Open Access Open Access  Restricted Access Subscription Access

Changes in pmoA Gene Containing Methanotrophic Population and Methane Oxidation Potential of Dry Deciduous Tropical Forest Soils


Affiliations
1 Centre of Advanced Study in Botany, Institute of Science, Banaras Hindu University, Varanasi 221 005, India
 

In natural ecosystems such as forests topographical gradients, species composition variability and seasonality, are the potential drivers of methane (CH4) metabolism, and thus, of the population size and activities of methane oxidizing bacteria (MOB). To test the hypothesis that topography, tree species and seasonal variability influence MOB population and soil methane oxidation potential (MOP), we conducted two consecutive years of study selecting three sites in a dry deciduous tropical forest in Chandauli district of eastern Uttar Pradesh, India. The qPCR results showed a large variation in MOB population size (copies g−1 dws), ranging from 1.0 × 106 to 2.1 × 107 and 9.0 × 105 to 2.2 × 107 during 2016 and 2017 respectively. The distribution of MOB population revealed the trend: hilltop > middle > hillbase with its maxima in the winter and minima in the rainy season. Laboratory incubation study revealed a similar trend in soil MOP (ng CH4 g−1 h−1 dws), it varied from 10.6 to 20.6 and 10.5 to 20.7 during 2016 and 2017 respectively. The outer canopy soils showed lower MOB population and MOP compared to under canopy soils of tree species Butea monosperma, Madhuca indica and Tectona grandis during both years of study. The topography, season and tree species significantly influenced the MOB population size and MOP. Soil MOP showed a highly significant correlation (r = 0.89; p < 0.01) with MOB population, and a negative correlation was found with soil moisture (r = 0.76; p < 0.01). The results indicate that the dry deciduous tropical forest soils are potential sinks of atmospheric CH4 wherein, the MOB population characteristically responds to topographical changes, tree species and seasonal shifts driving collectively the overall MOP of forest soils.

Keywords

Methanotrophs, Topography, Season, Tree Species, Tropical Dry Deciduous Forest.
User
Notifications
Font Size

  • Ciais, P. et al., Carbon and other biogeochemical cycles. In Climate Change 2013: The Physical Science Basis. Contribution of Working Group I to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change (eds Stocker, T. F. et al.), Cambridge University Press, Cambridge, United Kingdom and New York, NY, USA, 2013, pp. 465–570.
  • IPCC, Climate Change 2013: The Physical Science Basis. Contribution of Working Group I to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change, Cambridge University Press, Cambridge, United Kingdom and New York, NY, USA, 2013, 1535.
  • Saunois, M. et al., The global methane budget 2000–2012. Earth Syst. Sci. Data, 2016, 8(2), 697–751.
  • Murguia-Flores, F., Arndt, S., Ganesan, A. L., Murray-Tortarolo, G. and Hornibrook, E. R. C., Soil Methanotrophy Model (MeMo v1.0): a process-based model to quantify global uptake of atmospheric methane by soil. Geosci. Model Dev., 2018, 11(6), 2009– 2032.
  • Dutaur, L. and Verchot, L. V., A global inventory of the soil CH4 sink. Global Biogeochem. Cy., 2007, 21(4), 1–9.
  • Hanson, R. S. and Hanson, T. E., Methanotrophic bacteria. Microbiol. Rev., 1996, 60(2), 439–471.
  • Dubey, S. K., Microbial ecology of methane emission in rice agroecosystem: a review. Appl. Ecol. Environ. Res., 2005, 3(2), 1– 27.
  • Guckland, A., Flessa, H. and Prenzel, J., Controls of temporal and spatial variability of methane uptake in soils of a temperate deciduous forest with different abundance of European beech (Fagus sylvatica L.). Soil Biol. Biochem., 2009, 41(8), 1659–1667.
  • Ishizuka, S., Sakata, T. and Ishizuka, K., Methane oxidation in Japanese forest soils. Soil Biol. Biochem., 2000, 32(6), 769–777.
  • Jang, I., Lee, S., Zoh, K. D. and Kang, H., Methane concentrations and methanotrophic community structure influence the response of soil methane oxidation to nitrogen content in a temperate forest. Soil Biol. Biochem., 2011, 43(3), 620–627.
  • Ueyama, M. et al., Methane uptake in a temperate forest soil using continuous closed-chamber measurements. Agr. Forest Meteorol., 2015, 213, 1–9.
  • Singh, J. S. et al., Effect of soil nitrogen, carbon and moisture on methane uptake by dry tropical forest soils. Plant Soil, 1997, 196(1), 115–121.
  • Yan, Y. P. et al., Fluxes of CH4 and N2O from soil under a tropical seasonal rain forest in Xishuangbanna, Southwest China. J. Environ. Sci. China, 2008, 20(2), 207–215.
  • Yu, L. J., Huang, Y., Zhang, W., Li, T. T. and Sun, W. J., Methane uptake in global forest and grassland soils from 1981 to 2010. Sci. Total Environ., 2017, 607, 1163–1172.
  • Dubey, S. K., Sinha, A. S. K. and Singh, J. S., Differential inhibition of CH4 oxidation in bare, bulk and rhizosphere soils of dryland rice field by nitrogen fertilizers. Basic Appl. Ecol., 2002, 3(4), 347–355.
  • Steudler, P. A., Bowden, R. D., Melillo, J. M. and Aber, J. D., Influence of nitrogen-fertilization on methane uptake in temperate forest soils. Nature, 1989, 341(6240), 314–316.
  • Tate, K. R. et al., Methane uptake in soils from Pinus radiata plantations, a reverting shrubland and adjacent pastures: effects of land-use change, and soil texture, water and mineral nitrogen. Soil Biol. Biochem., 2007, 39(7), 1437–1449.
  • Luo, G. J., Kiese, R., Wolf, B. and Butterbach-Bahl, K., Effects of soil temperature and moisture on methane uptake and nitrous oxide emissions across three different ecosystem types. Biogeosciences, 2013, 10(5), 3205–3219.
  • Benstead, J. and King, G. M., The effect of soil acidification on atmospheric methane uptake by a Maine forest soil. FEMS Microbiol. Ecol., 2001, 34(3), 207–212.
  • Zhang, J. F., Li, Z. J., Ning, T. Y. and Gu, S. B., Methane uptake in salt-affected soils shows low sensitivity to salt addition. Soil Biol. Biochem., 2011, 43(7), 1434–1439.
  • Shrestha, P. M., Kammann, C., Lenhart, K., Dam, B. and Liesack, W., Linking activity, composition and seasonal dynamics of atmospheric methane oxidizers in a meadow soil. ISME J., 2012, 6(6), 1115–1126.
  • Wolf, K., Flessa, H. and Veldkamp, E., Atmospheric methane uptake by tropical montane forest soils and the contribution of organic layers. Biogeochemistry, 2012, 111, 469–483.
  • Reay, D. S., Nedwell, D. B., McNamara, N. and Ineson, P., Effect of tree species on methane and ammonium oxidation capacity in forest soils. Soil Biol. Biochem., 2005, 37(4), 719–730.
  • Ishizuka, S. et al., Methane uptake rates in Japanese forest soils depend on the oxidation ability of topsoil, with a new estimate for global methane uptake in temperate forest. Biogeochemistry, 2009, 92, 281–295.
  • Mohanty, S. R., Bodelier, P. L. and Conrad, R., Effect of temperature on composition of the methanotrophic community in rice field and forest soil. FEMS Microbiol. Ecol., 2007, 62(1), 24–31.
  • Kravchenko, I. K. et al., Physicochemical and biological factors affecting atmospheric methane oxidation in gray forest soils. Microbiology, 2005, 74(2), 216–220.
  • Smith, C. J. and Osborn, A. M., Advantages and limitations of quantitative PCR (Q-PCR)-based approaches in microbial ecology. FEMS Microbiol. Ecol., 2009, 67(1), 6–20.
  • Barcena, T. G. et al., Conversion of cropland to forest increases soil CH4 oxidation and abundance of CH4 oxidizing bacteria with stand age. Appl. Soil Ecol., 2014, 79, 49–58.
  • Malghani, S. et al., Soil methanotroph abundance and community composition are not influenced by substrate availability in laboratory incubations. Soil Biol. Biochem., 2016, 101, 184–194.
  • Giri, D. D. et al., Variation in methanotrophic bacterial population along an altitude gradient at two slopes in tropical dry deciduous forest. Soil Biol. Biochem., 2007, 39(9), 2424–2426.
  • Keenan, R. J. et al., Dynamics of global forest area: results from the fao global forest resources assessment. Forest Ecol. Manage., 2015, 352, 9–20.
  • Champion, H. G. and Seth, S. K., A Revised Survey of the Forest Types of India, 1968; https://dds.crl.edu/crldelivery/23005.
  • Vishwakarma, P. and Dubey, S. K., The effect of soil type and plant age on the population size of rhizospheric methanotrophs and their activities in tropical rice soils. J. Basic Microbiol., 2007, 47(4), 351–357.
  • Bouyoucos, G. J., Hydrometer method improved for making particle size analyses of soils. Agron. J., 1962, 54(5), 464–465.
  • Piper, C. S., Soil and Plant Analysis, Inter Science Publication, Inc., Adelaide, Australia, 1944.
  • Jackson, M. L., Soil Chemical Analysis, Prentice Hall, New Jersey, USA, 1958.
  • Walkley, A., A critical examination of a rapid method for determining organic carbon in soils-effect of variations in digestion conditions and of inorganic soil constituents. Soil Sci., 1947, 63(4), 251–264.
  • APHA, Standard methods for the examination of water and wastewater. American Public Health Association, Washington, 1985.
  • Costello, A. M. and Lidstrom, M. E., Molecular characterization of functional and phylogenetic genes from natural populations of methanotrophs in lake sediments. Appl. Environ. Microbiol., 1999, 65(11), 5066–5074.
  • Bourne, D. G., Mcdonald, I. R. and Murell, J. C., Comparison of pmoA PCR primer sets as tools for investigating methanotroph diversity in three Danish soils. Appl. Environ. Microbiol., 2001, 67(9), 3802–3809.
  • Zhang, T. and Fang, H. H. P., Applications of real-time polymerase chain reaction for quantification of microorganisms in environmental samples. Appl. Microbiol. Biot., 2006, 70(3), 281–289.
  • IBM Corp. Released 2011, IBM SPSS Statistics for Windows, Version 20.0, Armonk, NY, IBM Corp.
  • Borken, W., Davidson, E. A., Savage, K., Sundquist, E. T. and Steudler, P., Effect of summer throughfall exclusion, summer drought, and winter snow cover on methane fluxes in a temperate forest soil. Soil Biol. Biochem., 2006, 38(6), 1388–1395.
  • Jang, I., Lee, H. and Kang, H., The response of nitrogen deposition to methane oxidation availability and microbial enzyme activities in forest soils. Environ. Engine. Res., 2010, 15(3), 157– 161.
  • Boeckx, P., VanCleemput, O. and Villaralvo, I., Methane oxidation in soils with different textures and land use. Nutr. Cycl. Agroecosys., 1997, 49(1–3), 91–95.
  • Adamsen, A. P. and King, G. M., Methane consumption in temperate and subarctic forest soils: rates, vertical zonation, and responses to water and nitrogen. Appl. Environ. Microbiol., 1993, 59(2), 485–490.
  • Brumme, R. and Borken, W., Site variation in methane oxidation as affected by atmospheric deposition and type of temperate forest ecosystem. Global Biogeochem. Cy., 1999, 13(2), 493–501.
  • Menyailo, O. V. and Hungate, B. A., Interactive effects of tree species and soil moisture on methane consumption. Soil Biol. Biochem., 2003, 35(4), 625–628.
  • Striegl, R. G., Mcconnaughey, T. A., Thorstenson, D. C., Weeks, E. P. and Woodward, J. C., Consumption of atmospheric methane by desert soils. Nature, 1992, 357(6374), 145–147.
  • Saynes, V., Hidalgo, C., Etchevers, J. D. and Campo, J. E., Soil C and N dynamics in primary and secondary seasonally dry tropical forests in Mexico. Appl. Soil Ecol., 2005, 29(3), 282–289.
  • Bodelier, P. L. E. and Laanbroek, H. J., Nitrogen as a regulatory factor of methane oxidation in soils and sediments. FEMS Microbiol. Ecol., 2004, 47(3), 265–277.
  • Mohanty, S. R., Bodelier, P. L. E., Floris, V. and Conrad, R., Differential effects of nitrogenous fertilizers on methane-consuming microbes in rice field and forest soils. Appl. Environ. Microbiol., 2006, 72(2), 1346–1354.
  • Bodelier, P. L. E., Roslev, P., Henckel, T. and Frenzel, P., Stimulation by ammonium-based fertilizers of methane oxidation in soil around rice roots. Nature, 2000, 403(6768), 421–424.
  • Menyailo, O. V., Abraham, W. R. and Conrad, R., Tree species affect atmospheric CH4 oxidation without altering community composition of soil methanotrophs. Soil Biol. Biochem., 2010, 42(1), 101–107.

Abstract Views: 3

PDF Views: 0




  • Changes in pmoA Gene Containing Methanotrophic Population and Methane Oxidation Potential of Dry Deciduous Tropical Forest Soils

Abstract Views: 3  |  PDF Views: 0

Authors

Yashpal Bhardwaj
Centre of Advanced Study in Botany, Institute of Science, Banaras Hindu University, Varanasi 221 005, India
Suresh Kumar Dubey
Centre of Advanced Study in Botany, Institute of Science, Banaras Hindu University, Varanasi 221 005, India

Abstract


In natural ecosystems such as forests topographical gradients, species composition variability and seasonality, are the potential drivers of methane (CH4) metabolism, and thus, of the population size and activities of methane oxidizing bacteria (MOB). To test the hypothesis that topography, tree species and seasonal variability influence MOB population and soil methane oxidation potential (MOP), we conducted two consecutive years of study selecting three sites in a dry deciduous tropical forest in Chandauli district of eastern Uttar Pradesh, India. The qPCR results showed a large variation in MOB population size (copies g−1 dws), ranging from 1.0 × 106 to 2.1 × 107 and 9.0 × 105 to 2.2 × 107 during 2016 and 2017 respectively. The distribution of MOB population revealed the trend: hilltop > middle > hillbase with its maxima in the winter and minima in the rainy season. Laboratory incubation study revealed a similar trend in soil MOP (ng CH4 g−1 h−1 dws), it varied from 10.6 to 20.6 and 10.5 to 20.7 during 2016 and 2017 respectively. The outer canopy soils showed lower MOB population and MOP compared to under canopy soils of tree species Butea monosperma, Madhuca indica and Tectona grandis during both years of study. The topography, season and tree species significantly influenced the MOB population size and MOP. Soil MOP showed a highly significant correlation (r = 0.89; p < 0.01) with MOB population, and a negative correlation was found with soil moisture (r = 0.76; p < 0.01). The results indicate that the dry deciduous tropical forest soils are potential sinks of atmospheric CH4 wherein, the MOB population characteristically responds to topographical changes, tree species and seasonal shifts driving collectively the overall MOP of forest soils.

Keywords


Methanotrophs, Topography, Season, Tree Species, Tropical Dry Deciduous Forest.

References





DOI: https://doi.org/10.18520/cs%2Fv118%2Fi5%2F750-758