Nitrogen deposition suppresses fungal biomass and oxidase activity in faeces of the millipede Spirobolus formosae in a temperate forest

Mengru Wang, Shenglei Fu, Hongzhi Zhang, Meina Wang, Haixiang Xu, Leilei Shi

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Soil Ecology Letters ›› 2019, Vol. 1 ›› Issue (1-2) : 42-49. DOI: 10.1007s42832-019-0004-z
RESEARCH ARTICLE
RESEARCH ARTICLE

Nitrogen deposition suppresses fungal biomass and oxidase activity in faeces of the millipede Spirobolus formosae in a temperate forest

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Abstract

Atmospheric nitrogen (N) deposition has increased dramatically since the industrial revolution due to human activities. In terrestrial ecosystems, excess nitrogen inputs can greatly affect soil chemical properties, plant growth, and activities of soil microbes and fauna. Millipedes can fragment and consume large quantities of litter, and they regulate nutrient cycling and affect soil fertility through excretion of faeces. Many soil fauna graze on the faeces of millipedes as a part of the soil food web. The decomposition and stabilization of these millipede faeces are especially important in soil carbon dynamics and nutrient cycling, and these processes rely heavily upon microbial activity. However, very few studies have investigated how microbial community structure and oxidase activity of millipede faeces respond to climate change, especially N deposition. Therefore, we designed a microcosm study to investigate this question, which included two treatments, N addition treatment and control (without N addition).We found that: (i) microbial community structure in millipede faeces was altered and the biomass of fungi and actinomycetes in faecal pellets were significantly reduced after N addition, but bacteria still dominated in millipede faeces after N addition, (ii) oxidase activity was suppressed in response to N addition, and (iii) microbial community structure and oxidase activities were significantly correlated to organic carbon and dissolved total nitrogen of faeces. All these changes suggest that millipede excretion activities under nitrogen deposition contribute to carbon stabilization and reduction in greenhouse gas emission owing to the significant role of fungi and associated oxidase in carbon mineralization. It is noteworthy to pay more attention to the function of saprotrophic invertebrates in future N deposition studies.

Keywords

N deposition / Microbial community structure / Phenol oxidase / Peroxidase / Millipede faeces / Macroarthropods / PLFA

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Mengru Wang, Shenglei Fu, Hongzhi Zhang, Meina Wang, Haixiang Xu, Leilei Shi. Nitrogen deposition suppresses fungal biomass and oxidase activity in faeces of the millipede Spirobolus formosae in a temperate forest. Soil Ecology Letters, 2019, 1(1-2): 42‒49 https://doi.org/10.1007s42832-019-0004-z

References

[1]
Anderson, J.M., Bignell, D.E., 1980. Bacteria in the food, gut contents and faeces of the litter-feeding millipede Glomeris marginata (Villers). Soil Biology & Biochemistry 12, 251–254
CrossRef Google scholar
[2]
Bååth, E., Anderson, T.H., 2003. Comparison of soil fungal/bacterial ratios in a pH gradient using physiological and PLFA-based techniques. Soil Biology & Biochemistry 35, 955–963
CrossRef Google scholar
[3]
Bai, Z., Zhang, X., He, H., Yan, Y., Hou, S., Chen, Y., Xie, H., 2007. Effects of long-time niterogen fertilizer application on NLFA and PLFA in mollisol farmland. Acta Pedologica Sinical 44, 709–716.
[4]
Bossio, D.A., Scow, K.M., 1998. Impacts of carbon and flooding on soil microbial communities: phospholipid fatty acid profiles and substrate utilization patterns. Microbial Ecology 35, 265–278
CrossRef Pubmed Google scholar
[5]
Byzov, B.A., Kurakov, A.V., Tretyakova, E.B., Thanh, V.N., Luu, N.D.T., Rabinovich, Y.M., 1998. Principles of the digestion of microorganisms in the gut of soil millipedes: Specificity and possible mechanisms. Applied Soil Ecology 9, 145–151
CrossRef Google scholar
[6]
Carreiro, M.M., Sinsabaugh, R.L., Repert, D.A., Parkhurst, D.F., 2000. Microbial enzyme shifts explain litter decay responses to simulated nitrogen deposition. Ecology 81, 2359–2365
CrossRef Google scholar
[7]
Cromack, K., Sollins, P., Todd, R.L., Fogel, R., Todd, A.W., Fender, W.M., 1977. The role of oxalic acid and bicarbonate in calcium cycling by fungi and bacteria: Some possible implications for soil animals. Ecological Bulletins 25, 246–252.
[8]
Crowther, T.W., Boddy, L., Jones, T.H., 2011. Species-specific effects of soil fauna on fungal foraging and decomposition. Oecologia 167, 535–545
CrossRef Pubmed Google scholar
[9]
Cusack, D.F., Silver, W.L., Torn, M.S., Burton, S.D., Firestone, M.K., 2011. Changes in microbial community characteristics and soil organic matter with nitrogen additions in two tropical forests. Ecology 92, 621–632
CrossRef Pubmed Google scholar
[10]
David, J.F., 2014. The role of litter-feeding macroarthropods in decomposition processes: a reappraisal of common views. Soil Biology & Biochemistry 76, 109–118
CrossRef Google scholar
[11]
David, J.F., Gillon, D., 2002. Annual feeding rate of the millipede Glomeris marginata, on holm oak (Quercus ilex) leaf litter under Mediterranean conditions. Pedobiologia 46, 42–52
CrossRef Google scholar
[12]
Diepen, L.T., Lilleskov, E.A., Pregitzer, K.S., Miller, R.M., 2010. Simulated nitrogen deposition causes a decline of intra-and extraradical abundance of arbuscular mycorrhizal fungi and changes in microbial community structure in northern hardwood forests. Ecosystems (New York, N.Y.) 13, 683–695
CrossRef Google scholar
[13]
Fields, S., 2004. Global nitrogen: cycling out of control. Environmental Health Perspectives 112, A556–A563
CrossRef Pubmed Google scholar
[14]
Frostegård, A., Bååth, E., 1996. The use of phospholipid fatty acid analysis to estimate bacterial and fungal biomass in soil. Biology and Fertility of Soils 22, 59–65
CrossRef Google scholar
[15]
IUSS Working Group WRB, 2015. World Reference Base for Soil Resources 2014, update 2015. International soil classification system for naming soils and creating legends for soil maps. FAO, Rome.
[16]
Jia, Y., Yu, G., He, N., Zhan, X., Fang, H., Sheng, W., Zuo, Y., Zhang, D., Wang, Q., 2014. Spatial and decadal variations in inorganic nitrogen wet deposition in China induced by human activity. Scientific Reports 4, 3763
CrossRef Pubmed Google scholar
[17]
Liu, X., Zhang, Y., Han, W., Tang, A., Shen, J., Cui, Z., Vitousek, P., Erisman, J.W., Goulding, K., Christie, P., Fangmeier, A., Zhang, F., 2013. Enhanced nitrogen deposition over China. Nature 494, 459–462
CrossRef Pubmed Google scholar
[18]
Lu, R., 2000. Soil argrochemistry analysis protocoes. Beijing: China Agriculture Science Press.
[19]
Maraun, M., Scheu, S., 1996. Changes in microbial biomass, respiration and nutrient status of beech (Fagus sylvatica) leaf litter processed by millipedes (Glomeris marginata). Oecologia 107, 131–140
CrossRef Pubmed Google scholar
[20]
Oravecz, O., 2002. A molecular approach in the analysis of the faecal bacterial community in an African millipede belonging to the family Spirostreptidae (Diplopoda). European Journal of Soil Biology 38, 67–70
CrossRef Google scholar
[21]
Osono, T., 2007. Ecology of ligninolytic fungi associated with leaf litter decomposition. Ecological Research 22, 955–974
CrossRef Google scholar
[22]
Rawlins, A.J., Bull, I.D., Ineson, P., Evershed, R.P., 2007. Stabilisation of soil organic matter in invertebrate faecal pellets through leaf litter grazing. Soil Biology & Biochemistry 39, 1202–1205
CrossRef Google scholar
[23]
Rawlins, A.J., Bull, I.D., Poirier, N., Ineson, P., Evershed, R.P., 2006. The biochemical transformation of oak (Quercus robur) leaf litter consumed by the pill millipede (Glomeris marginata). Soil Biology & Biochemistry 38, 1063–1076
CrossRef Google scholar
[24]
Saiya-Cork, K.R., Sinsabaugh, R.L., Zak, D.R., 2002. The effects of long term nitrogen deposition on extracellular enzyme activity in an acer saccharum, forest soil. Soil Biology & Biochemistry 34, 1309–1315
CrossRef Google scholar
[25]
Sakamoto, K., Iijima, T., Higuchi, R., 2004. Use of specific phospholipid fatty acids for identifying and quantifying the external hyphae of the arbuscular mycorrhizal fungus Gigaspora rosea. Soil Biology & Biochemistry 36, 1827–1834
CrossRef Google scholar
[26]
Shi, L., Zhang, H., Liu, T., Mao, P., Zhang, W., Shao, Y., Fu, S., 2018. An increase in precipitation exacerbates negative effects of nitrogen deposition on soil cations and soil microbial communities in a temperate forest. Environ Pollut 235, 293–301
CrossRef Pubmed Google scholar
[27]
Shi, L., Zhang, H., Liu, T., Zhang, W., Shao, Y., Ha, D., Li, Y., Zhang, C., Cai, X.A., Rao, X., Lin, Y., Zhou, L., Zhao, P., Ye, Q., Zou, X., Fu, S., 2016. Consistent effects of canopy vs. understory nitrogen addition on the soil exchangeable cations and microbial community in two contrasting forests. Science of the Total Environment 553, 349–357
CrossRef Pubmed Google scholar
[28]
Sierwald, P., Bond, J.E., 2007. Current status of the Myriapod class diplopoda (millipedes): taxonomic diversity and phylogeny. Annual Review of Entomology 52, 401–420
CrossRef Pubmed Google scholar
[29]
Sinsabaugh, R.L., 2010. Phenol oxidase, peroxidase and organic matter dynamics of soil. Soil Biology & Biochemistry 42, 391–404
CrossRef Google scholar
[30]
Tajovsky, K., Santruckova, H., Hanel, L., Balik, V., Lukesova, A., 1992. Decomposition of faecal pellets of the millipede Glomeris hexasticha (Diplopoda) in forest soil. Pedobiologia 36, 146–158.
[31]
Treseder, K.K., 2008. Nitrogen additions and microbial biomass: a meta-analysis of ecosystem studies. Ecology Letters 11, 1111–1120
CrossRef Pubmed Google scholar
[32]
Ye, Y., Li, P., Qu, W., 2014. Scientific survey on Henan Jigongshan Nature Reserve. Beijing: Science press.
[33]
Zak, D.R., Ringelberg, D.B., Pregitzer, K.S., Randlett, D.L., White, D.C., Curtis, P.S., 1996. Soil microbial communities beneath populus grandidentata grown under elevated atmospheric CO2. Ecological Applications 6, 257–262
CrossRef Google scholar
[34]
Zelles, L., 1997. Phospholipid fatty acid profiles in selected members of soil microbial communities. Chemosphere 35, 275–294
CrossRef Pubmed Google scholar
[35]
Zhang, W., Shen, W., Zhu, S., Wan, S., Luo, Y., Yan, J., Wang, K., Liu, L., Dai, H., Li, P., Dai, K., Zhang, W., Liu, Z., Wang, F., Kuang, Y., Li, Z., Lin, Y., Rao, X., Li, J., Zou, B., Cai, X., Mo, J., Zhao, P., Ye, Q., Huang, J., Fu, S., 2015. CAN canopy addition of nitrogen better illustrate the effect of atmospheric nitrogen deposition on forest ecosystem? Scientific Reports 5, 11245
CrossRef Pubmed Google scholar

Acknowledgments

This research was funded by the National Natural Science Foundation of China (31700416, 31470559 and 31600434).

Conflict of interest statement

The authors declare no conflict of interest.

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2019 Higher Education Press
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