Effects of soil organism interactions and temperature on carbon use efficiency in three different forest soils

Simin Wang, Xiaoyun Chen, Debao Li, Jianping Wu

PDF(1255 KB)
PDF(1255 KB)
Soil Ecology Letters ›› 2021, Vol. 3 ›› Issue (2) : 156-166. DOI: 10.1007/s42832-020-0067-x
RESEARCH ARTICLE
RESEARCH ARTICLE

Effects of soil organism interactions and temperature on carbon use efficiency in three different forest soils

Author information +
History +

Highlights

• Three typical forest soils and three soil organisms were collected.

Ÿ• Interactions among soils and organisms were examined by incubation experiment.

• Biotic factors mainly affect microbial CUE by changing biomass.

• Temperature regulates microbial CUE by affecting microbial respiration.

Abstract

Microbial carbon use efficiency (CUE) affects the soil C cycle to a great extent, but how soil organisms and the abiotic environment combine to influence CUE at a regional scale remains poorly understood. In the current study, microcosms were used to investigate how microbial respiration, biomass, and CUE responded to biotic and abiotic factors in natural tropical, subtropical, and temperate forests. Soil samples from the forests were collected, sterilized, and populated with one or a combination of three types of soil organisms (the fungus Botrytis cinerea, the bacterium Escherichia coli, and the nematode Caenorhabditis elegans). The microcosms were then kept at the mean soil temperatures of the corresponding forests. Microbial respiration, biomass, and CUE were measured over one-month incubation period. The results showed that microbial biomass and CUE were significantly higher, but microbial respiration lower in the subtropical and temperate forest soils than in tropical forest soil. Biotic factors mainly affected CUE by their effect on microbial biomass, while temperature affected CUE by altering respiration. Our results indicate that temperature regulates the interactive effects of soil organisms on microbial biomass, respiration, and CUE, which would provide a basis for understanding the soil C cycle in forest ecosystems.

Keywords

Biotic interactions / Carbon use efficiency / Climate gradients / Soil carbon cycle / Soil organisms / Soil respiration

Cite this article

Download citation ▾
Simin Wang, Xiaoyun Chen, Debao Li, Jianping Wu. Effects of soil organism interactions and temperature on carbon use efficiency in three different forest soils. Soil Ecology Letters, 2021, 3(2): 156‒166 https://doi.org/10.1007/s42832-020-0067-x

References

[1]
Bardgett, R.D., van der Putten, W.H., 2014. Belowground biodiversity and ecosystem functioning. Nature 515, 505–511
CrossRef Google scholar
[2]
Butterly, C.R., Armstrong, R.D., Chen, D., Tang, C., 2019. Residue decomposition and soil carbon priming in three contrasting soils previously exposed to elevated CO2. Biology and Fertility of Soils 55, 17–29
CrossRef Google scholar
[3]
Chambers, J.Q., Tribuzy, E.S., Toledo, L.C., Crispim, B.F., Higuchi, N., Santos, J.D., Araujo, A.C., Kruijt, B., Nobre, A.D., Trumbore, S.E., 2004. Respiration from a tropical forest ecosystem: partitioning of sources and low carbon use efficiency. Ecological Applications 14, 72–88
CrossRef Google scholar
[4]
Crowther, T.W., Hoogen, J.V.D., Wan, J., Mayes, M.A., Keiser, A.D., Mo, L., 2019. The global soil community and its influence on biogeochemistry. Science 365, 1–10
CrossRef Google scholar
[5]
Crowther, T.W., Jones, T.H., Boddy, L., Baldrian, P., 2011. Invertebrate grazing determines enzyme production by basidiomycete fungi. Soil Biology & Biochemistry 43, 2060–2068
CrossRef Google scholar
[6]
Crowther, T.W., Thomas, S.M., Maynard, D.S., Baldrian, P., Covey, K., Frey, S.D., van Diepen, L.T.A., van Bradford, M.A., 2015. Biotic interactions mediate soil microbial feedbacks to climate change. Proceedings of the National Academy of Sciences of the United States of America 112, 7033–7038
CrossRef Google scholar
[7]
Davidson, E.A., Janssens, I.A., 2006. Temperature sensitivity of soil carbon decomposition and feedbacks to climate change. Nature 440, 165–173
CrossRef Google scholar
[8]
Davidson, E.A., Savage, K.E., Finzi, A.C., 2014. A big-microsite framework for soil carbon modeling. Global Change Biology 20, 3610–3620
CrossRef Google scholar
[9]
De Deyn, G.B., 2013. Ecosystem Carbon and Soil Biodiversity. In: Lal, R., Lorenz, K., Hüttl, R.F., Schneider, B.U., von Braun, J., eds. Ecosystem Services and Carbon Sequestration in the Biosphere. Springer, Netherlands, 131–153.
[10]
Delucia, E.H., Drake, J.E., Thomas, R.B., Gonzalez-Meler, M., 2007. Forest carbon use efficiency: is respiration a constant fraction of gross primary production? Global Change Biology 13, 1157–1167
CrossRef Google scholar
[11]
Dillaway, D.N., Kruger, E.L., 2014. Trends in seedling growth and carbon-use efficiency vary among broadleaf tree species along a latitudinal transect in eastern North America. Global Change Biology 20, 908–922
CrossRef Google scholar
[12]
Eberwein, J.R., Oikawa, P.Y., Allsman, L.A., Jenerette, G.D., 2015. Carbon availability regulates soil respiration response to nitrogen and temperature. Soil Biology & Biochemistry 88, 158–164
CrossRef Google scholar
[13]
Estruch, C., Macek, P., Armas, C., Pistón, N., Pugnaire, F.I., 2020. Species identity improves soil respiration predictions in a semiarid scrubland. Geoderma 363, 114153
CrossRef Google scholar
[14]
Fang, J., Yu, G., Liu, L., Hu, S., Chapin, F.S. III, 2018. Climate change, human impacts, and carbon sequestration in China. Proceedings of the National Academy of Sciences of the United States of America 115, 4015–4020
CrossRef Google scholar
[15]
Fang, Y., Singh, B.P., Collins, D., Armstrong, R., van Zwieten, L., Tavakkoli, E., 2020. Nutrient stoichiometry and labile carbon content of organic amendments control microbial biomass and carbon-use efficiency in a poorly structured sodic-subsoil. Biology and Fertility of Soils 56, 219–223
CrossRef Google scholar
[16]
Fu, S., Ferris, H., Brown, D., Plant, R., 2005. Does the positive feedback effect of nematodes on the biomass and activity of their bacteria prey vary with nematode species and population size? Soil Biology & Biochemistry 37, 1979–1987
CrossRef Google scholar
[17]
Geisen, S., Briones, M., Gan, H., Behan-Pelletier, V., Friman, V.P., Groot, G., Hannula, S., Lindo, Z., Philippot, L., Tivnov, A., Wall, D., 2019. A methodological framework to embrace soil biodiversity. Soil Biology & Biochemistry 136, 107536
CrossRef Google scholar
[18]
Geyer, K.M., Kyker-Snowman, E., Grandy, A.S., Frey, S.D., 2016. Microbial carbon use efficiency: accounting for population, community, and ecosystem-scale controls over the fate of metabolized organic matter. Biogeochemistry 127, 173–188
CrossRef Google scholar
[19]
Giardina, C.P., Ryan, M.G., 2000. Evidence that decomposition rates of organic carbon in mineral soil donot vary with temperature. Nature 404, 858–861
CrossRef Google scholar
[20]
Graaff, M.A.D., Adkins, J., Kardol, P., Throop, H.L., 2015. A meta-analysis of soil biodiversity impacts on the carbon cycle. Soil (Göttingen) 1, 907–945
CrossRef Google scholar
[21]
Hiscox, J., Baldrian, P., Rogers, H.J., Boddy, L., 2010. Changes in oxidative enzyme activity during interspecific mycelial interactions involving the white-rot fungus Trametes versicolor. Fungal Genetics and Biology 47, 562–571
CrossRef Google scholar
[22]
Jing, W., Chen, S., Zheng, H., Zhang, X., 2015. Soil microbial respiration under different soil temperature conditions and its relationship to soil dissolved organic carbon and invertase. Environmental Sciences (Ruse) 36, 1497–1506.
[23]
Kane, E.S., Pregitzer, K.S., Burton, A.J., 2003. Soil respiration along environmental gradients in Olympic National Park. Ecosystems (New York, N.Y.) 6, 326–335
CrossRef Google scholar
[24]
Lal, R., 2004. Soil carbon sequestration impacts on global climate change and food security. Science 304, 1623–1627
CrossRef Google scholar
[25]
Li, J., Pei, J., Pendall, E., Fang, C., Nie, M., 2020. Spatial heterogeneity of temperature sensitivity of soil respiration: A global analysis of field observations. Soil Biology & Biochemistry 141, 107675
CrossRef Google scholar
[26]
Li, Y., Yang, X., Zou, X., Wu, J., 2009. Response of soil nematode communities to tree girdling in a subtropical evergreen broad-leaved forest of southwest China. Soil Biology & Biochemistry 41, 877–882
CrossRef Google scholar
[27]
Luo, R., Kuzyakov, Y., Liu, D., Fan, J., Luo, J., Stuart, L., He, J., Ding, W., 2020. Nutrient addition reduces carbon sequestration in a Tibetan grassland soil: Disentangling microbial and physical controls. Soil Biology & Biochemistry 144, 107764
CrossRef Google scholar
[28]
Mancinelli, R., Campiglia, E., Tizio, A.D., Marinari, S., 2010. Soil carbon dioxide emission and carbon content as affected by conventional and organic cropping systems in Mediterranean environment. Applied Soil Ecology 46, 64–72
CrossRef Google scholar
[29]
Maynard, D.S., Crowther, T.W., Bradford, M.A., 2017. Fungal interactions reduce carbon use efficiency. Ecology Letters 20, 1034–1042
CrossRef Google scholar
[30]
McGee, K.M., Eaton, W.D., Shokralla, S., Hajibabaei, M., 2019. Determinants of soil bacterial and fungal community composition toward carbon-use efficiency across primary and secondary forests in a Costa Rican conservation area. Microbial Ecology 77, 148–167
CrossRef Google scholar
[31]
Melillo, J.M., Frey, S.D., De Angelis, K.M., Werner, W.J., Bernard, M.J., Bowles, F.P., Pold, D., Knorr, M.A., Grandy, A.S., 2017. Long-term pattern and magnitude of soil carbon feedback to the climate system in a warming world. Science 358, 101–105
CrossRef Google scholar
[32]
Milcu, A., Lukac, M., Subke, J.A., Manning, P., Heinemeyer, A., Wildman, D., Anderson, R., Ineson, P., 2012. Biotic carbon feedbacks in a materially closed soil–vegetation–atmosphere system. Nature Climate Change 2, 291–294
CrossRef Google scholar
[33]
Moore, J.A.M., Jiang, J., Post, W.M., Classen, A.T., 2015. Decomposition by ectomycorrhizal fungi alters soil carbon storage in a simulation model. Ecosphere 6, 1–16
CrossRef Google scholar
[34]
Nielsen, U.N., Ayres, E., Wall, D.H., Bardgett, R.D., 2011. Soil biodiversity and carbon cycling: A review and synthesis of studies examining diversity-function relationships. European Journal of Soil Science 62, 105–116
CrossRef Google scholar
[35]
Piao, S., Wang, X., Wang, K., Li, X., Ana, B., Josep, G.C., Philippe, C., Pierre, F., Stephen, S., 2020. Interannual variation of terrestrial carbon cycle: Issues and perspectives. Global Change Biology 26, 300–318
CrossRef Google scholar
[36]
Reinsch, S., Koller, E., Sowerby, A., de Dato, D.G., Estiarte, M., Guidolotti, G., Kovács-Láng, E., Kröel-Dulay, G., Lellei-Kovács, E., Larsen, K.S., Liberati, D., Peñuelas, J., Ransijn, J., Robinson, D.A., Schmidt, I.K., Smith, A.R., Tietema, A., Dukes, J.S., Beier, C., Emmett, B.A., 2017. Shrubland primary production and soil respiration diverge along European climate gradient. Scientific Reports 7, 1–7
CrossRef Google scholar
[37]
Rodeghiero, M., Cescatti, A., 2010. Main determinants of forest soil respiration along an elevation/temperature gradient in the Italian Alps. Global Change Biology 11, 1024–1041
CrossRef Google scholar
[38]
Sanders-DeMott, R., Ouimette, A.P., Lepine, L.C., Fogarty, S.Z., Burakowski, E.A., Contosta, A.R., Ollinger, S.V., 2020. Divergent carbon cycle response of forest and grass-dominated northern temperate ecosystems to record winter warming. Global Change Biology 26, 1519–1531
CrossRef Google scholar
[39]
Sinsabaugh, R.L., Stefano, M., Moorhead, D.L., Andreas, R., 2013. Carbon use efficiency of microbial communities: stoichiometry, methodology and modelling. Ecology Letters 16, 930–939
CrossRef Google scholar
[40]
Stefano, M., Philip, T., Andreas, R., Amilcare, P., Agren, G.I., 2012. Environmental and stoichiometric controls on microbial carbon-use efficiency in soils. New Phytologist 196, 79–91
CrossRef Google scholar
[41]
Tang, X., Zhao, X., Bai, Y., Tang, Z., Wang, W., Zhao, Y., Wan,H., Xie, Z., Shi, X., Wu, B., Wang, G., Yan, J., Ma, K., Du, S., Li, S., Han, S., Ma, Y., Hu, H., He, N., Yang, Y., Han, W., He, H., Yu, G., Fang, G., Zhou, G., 2018. Carbon pools in China’s terrestrial ecosystems: New estimates based on an intensive field survey. Proceedings of the National Academy of Sciences of the United States of America 15, 4021–4026
CrossRef Google scholar
[42]
Tucker, C.L., Bell, J., Pendall, E., Ogle, K., 2012. Does declining carbon-use efficiency explain thermal acclimation of soil respiration with warming? Global Change Biology 19, 252–263
CrossRef Google scholar
[43]
Wu, C., Zhang, Y., Xu, X., Sha, L., You, G., Liu, Y., Xie, Y., 2014. Influence of interactions between litter decomposition and rhizosphere activity on soil respiration and on the temperature sensitivity in a subtropical montane forest in SW China. Plant and Soil 381, 215–224
CrossRef Google scholar
[44]
Wu, J., Wang, S., Cai, M., Wu, B., 2019. Review on on carbon use efficiency of plants and microbes and its influencing factors. Acta Ecologica Sinica 39, 7771–7779.
[45]
Wu, X., Xu, H., Tuo, D., Wang, C., Fu, B., Lv, Y., Liu, G., 2020. Land use change and stand age regulate soil respiration by influencing soil substrate supply and microbial community. Geoderma 359, 113991
CrossRef Google scholar
[46]
Zhou, H., Yu, W., Qiang, M., Lu, Z., 2009. A modified fumigation extraction method for the determination of soil microbial biomass carbon.Chinese Journal of Soil Science 40, 154–157.
[47]
Zhou, X., Chen, L., Xu, J., Brookes, P.C., 2020. Soil biochemical properties and bacteria community in a repeatedly fumigated-incubated soil. Biology and Fertility of Soils 56, 619–631
CrossRef Google scholar
[48]
Zhu, Z., Zeng, G., Ge, T., Hu, Y., Tong, C., Shibistova, O., He, X., Wang, J., Guggenberger, G., Wu, J., 2016. Fate of rice shoot and root residues, rhizodeposits, and microbe-assimilated carbon in paddy soil-Part 1: Decomposition and priming effect. Biogeosciences 13, 4481–4489
CrossRef Google scholar

Acknowledgments

We are grateful to Zhiyun Lu and Hui Chen from XTBG, CAS for their assistance in field sampling. This work was financially supported by the National Natural Science Foundation of China (No. 31971497) and by “Young Scholar” funding from Yunnan Province.

Author contributions

JPW and SMW conceived and designed the experiments. All authors analyzed the data and jointly wrote the manuscript.

Competing financial interests

The authors declare no competing financial interests.

RIGHTS & PERMISSIONS

2020 Higher Education Press
AI Summary AI Mindmap
PDF(1255 KB)

Accesses

Citations

Detail

Sections
Recommended

/