:CAS:528:DC%2BD1cXht1KnsrjE&md5=92a6fe666979670c578399700fd8b1a3CAS | open url image1

Teklay T, Nordgren A, Nyberg G, Malmer A (2007) Carbon mineralization of leaves from four Ethiopian agroforestry species under laboratory and field conditions. Applied Soil Ecology 35, 193–202.
Carbon mineralization of leaves from four Ethiopian agroforestry species under laboratory and field conditions.CrossRef | open url image1

Thiet RK, Frey SD, Six J (2006) Do growth yield efficiencies differ between soil microbial communities differing in fungal: bacterial ratios? Reality check and methodological issues. Soil Biology & Biochemistry 38, 837–844.
Do growth yield efficiencies differ between soil microbial communities differing in fungal: bacterial ratios? Reality check and methodological issues.CrossRef | 1:CAS:528:DC%2BD28XivVaqt78%3D&md5=e13183bdf3d5768a50f3228dfcfc179eCAS | open url image1

Vance ED, Brookes PC, Jenkinson DS (1987) An extraction method for measuring microbial biomass C. Soil Biology & Biochemistry 19, 703–707.
An extraction method for measuring microbial biomass C.CrossRef | 1:CAS:528:DyaL1cXjs1KqsA%3D%3D&md5=619d5036dacd709b54824b460cae8c88CAS | open url image1

Xu RK, Ji GL (2001) Effects of H2SO4 and HNO3 on soil acidification and aluminum speciation in variable and constant charge soils. Water, Air, and Soil Pollution 129, 33–43.
Effects of H2SO4 and HNO3 on soil acidification and aluminum speciation in variable and constant charge soils.CrossRef | 1:CAS:528:DC%2BD3MXlsVGjtL8%3D&md5=62d6efae0a5a97999a015c3646a45baaCAS | open url image1

Yeomans JC, Bremner JM (1988) A rapid and precise method for routine determination of organic carbon in soil. Communications in Soil Science and Plant Analysis 19, 1467–1476.
A rapid and precise method for routine determination of organic carbon in soil.CrossRef | 1:CAS:528:DyaL1cXlt1Oru7w%3D&md5=d82b7e08c8f3f16790508facae7221c1CAS | open url image1

Zak DR, Ringelberg DB, Pregitzer KS, Randlett DL, White DC, Curtis PS (1996) Soil microbial communities beneath Populus grandidentata grown under elevated atmospheric CO2. Ecological Applications 6, 257–262.
Soil microbial communities beneath Populus grandidentata grown under elevated atmospheric CO2.CrossRef | open url image1

Zhang NL, Wan SQ, Li LH, Bi J, Zhao MM, Ma KP (2008) Impacts of urea N addition on soil microbial community in a semi-arid temperate steppe in northern China. Plant and Soil 311, 19–28.
Impacts of urea N addition on soil microbial community in a semi-arid temperate steppe in northern China.CrossRef | 1:CAS:528:DC%2BD1cXhtVyju7rK&md5=08d813e0c84b992a26368e62453c4a2fCAS | open url image1

Zhao X, Xing G (2009) Variation in the relationship between nitrification and acidification of subtropical soils as affected by the addition of urea or ammonium sulfate. Soil Biology & Biochemistry 41, 2584–2587.
Variation in the relationship between nitrification and acidification of subtropical soils as affected by the addition of urea or ammonium sulfate.CrossRef | 1:CAS:528:DC%2BD1MXhtlGitr7N&md5=692f27f287ab4f9d7247979f1f6e625fCAS | open url image1


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