Temperature Affects New Carbon Input Utilization by Soil Microbes: Evidence based on a Rapid δ13C Measurement Technology

doi:10.5814/j.issn.1674-764X.2019.02.011

Abstract

Abstract:

Strong and rapid responses of soil microbial respiration to pulses, such as those from available soil organic matter (SOM) or water input from precipitation (especially in arid areas), are common. However, how soil microbes utilize new SOM inputs and the effects that temperature may have on their activities are unclear owing to the limitation in the application of traditional isotopic techniques at minute scales. In the present study, we developed a system of measuring ¹²CO₂ and δ¹³C minutely and synchronously under controlled incubation temperatures, i.e., for 48 h at 7, 10, 15, 20, and 25 °C, to explore the carbon utilization strategies of soil microbes. We measured the respiration rates of soil microbes in response to different carbon sources, i.e., added glucose (Rg) and initial SOM (Rs), as well as the total respiration rate (Rt). All responses were rapid and characterized by unimodal curves. Furthermore, the characteristic values of these curves, such as the maximum of rate (R-max), the time required to achieve R-max, and the ratio of the duration of R-max to that of 1/2 R-max, were all dependent on incubation temperature. Interestingly, temperature greatly influenced the strategy that microorganisms employed to utilize different carbon sources. The effects of temperature on the intensity of the microbial respiratory response and the ratio of Rg/Rs are important for evaluating the effect of land-use changes or variations in seasonal temperature on SOM turnover and should be considered in ecological models in future studies.

Key words: soil respiration, decomposition, isotopic, pulse, soil organic matter, turnover

CAO Yingqiu,ZHANG Zhen,XU Li,CHEN Zhi,HE Nianpeng. Temperature Affects New Carbon Input Utilization by Soil Microbes: Evidence based on a Rapid δ¹³C Measurement Technology[J]. Journal of Resources and Ecology, 2019, 10(2): 202-212.

Figures/Tables 7

Fig. 1 Changes in the respiration rate using glucose (Rg, (a)) and soil organic matter (Rs, (b)), and the total respiration rate (Rt, (c)) in a glucose addition treatment conducted at a minute scale.Note: Here, Rt = Rg + Rs; triangular symbols represent the data points of the initial respiration rate without glucose addition.

Fig. 2 The Rg-max, Rs-max, Rt-max, TRg-max, TRs-max, and TRt-max at different temperatures.Note: Rg-max, Rs-max, Rt-max represent the maximum value of glucose soil respiration rate within the 48 h test period, soil organic matter respiration rate, and total soil respiration rate, respectively; TRg-max, TRs-max, and TRt-max represent the time required to reach the Rg-max, Rs-max, and Rt-max, respectively, after glucose addition. Columns with the same lowercase letters are not significantly different at the P < 0.05.

Fig. 3 The changing trend for the ratio of Rg/Rs at different incubation temperaturesNote: Rg, the respiration rate while using glucose as the respiratory substrate; Rs, the respiration rate while using soil organic matter as the respiratory substrate.

Fig. 4 Changes in the ratio of Rg/Rt and Rs/Rt at different incubation temperaturesNote: Rg, the respiration rate while using glucose as the respiratory substrate; Rs, the respiration rate while using soil organic matter as the respiratory substrate; Rt = Rg + Rs.

Fig. 5 The accumulation of C emission from Rg, Rs, and Rt within 48 h at different temperatures.Note: Rt, total soil respiration rate; Rg, the respiration rate while using glucose as the respiratory substrate; Rs, the respiration rate while using soil organic matter as the respiratory substrate. Columns with the same lowercase letters are not significantly different at the P < 0.05 level.

Fig. 6 The relationship of the absolute changes in Rt (ΔRt), Rg (ΔRg), Rg/Rt (ΔRg/Rt), Rs/Rt (ΔRs/Rt), and Rg/Rs (ΔRg/Rs) with temperature under adequate substrate supply.Note: Rt, total soil respiration rate; Rg, the respiration rate while using glucose as the respiratory substrate; Rs, the respiration rate while using soil organic matter as the respiratory substrate; Rg/Rs, the ratio of Rg and Rs; Rg/Rt, the ratio of Rg and Rt; Rs/Rt, the ratio of Rs and Rt.

Fig. 7 Correlation test of three groups of repeated data

References 55

[1]	Baumann A, Schimmack W, Steindl H, et al.1996. Association of fallout radiocesium with soil constituents: effect of sterilization of forest soils by fumigation with chloroform.Radiation & Environmental Biophysics, 35(3): 229-233.
[2]	Bhattacharya S S, Kim K, Das S, et al.2016. A review on the role of organic inputs in maintaining the soil carbon pool of the terrestrial ecosystem.Journal of Environmental Management, 167(167): 214-227.
[3]	Blaud A, Lerch T Z, Chevallier T, et al.2012. Dynamics of bacterial communities in relation to soil aggregate formation during the decomposition of 13C-labelled rice straw.Applied Soil Ecology, 53(1): 1-9.
[4]	Brand W A.2010. Comments on “Discrepancies between isotope ratio infrared spectroscopy and isotope ratio mass spectrometry for the stable isotope analysis of plant and soil waters”.Rapid Communications in Mass Spectrometry, 24(17): 2687-2688.
[5]	Cable J M, Ogle K, Williams D G, et al, 2008. Soil texture drives responses of soil respiration to precipitation pulses in the sonoran desert: implications for climate change.Ecosystems, 11(6): 961-979.
[6]	Chamberlain P M, Bull I D, Black H I, et al.2006. Collembolan trophic preferences determined using fatty acid distributions and compound- specific stable carbon isotope values.Soil Biology & Biochemistry, 38(6): 1275-1281.
[7]	Cui M Y, Caldwell M M.1997. A large ephemeral release of nitrogen upon wetting of dry soil and corresponding root responses in the field.Plant and Soil, 191(2): 291-299.
[8]	Daniel R M, Danson M J.2010. A new understanding of how temperature affects the catalytic activity of enzymes.Trends in Biochemical Sciences, 35(10): 584-591.
[9]	Daniel R M, Danson M J, Eisenthal R, et al.2001. The temperature optima of enzymes: a new perspective on an old phenomenon.Trends in Biochemical Sciences, 26(4): 223-225.
[10]	Davidson E A, Janssens I A.2006. Temperature sensitivity of soil carbon decomposition and feedbacks to climate change.Nature, 440(7081): 165-173.
[11]	De Nobili M, Contin M, Mondini C, et al.2001. Soil microbial biomass is triggered into activity by trace amounts of substrate.Soil Biology & Biochemistry, 33(9): 1163-1170.
[12]	De Troyer I, Amery F, Van Moorleghem C, et al.2011. Tracing the source and fate of dissolved organic matter in soil after incorporation of a 13C labelled residue: A batch incubation study.Soil Biology & Biochemistry, 43(3): 513-519.
[13]	Deng Q, Cheng X L, Hui D F, et al.2016. Soil microbial community and its interaction with soil carbon and nitrogen dynamics following afforestation in central China.Science of The Total Environment, 541: 230-237.
[14]	Dijkstra F A, Cheng W, Johnson D W, et al.2006. Plant biomass influences rhizosphere priming effects on soil organic matter decomposition in two differently managed soils.Soil Biology & Biochemistry, 38(9): 2519-2526.
[15]	Fontaine S, Mariotti A, Abbadie L, et al.2003. The priming effect of organic matter: a question of microbial competition?Soil Biology & Biochemistry, 35(6): 837-843.
[16]	Gallaher R N, Weldon C O, Boswell F C.1976. A semiautomated procedure for total nitrogen in plant and soil samples. Soil Science Society of America Journal, 40(6): 887-889.
[17]	Gregorich E G, Beare M H, Stoklas U, et al.2003. Biodegradability of soluble organic matter in maize-cropped soils.Geoderma, 113(3): 237-252.
[18]	He N P, Wang R L, Gao Y, et al.2013. Changes in the temperature sensitivity of SOM decomposition with grassland succession: implications for soil C sequestration.Ecology & Evolution, 3(15): 5045-5054.
[19]	Ise T, Moorcroft P R.2006. The global-scale temperature and moisture dependencies of soil organic carbon decomposition: an analysis using a mechanistic decomposition model.Biogeochemistry, 80(3):217-231.
[20]	Kempner E S, Haigler H T.1982. The influence of low temperature on the radiation sensitivity of enzymes.Journal of Biological Chemistry, 257(22): 13297-13299.
[21]	Kendall C, Silva S R, Kelly V J, et al.2001. Carbon and nitrogen isotopic compositions of particulate organic matter in four large river systems across the United States.Hydrological Processes, 15(7): 1301-1346.
[22]	Lee P S, Majkowski R F.1986. High resolution infrared diode laser spectroscopy for isotope analysis—Measurement of isotopic carbon monoxide.Applied Physics Letters, 48(10): 619-621.
[23]	Leis H J, Gleispach H, Malle E.1988. A convenient route to stable-isotope- labelled compounds for use in quantitative gas chromatography/mass spectrometry.Rapid Communications in Mass Spectrometry, 2(12): 263-265.
[24]	Li J, He N P, Wei X H, et al.2015. Changes in temperature sensitivity and activation energy of soil organic matter decomposition in different Qinghai-Tibet Plateau grasslands.Plos One, 10(7): 1-14.
[25]	Li J, He N P, Xu L, et al.2017. Asymmetric responses of soil heterotrophic respiration to rising and decreasing temperatures.Soil Biology & Biochemistry, 106(1): 18-27.
[26]	Lipson D A, Schmidt S K, Monson R K, et al.2000. Carbon availability and temperature control the post-snowmelt decline in alpine soil microbial biomass.Soil Biology & Biochemistry, 32(4): 441-448.
[27]	Liu E, Wang J, Zhang Y, et al.2015. Priming effect of (13) C-labelled wheat straw in no-tillage soil under drying and wetting cycles in the Loess Plateau of China.Scientific Reports, 5(1): 13826-13826.
[28]	Liu Y, He N P, Zhu J X, et al.2017. Regional variation in the temperature sensitivity of soil organic matter decomposition in China's forests and grasslands. Global Change Biology, 23(8): 3393-3402.
[29]	Liu Y, Wen X F, Zhang Y H, et al.2018. Widespread asymmetric response of soil heterotrophic respiration to warming and cooling.Science of the Total Environment, 635: 423-431.
[30]	Lloyd J, Taylor J A.1994. On the temperature dependence of soil respiration. Functional Ecology, 8(3): 315-323.
[31]	Lundquist E J, Jackson L E, Scow K M, et al.1999. Wet-dry cycles affect dissolved organic carbon in two California agricultural soils.Soil Biology & Biochemistry, 31(7): 1031-1038.
[32]	Moore-Kucera J, Dick R P, 2008. Application of 13C-labeled litter and root materials for in situ decomposition studies using phospholipid fatty acids. Soil Biology & Biochemistry, 40(10): 2485-2493.
[33]	Mu C C, Zhang T J, Zhang X, et al.2016. Sensitivity of soil organic matter decomposition to temperature at different depths in permafrost regions on the northern Qinghai-Tibet Plateau.European Journal of Soil Science, 67(6): 773-781.
[34]	Nelson D W, Sommers L E, Sparks D L, et al.1996. Total carbon, organic carbon, and organic matter.Methods of Soil Analysis, 9(6): 961-1010.
[35]	Paterson E, Gebbing T, Abel C, et al.2007. Rhizodeposition shapes rhizosphere microbial community structure in organic soil.New Phytologist, 173(3): 600-610.
[36]	Phillips J D, Marion D A.2007. Soil geomorphic classification, soil taxonomy, and effects on soil richness assessments.Geoderma, 141(1-2): 89-97.
[37]	Pietikainen J, Pettersson M, Baath E, et al.2005. Comparison of temperature effects on soil respiration and bacterial and fungal growth rates.FEMS Microbiology Ecology, 52(1): 49-58.
[38]	Reid J, Adair E C, Hobbie S E, et al.2012. Biodiversity, nitrogen deposition, and CO2 affect grassland soil carbon cycling but not storage.Ecosystems, 15(4): 580-590.
[39]	Sawada K, Funakawa S, Kosaki T, et al.2016. Short-term respiration responses to drying-rewetting in soils from different climatic and land use conditions.Applied Soil Ecology, 103: 13-21.
[40]	Schaeffer S M, Evans R D.2005. Pulse additions of soil carbon and nitrogen affect soil nitrogen dynamics in an arid Colorado Plateau shrubland.Oecologia, 145(3): 425-433.
[41]	Schulze E D, Turner N C, Nicolle D, et al.2006. Leaf and wood carbon isotope ratios, specific leaf areas and wood growth of Eucalyptus species across a rainfall gradient in Australia.Tree Physiology, 26(4): 479-492.
[42]	Schwinning S, Sala O E.2004. Hierarchy of responses to resource pulses in arid and semi-arid ecosystems.Oecologia, 141(2): 211-220.
[43]	Shahbaz M, Kumar A, Kuzyakov Y, et al.2018. Priming effects induced by glucose and decaying plant residues on SOM decomposition: A three- source 13C/ 14C partitioning study.Soil Biology & Biochemistry, 121: 138-146.
[44]	Shi A, Marschner P.2014. Drying and rewetting frequency influences cumulative respiration and its distribution over time in two soils with contrasting management.Soil Biology & Biochemistry, 72: 172-179.
[45]	Song X L, Zhu J X, He N P, et al.2017.Asynchronous pulse responses of soil carbon and nitrogen mineralization to rewetting events at a short-term: Regulation by microbes.Scientific Reports, 7(1):7492.
[46]	Unger S, Cristina Máguas, Pereira J S, et al.2010. The influence of precipitation pulses on soil respiration - Assessing the “Birch effect” by stable carbon isotopes.Soil Biology & Biochemistry, 42(10): 1800-1810.
[47]	Van Geldern R, Barth J A.2012. Optimization of instrument setup and post-run corrections for oxygen and hydrogen stable isotope measurements of water by isotope ratio infrared spectroscopy (IRIS).Limnology and Oceanography-methods, 10(12): 1024-1036.
[48]	Wang Q, He N P, Liu Y, et al.2016. Strong pulse effects of precipitation events on soil microbial respiration in temperate forests.Geoderma, 275(1): 67-73.
[49]	Wang W, Liu W Q, Zhang T S, et al.2013. Measurements of stable isotopes in atmospheric CO2 and H2O by open-path Fourier transform infrared spectrometry.Spectroscopy & Spectral Analysis, 33(8): 2017-2023.
[50]	Wildung R E, Garland T R, Buschbom R L, et al.1975. The interdependent effects of soil temperature and water content on soil respiration rate and plant root decomposition in arid grassland soils.Soil Biology & Biochemistry, 7(6): 373-378.
[51]	Williams M A, Rice C W.2007. Seven years of enhanced water availability influences the physiological, structural, and functional attributes of a soil microbial community.Applied Soil Ecology, 35(3): 535-545.
[52]	Xu Z W, Yu G R, Zhang X Y, et al.2015. The variations in soil microbial communities, enzyme activities and their relationships with soil organic matter decomposition along the northern slope of Changbai Mountain.Applied Soil Ecology, 86(86): 19-29.
[53]	Yan J F, Wang L, Hu Y, et al.2018. Plant litter composition selects different soil microbial structures and in turn drives different litter decomposition pattern and soil carbon sequestration capability.Geoderma, 319(2): 194-203.
[54]	Yu X N, Huang Y M, Li E H, et al.2018. Effects of rainfall and vegetation to soil water input and output processes in the Mu Us Sandy Land, northwest China.Catena, 161(1): 96-103.
[55]	Zhang W D, Wang X F, Wang S L, et al.2013. Addition of external organic carbon and native soil organic carbon decomposition: a meta- analysis.Plos One, 8(2): 1-6.

Temperature Affects New Carbon Input Utilization by Soil Microbes: Evidence based on a Rapid δ¹³C Measurement Technology

RichHTML

PDF (PC)

Knowledge

Abstract

Cite this article

share this article

Figures/Tables 7

References 55

Related Articles 14

Recommended Articles

Metrics

Comments

[1]	LIU Xianzhao*. A Comparative Decomposition Analysis of the Factors Driving Energy-related Carbon Emissions from Three Typical Provinces in China: Jiangsu, Henan and Inner Mongolia [J]. Journal of Resources and Ecology, 2020, 11(5): 483-498.
[2]	DU Wei,WU Shanmei,NIE Cheng,LI Yue,SHAO Rui,LIU Yinghui,SUN Nan. Soil Respiration Dynamics and Influencing Factors in Typical Steppe of Inner Mongolia under Long-term Nitrogen Addition [J]. Journal of Resources and Ecology, 2019, 10(2): 155-162.
[3]	LV Ligang, LI Yongle, SUN Yan. The Spatio-temporal Pattern of Regional Land Use Change and Eco-environmental Responses in Jiangsu, China [J]. Journal of Resources and Ecology, 2017, 8(3): 268-276.
[4]	YANG Hao, HE Nianpeng, LI Shenggong, YU Guirui, GAO Yang, WANG Ruomeng. Impact of Land Cover on Temperature and Moisture Sensitivity of Soil Organic Matter Mineralization in Subtropical Southeastern China [J]. Journal of Resources and Ecology, 2016, 7(2): 85-91.
[5]	JIN Tao, QING Xiaoyu, HUANG Liyan. Changes in Grain Production and the Optimal Spatial Allocation of Water Resources in China [J]. Journal of Resources and Ecology, 2016, 7(1): 28-35.
[6]	LI Yanmei*, ZHAO Jianfeng and LIU Guangsheng. Decomposition Analysis of Carbon Emissions Growth of Tertiary Industry in Beijing [J]. Journal of Resources and Ecology, 2015, 6(5): 324-330.
[7]	LIU Junling, WANG Ke, ZOU Ji. The Net Flow of Carbon Emissions Embodied in Trade of China [J]. Journal of Resources and Ecology, 2015, 6(3): 146-154.
[8]	HUANG Qi, KANG Jiancheng, HUANG Chenhao. Construction of the Comprehensive Energy Consumption Assessment Model for Star-rated Hotels and the Difference Analysis [J]. Journal of Resources and Ecology, 2015, 6(3): 164-171.
[9]	LIU Yi, TENG Fei, SONG Jinping, Catherine BAUMONT. Decomposition Analysis of Changes in Metropolitan Energy Consumption in China Based on the Logarithmic Mean Divisia Index [J]. Journal of Resources and Ecology, 2014, 5(3): 228-236.
[10]	LI Yanmei, ZHAO Jianfeng, YANG Tao, CHEN Bao. Structural Decomposition Analysis of the Decline in China’s CO₂ Emission Intensity 2005-2010 [J]. Journal of Resources and Ecology, 2013, 4(4): 311-316.
[11]	GUO Juan, LIU Changxin, SUN Ping. Carbon Emissions from Industrial Sectors in China: Driving Factors and the Potential for Emission Reduction [J]. Journal of Resources and Ecology, 2013, 4(2): 132-140.
[12]	ZHANG Leqin, CHEN Suping, ZHU Yawen, XU Xinwang. The Measurement of Carbon Emission Effect of Construction Land Changes in Anhui Province Based on the Extended LMDI Model [J]. Journal of Resources and Ecology, 2013, 4(2): 186-192.
[13]	Siegfried FLEISCHER. Interaction between N and C in Soil Has Consequences for Global Carbon Cycling [J]. Journal of Resources and Ecology, 2012, 3(1): 16-19.
[14]	XIAO Yu, AN Kai, XIE Gaodi, LU Chunxia. Evaluation of Ecosystem Services Provided by 10 Typical Rice Paddies in China [J]. Journal of Resources and Ecology, 2011, 2(4): 328-337.