Trade-off between microbial carbon use efficiency and specific nutrient-acquiring extracellular enzyme activities under reduced oxygen

Abstract

● Reduced oxygen increased microbial metabolic quotient (qCO₂).

● Reduced oxygen enhanced microbial specific C-, N- and P-acquiring enzyme activity.

● Reduced oxygen increased microbial C relative to N and P limitation.

● Reduced oxygen increased microbial N relative to P limitation.

● Specific enzyme activity was positively related to qCO₂ under reduced oxygen.

Mangroves are one of the most ecologically sensitive ecosystems to global climate change, which have cascading impacts on soil carbon (C), nitrogen (N) and phosphorus (P) cycling. Moreover, mangroves are experiencing increasing N and P loadings and reduced oxygen availability due to intensified climate change and human activities. However, both direct and interactive effects of these perturbations on microbially mediated soil C, N and P cycling are poorly understood. Here, we simultaneously investigated the effects of N and P loadings and reduced oxygen on microbial biomass, microbial respiration, and extracellular enzyme activities (EEAs) in mangrove soils. We calculated the microbial metabolic quotient (qCO₂), which is regarded as a useful inverse metric of microbial C use efficiency (CUE). Our results show that reduced oxygen significantly increases both qCO₂ and microbial specific EEAs (enzyme activity per unit of microbial biomass) for C-, N- and P-acquisition regardless of N or P loadings. Furthermore, we found that qCO₂ positively correlated with microbial specific EEAs under reduced oxygen, whereas no clear relationship was detected under ambient oxygen. These results suggest that reduced oxygen increases microbial specific EEAs at the expense of increasing microbial respiration per unit biomass, indicating higher energy cost per unit enzyme production.

Graphical abstract

Keywords

reduced oxygen / extracellular enzyme / microbial respiration / nutrient acquisition / nutrient addition / mangrove

References

[1] Allison, S.D., Wallenstein, M.D., Bradford, M.A., 2010. Soil-carbon response to warming dependent on microbial physiology. Nature Geoscience3, 336–340.

[2] Atwood, T.B., Connolly, R.M., Almahasheer, H., Carnell, P.E., Duarte, C.M., Ewers Lewis, C.J., Irigoien, X., Kelleway, J.J., Lavery, P.S., Macreadie, P.I., Serrano, O., Sanders, C.J., Santos, I., Steven, A.D.L., Lovelock, C.E., 2017. Global patterns in mangrove soil carbon stocks and losses. Nature Climate Change7, 523–528.

[3] Barton, K., Barton, M.K., 2015. Package ‘mumin’. Version.1, 439.

[4] Behera, B.C., Sethi, B.K., Mishra, R.R., Dutta, S.K., Thatoi, H.N., 2017. Microbial cellulases – Diversity & biotechnology with reference to mangrove environment: A review. Journal of Genetic Engineering and Biotechnology15, 197–210.

[5] Bouillon, S., Borges, A.V., Castañeda-Moya, E., Diele, K., Dittmar, T., Duke, N.C., Kristensen, E., Lee, S.Y., Marchand, C., Middelburg, J.J., Rivera-Monroy, V.H., Smith, T.J. III, Twilley, R.R., 2008. Mangrove production and carbon sinks: A revision of global budget estimates. Global Biogeochemical Cycles22, GB2013.

[6] Brookes, P.C., Landman, A., Pruden, G., Jenkinson, D.S., 1985. Chloroform fumigation and the release of soil nitrogen: A rapid direct extraction method to measure microbial biomass nitrogen in soil. Soil Biology & Biochemistry17, 837–842.

[7] Brune, A., Frenzel, P., Cypionka, H., 2000. Life at the oxic–anoxic interface: microbial activities and adaptations. FEMS Microbiology Reviews24, 691–710.

[8] Chapman, S.K., Hayes, M.A., Kelly, B., Langley, J.A., 2019. Exploring the oxygen sensitivity of wetland soil carbon mineralization. Biology Letters15, 20180407.

[9] Chen, J., Elsgaard, L., van Groenigen, K.J., Olesen, J.E., Liang, Z., Jiang, Y., Lærke, P.E., Zhang, Y., Luo, Y., Hungate, B.A., Sinsabaugh, R.L., Jørgensen, U., 2020a. Soil carbon loss with warming: New evidence from carbon-degrading enzymes. Global Change Biology26, 1944–1952.

[10] Chen, J., Luo, Y., Li, J., Zhou, X., Cao, J., Wang, R.W., Wang, Y., Shelton, S., Jin, Z., Walker, L.M., Feng, Z., Niu, S., Feng, W., Jian, S., Zhou, L., 2017. Costimulation of soil glycosidase activity and soil respiration by nitrogen addition. Global Change Biology23, 1328–1337.

[11] Chen, J., Luo, Y., van Groenigen, K. J., Hungate, B. A., Cao, J., Zhou, X., Wang, R.W., 2018. A keystone microbial enzyme for nitrogen control of soil carbon storage. Science Advances4, eaaq1689.

[12] Chen, J., Sinsabaugh, R.L., 2021. Linking microbial functional gene abundance and soil extracellular enzyme activity: Implications for soil carbon dynamics. Global Change Biology27, 1322–1325.

[13] Chen, J., van Groenigen, K.J., Hungate, B.A., Terrer, C., van Groenigen, J.W., Maestre, F.T., Ying, S.C., Luo, Y., Jørgensen, U., Sinsabaugh, R.L., Olesen, J.E., Elsgaard, L., 2020b. Long-term nitrogen loading alleviates phosphorus limitation in terrestrial ecosystems. Global Change Biology26, 5077–5086.

[14] Cohen, M.C.L., de Souza, A.V., Rossetti, D.F., Pessenda, L.C.R., França, M.C., 2018. Decadal-scale dynamics of an Amazonian mangrove caused by climate and sea level changes: Inferences from spatial–temporal analysis and digital elevation models. Earth Surface Processes and Landforms43, 2876–2888.

[15] Cavanaugh, K. C., Kellner, J. R., Forde, A. J., Gruner, D. S., Parker, J. D., Rodriguez, W., Feller, I. C., 2014. Poleward expansion of mangroves is a threshold response to decreased frequency of extreme cold events. Proceedings of the National Academy of Sciences111, 723–727.

[16] Craig, H., Antwis, R.E., Cordero, I., Ashworth, D., Robinson, C.H., Osborne, T.Z., Bardgett, R.D., Rowntree, J.K., Simpson, L.T., 2021. Nitrogen addition alters composition, diversity, and functioning of microbial communities in mangrove soils: An incubation experiment. Soil Biology & Biochemistry153, 108076.

[17] Cui, Y., Bing, H., Moorhead, D.L., Delgado-Baquerizo, M., Ye, L., Yu, J., Zhang, S., Wang, X., Peng, S., Guo, X., Zhu, B., Chen, J., Tan, W., Wang, Y., Zhang, X., Fang, L., 2022. Ecoenzymatic stoichiometry reveals widespread soil phosphorus limitation to microbial metabolism across Chinese forests. Communications Earth & Environment3, 184.

[18] Dangremond, E.M., Simpson, L.T., Osborne, T.Z., Feller, I.C., 2020. Nitrogen enrichment accelerates mangrove range expansion in the temperate–tropical ecotone. Ecosystems (New York, N.Y.)23, 703–714.

[19] DeAngelis, K.M., Silver, W.L., Thompson, A.W., Firestone, M.K., 2010. Microbial communities acclimate to recurring changes in soil redox potential status. Environmental Microbiology12, 3137–3149.

[20] DeForest, J.L., 2009. The influence of time, storage temperature, and substrate age on potential soil enzyme activity in acidic forest soils using MUB-linked substrates and l-DOPA. Soil Biology & Biochemistry41, 1180–1186.

[21] Dijkstra, P., Thomas, S.C., Heinrich, P.L., Koch, G.W., Schwartz, E., Hungate, B.A., 2011. Effect of temperature on metabolic activity of intact microbial communities: Evidence for altered metabolic pathway activity but not for increased maintenance respiration and reduced carbon use efficiency. Soil Biology & Biochemistry43, 2023–2031.

[22] Domeignoz-Horta, L.A., Pold, G., Liu, X.J.A., Frey, S.D., Melillo, J.M., DeAngelis, K.M., 2020. Microbial diversity drives carbon use efficiency in a model soil. Nature Communications11, 3684.

[23] Donato, D.C., Kauffman, J.B., Murdiyarso, D., Kurnianto, S., Stidham, M., Kanninen, M., 2011. Mangroves among the most carbon-rich forests in the tropics. Nature Geoscience4, 293–297.

[24] Duarte, C.M., Losada, I.J., Hendriks, I.E., Mazarrasa, I., Marbà N., 2013. The role of coastal plant communities for climate change mitigation and adaptation. Nature Climate Change3, 961–968.

[25] Feller, I.C., Lovelock, C.E., Berger, U., McKee, K.L., Joye, S.B., Ball, M.C., 2009. Biocomplexity in mangrove ecosystems. Annual Review of Marine Science2, 395–417.

[26] Feng, J., Wei, K., Chen, Z., Lü X., Tian, J., Wang, C., Chen, L., 2019. Coupling and decoupling of soil carbon and nutrient cycles across an aridity gradient in the drylands of Northern China: Evidence from ecoenzymatic stoichiometry. Global Biogeochemical Cycles33, 559–569.

[27] Ferenci, T., 2016. Trade-off mechanisms shaping the diversity of bacteria. Trends in Microbiology24, 209–223.

[28] Freeman, C., Ostle, N., Kang, H., 2001. An enzymic ‘latch’ on a global carbon store. Nature409, 149–149.

[29] Friesen, S.D., Dunn, C., Freeman, C., 2018. Decomposition as a regulator of carbon accretion in mangroves: a review. Ecological Engineering114, 173–178.

[30] Garcia, M.O., Templer, P.H., Sorensen, P.O., Sanders-DeMott, R., Groffman, P.M., Bhatnagar, J.M., 2020. Soil microbes trade-off biogeochemical cycling for stress tolerance traits in response to year-round climate change. Frontiers in Microbiology11, 616.

[31] 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. Biogeochemistry127, 173–188.

[32] Han, H., Hemp, J., Pace, L.A., Ouyang, H., Ganesan, K., Roh, J.H., Daldal, F., Blanke, S.R., Gennis, R.B., 2011. Adaptation of aerobic respiration to low O₂ environments. Proceedings of the National Academy of Sciences of the United States of America108, 14109–14114.

[33] Hayes, M.A., Jesse, A., Tabet, B., Reef, R., Keuskamp, J.A., Lovelock, C.E., 2017. The contrasting effects of nutrient enrichment on growth, biomass allocation and decomposition of plant tissue in coastal wetlands. Plant and Soil416, 193–204.

[34] Hoehler, T.M., Jørgensen, B.B., 2013. Microbial life under extreme energy limitation. Nature Reviews Microbiology11, 83–94.

[35] Holguin, G., Vazquez, P., Bashan, Y., 2001. The role of sediment microorganisms in the productivity, conservation, and rehabilitation of mangrove ecosystems: an overview. Biology and Fertility of Soils33, 265–278.

[36] Huang, W., Ye, C., Hockaday, W.C., Hall, S.J., 2020. Trade-offs in soil carbon protection mechanisms under aerobic and anaerobic conditions. Global Change Biology26, 3726–3737.

[37] Jackson, C.R., Tyler, H.L., Millar, J.J., 2013. Determination of microbial extracellular enzyme activity in waters, soils, and sediments using high throughput microplate assays. Journal of Visualized Experiments80, e50399.

[38] Jardine, S.L., Siikamäki, J.V., 2014. A global predictive model of carbon in mangrove soils. Environmental Research Letters9, 104013.

[39] 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 & Biochemistry101, 32–43.

[40] Keuskamp, J.A., Schmitt, H., Laanbroek, H.J., Verhoeven, J.T.A., Hefting, M.M., 2013. Nutrient amendment does not increase mineralisation of sequestered carbon during incubation of a nitrogen limited mangrove soil. Soil Biology & Biochemistry57, 822–829.

[41] Li, Q., Chen, J., Feng, J., Wu, J., Zhang, Q., Jia, W., Lin, Q., Cheng, X., 2020. How do biotic and abiotic factors regulate soil enzyme activities at plot and microplot scales under afforestation? Ecosystems (New York, N. Y.)23, 1408–1422.

[42] Liu, J., Chen, J., Chen, G., Guo, J., Li, Y., 2020. Enzyme stoichiometry indicates the variation of microbial nutrient requirements at different soil depths in subtropical forests. PLoS One15, e0220599.

[43] Liu, Y., Luo, M., Chen, J., Ye, R., Tan, J., Zhai, Z., Yang, Y., Huang, J., 2021. Root iron plaque abundance as an indicator of carbon decomposition rates in a tidal freshwater wetland in response to salinity and flooding. Soil Biology & Biochemistry162, 108403.

[44] Lovelock, C.E., Feller, I.C., Ball, M.C., Engelbrecht, B.M.J., Ewe, M.L., 2006. Differences in plant function in phosphorus- and nitrogen-limited mangrove ecosystems. New Phytologist172, 514–522.

[45] Malik, A.A., Puissant, J., Goodall, T., Allison, S.D., Griffiths, R.I., 2019. Soil microbial communities with greater investment in resource acquisition have lower growth yield. Soil Biology & Biochemistry132, 36–39.

[46] Möller, K., Müller, T., 2012. Effects of anaerobic digestion on digestate nutrient availability and crop growth: A review. Engineering in Life Sciences12, 242–257.

[47] Moore, J.A.M., Anthony, M.A., Pec, G.J., Trocha, L.K., Trzebny, A., Geyer, K.M., Diepen, L.T.A., Frey, S.D., 2021. Fungal community structure and function shifts with atmospheric nitrogen deposition. Global Change Biology27, 1349–1364.

[48] 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 & Biochemistry93, 1–7.

[49] Mooshammer, M., Hofhansl, F., Frank, A.H., Wanek, W., Hämmerle, I., Leitner, S., Schnecker, J., Wild, B., Watzka, M., Keiblinger, K.M., Zechmeister-Boltenstern, S., Richter, A., 2017. Decoupling of microbial carbon, nitrogen, and phosphorus cycling in response to extreme temperature events. Science Advances3, e1602781.

[50] Mori, T 2020. Does ecoenzymatic stoichiometry really determine microbial nutrient limitations?. Soil Biology & Biochemistry146, 107816.

[51] Naidoo, G., 2009. Differential effects of nitrogen and phosphorus enrichment on growth of dwarf Avicennia marina mangroves. Aquatic Botany90, 184–190.

[52] Ng, E.L., Patti, A.F., Rose, M.T., Schefe, C.R., Smernik, R.J., Cavagnaro, T.R., 2015. Do organic inputs alter resistance and resilience of soil microbial community to drying?. Soil Biology & Biochemistry81, 58–66.

[53] Pett-Ridge, J., Petersen, D.G., Nuccio, E., Firestone, M.K., 2013. Influence of oxic/anoxic fluctuations on ammonia oxidizers and nitrification potential in a wet tropical soil. FEMS Microbiology Ecology85, 179–194.

[54] Pinheiro, J., Bates, D., DebRoy, S., Sarkar, D., Heisterkamp, S., Van Willigen, B., Ranke, J., R Core Team, 2017. Package ‘nlme’. Linear and nonlinear mixed effects models, version.3.

[55] R Core Team, 2019. R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria

[56] Ren, C., Chen, J., Lu, X., Doughty, R., Zhao, F., Zhong, Z., Han, X., Yang, G., Feng, Y., Ren, G., 2018. Responses of soil total microbial biomass and community compositions to rainfall reductions. Soil Biology & Biochemistry116, 4–10.

[57] Rysgaard, S., Risgaard-Petersen, N., Niels Peter, S., Kim, J., Lars Peter, N., 1994. Oxygen regulation of nitrification and denitrification in sediments. Limnology and Oceanography39, 1643–1652.

[58] Schimel, J., Balser, T.C., Wallenstein, M., 2007. Microbial stress-response physiology and its implications for ecosystem function. Ecology88, 1386–1394.

[59] Schimel, J., Weintraub, M.N., Moorhead, D., 2022. Estimating microbial carbon use efficiency in soil: Isotope-based and enzyme-based methods measure fundamentally different aspects of microbial resource use. Soil Biology & Biochemistry169, 108677.

[60] Siikamäki, J., Sanchirico, J.N., Jardine, S.L., 2012. Global economic potential for reducing carbon dioxide emissions from mangrove loss. Proceedings of the National Academy of Sciences of the United States of America109, 14369–14374.

[61] Simpson, L.T., Lovelock, C.E., Cherry, J.A., Feller, I.C., 2020. Short-lived effects of nutrient enrichment on Avicennia germinans decomposition in a saltmarsh-mangrove ecotone. Estuarine, Coastal and Shelf Science235, 106598.

[62] Sinsabaugh, R.L., Follstad Shah, J.J., 2012. Ecoenzymatic stoichiometry and ecological theory. Annual Review of Ecology, Evolution, and Systematics43, 313–343.

[63] 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 Letters11, 1252–1264.

[64] Spohn, M., Chodak, M., 2015. Microbial respiration per unit biomass increases with carbon-to-nutrient ratios in forest soils. Soil Biology & Biochemistry81, 128–133.

[65] Wang, G., Gao, Q., Yang, Y., Hobbie, S.E., Reich, P.B., Zhou, J., 2022. Soil enzymes as indicators of soil function: A step toward greater realism in microbial ecological modeling. Global Change Biology28, 1935–1950.

[66] Wang, S., Wang, W., Zhao, S., Wang, X., Hefting, M.M., Schwark, L., Zhu, G., 2019. Anammox and denitrification separately dominate microbial N-loss in water saturated and unsaturated soils horizons of riparian zones. Water Research162, 139–150.

[67] Widdig, M., Schleuss, P.M., Biederman, L.A., Borer, E.T., Crawley, M.J., Kirkman, K.P., Seabloom, E.W., Wragg, P.D., Spohn, M., 2020. Microbial carbon use efficiency in grassland soils subjected to nitrogen and phosphorus additions. Soil Biology & Biochemistry146, 107815.

[68] Yang, Y., Moorhead, D. L., Craig, H., Luo, M., Chen, X., Huang, J., Olesen, J.E., Chen, J., 2022. Differential responses of soil extracellular enzyme activities to salinization: implications for soil carbon cycling in tidal wetlands. Global Biogeochemical Cycles.36, e2021GB007285.

[69] Zhai, Z., Luo, M., Yang, Y., Liu, Y., Chen, X., Zhang, C., Huang, J., Chen, J., 2022. Trade-off between microbial carbon use efficiency and microbial phosphorus limitation under salinization in a tidal wetland. Catena209, 105809.

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