Does anthropogenic phosphorus input reduce soil microbial resource allocation to acquire nitrogen relative to carbon?

Abstract

We aimed to test if anthropogenic P input into ecosystems reduces microbial resource allocation to acquire N (and alleviate N shortage if any) because microbes no longer produce N-rich phosphatase for P acquisition. Literatures reporting the effect of P fertilization on C-acquiring (β-1,4-glucosidase, BG) and N-acquiring (β-1,4-N-acetylglucosaminidase, NAG, which also acquires C) enzymes were collected and synthesized. We predicted that P addition elevates BG:NAG especially in P-poor ecosystems because P addition alleviates N shortage and reduces the microbial resource allocation to acquire N relative to C. The synthesized data demonstrated that P fertilization occasionally reduced BG:NAG, which is inconsistent with the prediction. However, this might not mean that the initial hypothesis was rejected. Stimulated microbial activity and turnover by P fertilization could have caused microbes depend the C sources more on chitin (and peptidoglycan) compared with on cellulose because chitin (and peptidoglycan) is a main component of microbial body and re-provided through microbial turnover. The changes in C resources accompanied by the altered P availability may have largely influenced BG:NAG, masking the role of BG:NAG for indicating microbial resource allocation to C and N acquisitions.

Keywords

• β-1,4-glucosidase (BG),4-N-acetylglucosaminidase (NAG),ecoenzymatic stoichiometry,phosphatase,phosphorus fertilization

References

1. Allison, S.D., Vitousek, P.M., 2005. Responses of extracellular enzymes to simple and complex nutrient inputs. Soil Biology and Biochemistry 37(5): 937–944.
2. Carrino-Kyker, S.R., Kluber, L.A., Petersen, S.M., Coyle, K.P., Hewins, C.R., DeForest, J.L., Smemo, K.A., Burke, D.J., 2016. Mycorrhizal fungal communities respond to experimental elevation of soil pH and P availability in temperate hardwood forests. FEMS Microbiology Ecology 92(3):1–19.
3. Dong, W.Y., Zhang, X.Y., Liu, X.Y., Fu, X.L., Chen, F.S., Wang, H.M., Sun, X.M., Wen, X.F., 2015. Responses of soil microbial communities and enzyme activities to nitrogen and phosphorus additions in Chinese fir plantations of subtropical China. Biogeosciences 12(18): 5537–5546.
4. Fanin, N., Hättenschwiler, S., Schimann, H., Fromin, N., 2015. Interactive effects of C, N and P fertilization on soil microbial community structure and function in an Amazonian rain forest. Functional Ecology 29(1):140–150.
5. Houlton, B.Z., Wang, Y.P., Vitousek, P.M., Field, C.B., 2008, A unifying framework for dinitrogen fixation in the terrestrial biosphere. Nature 454:327–330.
6. Jian, S., Li, J., Chen, J., Wang, G., Mayes, M.A., Dzantor, K.E., Hui, D.,, Luo, Y., 2016. Soil extracellular enzyme activities, soil carbon and nitrogen storage under nitrogen fertilization: A meta-analysis. Soil Biology and Biochemistry 101:32–43.
7. Kaspari, M., Garcia, M., Harms, K.E., Santana, M., Wright S.J., Yavitt, J.B., 2008. Multiple nutrients limit litterfall and decomposition in a tropical forest. Ecology Letters 11(1): 35–43.
8. Marklein, A.R., Houlton, B.Z., 2012. Nitrogen inputs accelerate phosphorus cycling rates across a wide variety of terrestrial ecosystems. The New Phytologist 193(3): 696–704.

9. Mineau, M.M., Fatemi, F.R., Fernandez, I.J., Simon, K.S., 2014. Microbial enzyme activity at the watershed scale: Response to chronic nitrogen deposition and acute phosphorus enrichment. Biogeochemistry 117(1): 131–142.
10. Moorhead, D.L., Sinsabaugh, R.L., Hill, B.H., Weintraub, M.N., 2016. Vector analysis of ecoenzyme activities reveal constraints on coupled C, N and P dynamics. Soil Biology and Biochemistry 93:1–7.
11. Mori, T., Imai, N., Yokoyama, D., Kitayama, K., 2018a. Effects of nitrogen and phosphorus fertilization on the ratio of activities of carbon-acquiring to nitrogen-acquiring enzymes in a primary lowland tropical rainforest in Borneo, Malaysia. Soil Science and Plant Nutrition 64(5): 554-557.
12. Mori, T., Lu, X., Aoyagi, R.., Mo, J., 2018b. Reconsidering the phosphorus limitation of soil microbial activity in tropical forests. Functional Ecology 32:1145–1154.
13. Olander, L.P., Vitousek, P.M., 2000 Regulation of soil phosphatase and chitinase activity by N and P availability. Biogeochemistry 49(2): 175–190.
14. Riggs, C.E., Hobbie, S.E., 2016. Mechanisms driving the soil organic matter decomposition response to nitrogen enrichment in grassland soils. Soil Biology and Biochemistry 99: 54–65.
15. Rosinger, C., Rousk, J., Sandén, H., 2018, Can enzymatic stoichiometry be used to determine growth-limiting nutrients for microorganisms? - A critical assessment in two subtropical soils. Soil Biology and Biochemistry 128: 115-126.
16. Sinsabaugh, R.L., Hill, B.H., Follstad Shah, J.J., 2009. Ecoenzymatic stoichiometry of microbial organic nutrient acquisition in soil and sediment. Nature 462:795–798.
17. Sinsabaugh, R.L., Lauber, C.L., Weintraub, M.N., Ahmed, B., Allison, S.D., Crenshaw, C., Contosta, A.R., Cusack, D., Frey, S., Gallo, M.E., Gartner, T.B., Hobbie, S.E., Holland, K., Keeler, B.L., Powers, J.S., Stursova, M., Takacs-Vesbach, C., Waldrop, M.P., Wallenstein, M.D., Zak, D.R., Zeglin, L.H., 2008. Stoichiometry of soil enzyme activity at global scale. Ecology Letters 11(11): 1252–1264.
18. Tatariw, C., MacRae, J.D., Fernandez, I.J., Gruselle’ M.C., Salvino, C.J., Simon, K.S., 2018. Chronic nitrogen enrichment at the watershed scale does not enhance microbial phosphorus limitation. Ecosystems 21(1): 178–189.
19. Treseder, K.K., Vitousek, P.M., 2001. Effects of soil nutrient availability on investment in acquisition of N and P in Hawaiian rainforests. Ecology 82: 946–954.
20. Turner, B.L., Wright, S.J., 2014. The response of microbial biomass and hydrolytic enzymes to a decade of nitrogen, phosphorus, and potassium addition in a lowland tropical rain forest. Biogeochemistry 117(1): 115–130.
21. Wang, C., Lu, X., Mori, T., Mao, Q., Zhou, K., Zhou, G., Nie, Y., Mo, J., 2018. Responses of soil microbial community to continuous experimental nitrogen additions for 13 years in a nitrogen-rich tropical forest. Soil Biology and Biochemistry 121: 103- 112.
22. Waring, B.G., Weintraub, S.R., Sinsabaugh, R.L., 2014. Ecoenzymatic stoichiometry of microbial nutrient acquisition in tropical soils. Biogeochemistry 117(1): 101–113.
23. Zhang, Q., Zhou, W., Liang, G., Sun, J., Wang, X., He, P., 2015a. Distribution of soil nutrients, extracellular enzyme activities and microbial communities across particle-size fractions in a long-term fertilizer experiment. Applied Soil Ecology 94: 59–71.
24. Zhang, X., Dong, W., Dai, X., Schaeffer, S., Yang, F., Radosevich, M., Xu, L., Liu, X., Sun, X., 2015b. Responses of absolute and specific soil enzyme activities to long term additions of organic and mineral fertilizer. Science of The Total Environment 536:59–67.
25. Zhou, Z., Wang, C., Jin, Y., 2017. Stoichiometric responses of soil microflora to nutrient additions for two temperate forest soils. Biology and Fertility of Soils 53(4): 397–406.