Abstract
Soil microbial community structure and gas exchange (CH4, N2O) were investigated in a rice paddy field, located in the Po plain, Italy. At eight sampling dates—representative for different soil conditions and crop stages—microbial community structure was characterized by phospholipid fatty acid (PLFA) analysis. Principal component analyses revealed differences in community composition as well as in soil fluxes during the monitored year. The vertical distribution of PLFAs was investigated by sampling at 0–15 and 15–30 cm; the uniformity in soil properties through the soil profile resulted in a vertical homogeneity of microbial biomass and community composition. Only temporary variations of soil conditions led to a distinction in microbial populations with depth. The ratio of Gram-positive to Gram-negative bacteria was higher in flooded than in non-flooded soils. The saturated and methyl-branched fatty acids typically present in Gram-positive bacteria appeared to be indicators of flooded and waterlogged conditions, which were favourable for CH4 emission as well as for N2O consumption. Gram-negative bacteria were instead most important for characterization of aerobic conditions and for the decomposition of fresh residues. In terms of microbial processes, the 16:1ω9 fatty acid appeared to be correlated with N2O fluxes.
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Andersen AJ, Petersen SO (2009) Effects of C and N availability and soil-water potential interactions on N2O evolution and PLFA composition. Soil Biol Biochem 41(8):1726–1733
Attard E, Recous S, Chabbi A, De Berranger C, Guillaumaud N, Labreuche J, Philippot L, Schmid B, Leroux X (2011) Soil environmental conditions rather than denitrifier abundance and diversity drive potential denitrification after changes in land uses. Glob Change Biol 17:1975–1989
Aulakh MS, Wassmann R, Rennenberg H (2001a) Methane transport capacity of twenty-two rice cultivars from five major Asian rice-growing countries. Agric Ecosyst Environ 91:59–71
Aulakh MS, Wassmann R, Rennenberg H (2001b) Methane emissions from rice fields: quantification, mechanisms, role and mitigation options. Adv Agron 70:193–260
Aulakh MS, Wassmann R, Bueno C, Rennenberg H (2001c) Impact of root exudates of different cultivars and plant development stages of rice (Oryza sativa L.) on methane production in a paddy soil. Plant Soil 230:77–86
Bååth E, Anderson TH (2003) Comparison of soil fungal/bacterial ratios in a pH gradient using physiological and PLFA-based techniques. Soil Biol Biochem 35:955–963
Bai Q, Gattinger A, Zelles L (2000) Characterisation of microbial consortia in paddy rice soil by phosholipid analysis. Microbiol Ecol 39:273–281
Bilek RS, Tyler SC, Sass RL, Fisher FM (1999) Differences in CH4 oxidation and pathways of production between rice cultivars deduced from measurements of CH4 flux and δ13C of CH4 and CO2. Global Biogeochem Cycles 13:1029–1044
Bossio DA, Scow KM (1995) Impact of carbon and flooding on the metabolic diversity of microbial communities in soils. Appl Environ Microbiol 61:4043–4050
Bossio DA, Scow KM (1998) Impacts of carbon and flooding on soil microbial communities: phosholipid fatty acid profiles and substrate utilization patterns. Microbiol Ecol 35:265–278
Burger M, Jackson LE, Lundquist EJ, Louie DT, Miller RL, Rolston DE, Scow KM (2005) Microbial responses and nitrous oxide emissions during wetting and drying of organically and conventionally managed soil under tomatoes. Biol Fertil Soils 42:109–118
Cai Z, Xing G, Yan X, Xu H, Tsuruta H, Yagi K, Minami K (1997) Methane and nitrous oxide emissions from rice paddy fields as affected by nitrogen fertilizers and water management. Plant Soil 196:7–14
Chidthaisong A, Conrad R (2000) Turnover of glucose and acetate coupled to reduction of nitrate, ferric iron and sulfate and to methanogenesis in anoxic rice field soil. FEMS Microbiol Ecol 31:73–86
Chidthaisong A, Watanabe I (1997a) Methane formation and emission from rice soil incorporated with13C-labeled rice straw. Soil Biol Biochem 29:1173–1181
Chidthaisong A, Watanabe I (1997b) Changes in concentration and δ13C values of soil entrapped CH4 and CO2 in flooded rice soil. Biol Fertil Soils 24:70–75
Conrad R (1993) Mechanisms controlling methane emission from wetland rice fields. In: Oremland RS (ed) The biogeochemistry of global change: radiative trace gases. Chapman and Hall, New York, pp 317–335
Conrad R (1996) Soil microorganisms as controllers of atmospheric trace gases (H2, CO, CH4, OCS, N2O, and NO). Microbiol Rev 60:609–640
Conrad R, Klose M (2000) Selective inhibition of reactions involved in methanogenesis and fatty acid production on rice roots. FEMS Microbiol Ecol 34:27–34
Coûteau MM, Bottner P, Berg B (1995) Litter decomposition, climate and litter quality. Trends Ecol Evol 10:63–66
Davidson EA, Swank WT, Perry TO (1986) Distinguishing between nitrification and denitrification as sources of gaseous nitrogen production in soil. Appl Environ Microbiol 52:1280–1286
Egozcue JJ, Pawlowsky-Glahn V, Mateu-Figueros F, Barcel′o-Vidal C (2003) Isometric logratio transformations for compositional data analysis. Math Geol 35:279–300
Fay L, Richli U (1991) Location of double bonds in polyunsaturated fatty acids by gas chromatography—mass spectroscopy after 4,4-dimethyloxazoline derivatization. J Chromatogr A 541:89–98
Fierer N, Schimel JP, Holden PA (2003) Variations in microbial community composition through two soil depth profiles. Soil Biol Biochem 35:167–176
Firestone MK, Davidson EA (1989) Microbiological basis of NO and N2O production and consumption in soil. In: Andreae MO, Schimel DS (eds) Exchange of trace gases between terrestrial ecosystems and the atmosphere. Wiley and Sons, Chichester, pp 7–21
Frostegård A, Tunlid A, Bååth E (1991) Microbial biomass measured as total lipid phosphate in soils of different organic content. J Microbiol Meth 14:151–163
Frostegård Å, Tunlid A, Bååth E (2011) Use and misuse of PLFA measurements in soils. Soil Biol Biochem 43:1621–1625
Green CT, Scow KM (2000) Analysis of phospholipid fatty acids (PLFA) to characterize microbial communities in acquifers. Hydrogeol J 8:126–141
Grogan DW, Cronan JE (1997) Cyclopropane ring formation in membrane lipids of bacteria. Microbiol Mol Biol Rev 61:429–441
Guckert JB, Antworth CP, Nichols PD, White DC (1985) Phospholipid, ester-linked fatty acid profiles as reproducible assays for changes in prokaryotic community structure of estuarine sediments. FEMS Microbiol Lett 31:147–158
Hackl E, Pfeffer M, Donat C, Bachmann G, Zechemeister-Boltenstern S (2005) Composition of the microbial communities in the mineral soil under different types of natural forest. Soil Biol Biochem 37:661–671
Harwood JL, Russel NJ (1984) Lipids in plants and microbes. Allen and Unwin, London
Heipieper HJ, Meinhardt F, Segura A (2003) The cis-trans isomerase of unsaturated fatty acids in Pseudomonas and Vibrio: biochemistry, molecular biology and physiological function of a unique stress adaptive mechanism. FEMS Microbiol Lett 229:1–7
Ibekwe AM, Kennedy AC (1998) Phospholipid fatty acid profiles and carbon utilization patterns for analysis of microbial community structure under field and greenhouse conditions. FEMS Microb Ecol 26:151–163
IPCC (2007) Climate Change 2007 Synthesis Report. In: Pachauri RK and Reisinger A (eds) Contribution of working groups I, II and III to the fourth assessment report of the intergovernmental panel on climate change. Core Writing Team, IPCC, Geneva
IUSS/ISRIC/FAO (2006) World Reference Base for Soil Resources (2006) World soil resources reports 103. FAO, Rome
Jandl G, Leinweber P, Schulten HR, Ekschmitt K (2005) Contribution of primary organic matter to the fatty acid pool in agricultural soils. Soil Biol Biochem 37:1033–1041
Jantzen E (1984) Analysis of cellular components in bacterial classification and diagnosis. In: Odham G, Larsson L, Mardh PA (eds) Gas chromatography/mass spectrometry—applications in microbiology. Plenum Press, New York, pp 257–302
Keeney DR, Nelson DW (1982) Nitrogen-Inorganic forms. In: Page AL, Miller RH (eds) Methods of soil analysis, part 2, chemical and microbiological properties. Agron Monogr 9, 2nd ed, ASA and SSSA, Madison, pp 643–698
Kirk G (2004) The biogeochemistry of submerged soils. Wiley and Sons, Chichester
Klamer M, Baath E (1998) Microbial community dynamics composting of straw material studied using phospholipid fatty acid analysis. FEMS Microb Ecol 27:9–20
Knivett VA, Cullen J (1965) Some factors affecting cyclopropane acid formation in Escherichia coli. Biochem J 96:771–776
Kroppenstedt RM (1985) Fatty acids and menaquinone analysis of actinomycetes and related organisms. In: Goodfellow M, Minnikin DE (eds) Chemical methods in bacterial systematics. Academic Press, London, pp 173–199
Lechevalier MP (1989) Lipids in bacterial taxonomy. In: O’Leary WM (ed) Practical handbook of microbiology. CRC, Boca Raton, pp 455–561
Livingston GP, Hutchinson GL (1995) Enclosure-based measurement of trace gas exchange: Application and sources of error. In: Harriss PC (ed) Matson PA. Measuring Emissions from Soil and Water. Blackwell Science Cambridge University Press, Biogenic Trace Gases, pp 14–51
Lu Y, Abraham WR, Conrad R (2007) Spatial variation of active microbiota in the rice rhizosphere revealed by in situ stable isotope probing of phospholipid fatty acids. Environ Microbiol 9:474–481
Ma WK, Farrell RE, Siciliano SD (2011) Nitrous oxide emissions from ephemeral wetland soils are correlated with microbial community composition. Front Microbiol 2:1–11
Macalady JL, Mack EE, Nelson DC, Scow KM (2000) Sediment microbial community structure and mercury methylation in mercury-polluted clear lake California. Appl Environ Microbiol 66(4):1479–1488
O’Leary WM, Wilkinson SG (1988) Gram-positive bacteria. In: Ratledge C, Wilkinson SG (eds) Microbial lipids, vol 1. Academic Press, London, pp 117–201
Olsson PA (1999) Signature fatty acids provide tools for determination of the distribution and interactions of mycorrhizal fungi in soil. FEMS Microbial Ecol 29:303–310
Parkers RJ, Taylor J (1983) The relationship between fatty acid distributions and bacterial respiratory types in contemporary marine sediments. Estuar Coast Shelf Sci 16:173–189
Pinkart HC, Ringelberg DB, Piceno YM, Macnaughton SJ, White DC (2002) Biochemical approaches to biomass measurements and community structure analysis. In: Hurst CJ, Crawford RL, Knudsen GR, McInerney MJ, Stetzenbach LD (eds) Manual of environmental microbiology, 2nd edn. ASM Press, Washington, pp 101–113
Raich JW, Schlesinger WH (1992) The global carbon dioxide flux in soil respiration and its relationship to vegetation and climate. Tellus 44B:81–99
Rajendran N, Matsuda O, Imamura N, Urushigawa Y (1992) Variation in microbial biomass and community structure in sediments of eutrophic bays as determined by phospholipid ester-linked fatty acids. Appl Environ Microbiol 58:562–571
Ratledge C, Wilkinson SG (1988) Microbial lipids, vol 1. Academic Press, London
Reed DW, Fujita Y, Delwiche ME, Blackwelder DB, Sheridan PP, Uchida T, Colwell FS (2002) Microbial communities from methane hydrate-bearing deep marine sediments in a forearc basin. Appl Environ Microbiol 68(8):3759–3770
Reichardt W, Briones A, de Jesus R, Padre B (2001) Microbial population shifts in experimental rice systems. Appl Soil Ecol 17:151–163
Rothfuss F, Conrad R (1993) Vertical profiles of CH4 concentrations, dissolved substrates and processes involved in CH4 production in a flooded italian rice field. Biogeochem 18:137–152
Schaufler G, Kitzler B, Schindlbacher A, Skiba U, Sutton MA, Zechmeister-Boltenstern S (2010) Greenhouse gas emissions from European soils under different land use: effects of soil moisture and temperature. Eur J Soil Sci 61:683–696
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 Biol Biochem 31:831–838
Soil Survey Staff (1999) Soil taxonomy: a basic system of soil classification for making and interpreting soil surveys, 2nd edn. Natural Resources Conservation Service. U.S. Department of Agriculture Handbook 436
Spitzer V (1997) Structure analysis of fatty acids by gas chromatography low resolution electron impact mass spectrometry of their 4,4-dimethyloxazoline derivatives: a review. Prog Lipid Res 35:387–408
Steenwerth KL, Jackson LE, Calderon FJ, Stromberg MR, Scow KM (2002) Soil microbial community composition and land use history in cultivated and grassland ecosystems of coastal California. Soil Biol Biochem 34:1599–1611
Su YH, Yang XY (2009) Interactions between selected PAHs and microbial community in rhizosphere of a paddy soil. Sci Total Environ 407(3):1027–1034
Sundh I, Börjesson G, Tunlid A (2000) Methane oxidation and phospholipid fatty acid composition in a podzolic soil profile. Soil Biol Biochem 32:1025–1028
White DC (1993) In situ measurement of microbial biomass, community structure and nutritional status. Philos Trans R Soc Lond B 344:59–67
White DC, Davis WM, Nickels JS, King JD, Bobbie RJ (1979) Determination of the sedimentary microbial biomass by extractable lipid phosphate. Oecologia 40:51–62
Wilkinson S, Anderson J, Scardelis S, Tisiafouli M, Taylor A, Wolters V (2002) PLFA profiles of microbial communities in decomposing conifer litters subject to moisture stress. Soil Biol Biochem 34:189–200
Wolf I, Russow R (2000) Different pathways of formation of N2O, N2 and NO in black earth soil. Soil Biol Biochem 32:229–239
Zelles L (1999) Fatty acid patterns of phospholipids and lipopolysaccharides in the characterization of microbial communities in soil: a review. Biol Fertil Soils 29:111–129
Acknowledgments
This work was partly funded by the European Commission through the NitroEurope project 017841. We received substantial support from Marco Gastel, the owner of Cascina Comuna (Castellaro de’ Giorgi). We thank Fabio Moia for help with field work, Ignacio Goded and Marlene Duerr for technical support, Michael Pfeffer for laboratory assistance.
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Ferré, C., Zechmeister-Boltenstern, S., Comolli, R. et al. Soil microbial community structure in a rice paddy field and its relationships to CH4 and N2O fluxes. Nutr Cycl Agroecosyst 93, 35–50 (2012). https://doi.org/10.1007/s10705-012-9497-x
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DOI: https://doi.org/10.1007/s10705-012-9497-x