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Microbial acclimation triggered loss of soil carbon fractions in subtropical wetlands subjected to experimental warming in a laboratory study

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Abstract

Aims

Wetlands store a substantial amount of soil organic carbon (SOC), and their response to climate warming is critical for predicating global carbon (C) cycling in future climate change.

Methods

To understand whether warming causes substantial C loss in wetland soils, a 6-year microcosm experiment was carried out to examine the impact of rising temperature (3–5 °C) on SOC and its two fractions (labile versus recalcitrant) in six types of wetland soils with varied nutrient status.

Results

Warming decreased SOC contents in nutrient-enriched soils by invoking a large loss in recalcitrant organic C fractions, while in nutrient-poor soils SOC loss was limited by substrate limitation. With low temperature ranges in the winter (1–10 °C), warming increased the microbial capacity for recalcitrant organic C acquisition greater than that for labile organic C fractions. A relatively higher cross-site contribution of fungi in warmed soils as one strategy of microbial acclimation to rising temperature implies an adjustment of microbial C utilization patterns, leading to substantial C loss in wetland soils.

Conclusions

In order to maintain the functional roles of wetlands for C sequestration, our results further suggested that more attention should be paid to nutrient-enriched wetlands in future climate warming scenarios.

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References

  • Allison SD, Treseder KK (2008) Warming and drying suppress microbial activity and carbon cycling in boreal forest soils. Glob Chang Biol 14:2898–2909

    Article  Google Scholar 

  • Allison SD, Wallenstein MD, Bradford MA (2010) Soil-carbon response to warming dependent on microbial physiology. Nat Geosci 3:336–340

    Article  CAS  Google Scholar 

  • Al-Raei AM, Bosselmann K, Bottcher ME, Hespenheide B, Tauber F (2009) Seasonal dynamics of microbial sulfate reduction in temperate intertidal surface sediments: controls by temperature and organic matter. Ocean Dyn 59:351–370. doi:10.1007/s10236-009-0186-5

    Article  Google Scholar 

  • Bao S (2000) Agro-chemical analysis of soil. China Agricultural Press, Beijing

    Google Scholar 

  • Belay-Tedla A, Zhou XH, Su B, Wan SQ, Luo YQ (2009) Labile, recalcitrant, and microbial carbon and nitrogen pools of a tallgrass prairie soil in the US Great Plains subjected to experimental warming and clipping. Soil Biol Biochem 41:110–116. doi:10.1016/j.soilbio.2008.10.003

    Article  CAS  Google Scholar 

  • Bradford MA, Davies CA, Frey SD, Maddox TR, Melillo JM, Mohan JE, Reynolds JF, Treseder KK, Wallenstein MD (2008) Thermal adaptation of soil microbial respiration to elevated temperature. Ecol Lett 11:1316–1327

    Article  PubMed  Google Scholar 

  • Branco de Freitas Maia CM, Novotny E, Rittl TF, Bermingham Hayes MH (2013) Soil organic matter: chemistry and physical characteristics and analytical methods. A review. Curr Org Chem 17:2985–2990

    Article  Google Scholar 

  • Chimner RA, Cooper DJ (2003) Influence of water table levels on CO2 emissions in a Colorado subalpine fen: an in situ microcosm study. Soil Biol Biochem 35:345–351

    Article  CAS  Google Scholar 

  • Conant RT, Steinweg JM, Haddix ML, Paul EA, Plante AF, Six J (2008) Experimental warming shows that decomposition temperature sensitivity increases with soil organic matter recalcitrance. Ecology 89:2384–2391

    Article  PubMed  Google Scholar 

  • Cytryn E, Minz D, Oremland RS, Cohen Y (2000) Distribution and diversity of archaea corresponding to the limnological cycle of a hypersaline stratified lake (Solar Lake, Sinai, Egypt). Appl Environ Microbiol 66:3269–3276. doi:10.1128/Aem.66.8.3269-3276.2000

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Darrouzet-Nardi A, Reed SC, Grote EE, Belnap J (2015) Observations of net soil exchange of CO2 in a dryland show experimental warming increases carbon losses in biocrust soils. Biogeochemistry 126:363–378. doi:10.1007/s10533-015-0163-7

    Article  CAS  Google Scholar 

  • Davidson EA, Janssens IA (2006) Temperature sensitivity of soil carbon decomposition and feedbacks to climate change. Nature 440:165–173. doi:10.1038/Nature04514

    Article  CAS  PubMed  Google Scholar 

  • Eliasson PE, McMurtrie RE, Pepper DA, Stromgren M, Linder S, Agren GI (2005) The response of heterotrophic CO2 flux to soil warming. Glob Chang Biol 11:167–181

    Article  Google Scholar 

  • Fierer N, Craine JM, McLauchlan K, Schimel JP (2005a) Litter quality and the temperature sensitivity of decomposition. Ecology 86:320–326. doi:10.1890/04-1254

    Article  Google Scholar 

  • Fierer N, Jackson JA, Vilgalys R, Jackson RB (2005b) Assessment of soil microbial community structure by use of taxon-specific quantitative PCR assays. Appl Environ Microbiol 71:4117–4120. doi:10.1128/Aem.71.7.4117-4120.2005

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fissore C, Giardina CP, Kolka RK, Trettin CC (2009) Soil organic carbon quality in forested mineral wetlands at different mean annual temperature. Soil Biol Biochem 41:458–466. doi:10.1016/j.soilbio.2008.11.004

    Article  CAS  Google Scholar 

  • Freeman C, Ostle NJ, Fenner N, Kang H (2004) A regulatory role for phenol oxidase during decomposition in peatlands. Soil Biol Biochem 36:1663–1667. doi:10.1016/j.soilbio.2004.07.012

    Article  CAS  Google Scholar 

  • Frey SD, Drijber R, Smith H, Melillo J (2008) Microbial biomass, functional capacity, and community structure after 12 years of soil warming. Soil Biol Biochem 40:2904–2907

    Article  CAS  Google Scholar 

  • German DP, Weintraub MN, Grandy AS, Lauber CL, Rinkes ZL, Allison SD (2011) Optimization of hydrolytic and oxidative enzyme methods for ecosystem studies. Soil Biol Biochem 43:1387–1397. doi:10.1016/j.soilbio.2011.03.017

    Article  CAS  Google Scholar 

  • Huang HQ, Zhang R, Fu DW, Luo JJ, Li ZY, Luo HY, Shi PJ, Yang PL, Diao QY, Yao B (2011) Diversity, abundance and characterization of ruminal cysteine phytases suggest their important role in phytate degradation. Environ Microbiol 13:747–757. doi:10.1111/j.1462-2920.2010.02379.x

    Article  CAS  PubMed  Google Scholar 

  • IPCC (2013) Technical summary. In: Climate change 2013: the physical science basis. Contribution of working group I to the fifth assessment report of the intergovernmental panel on climate change. Cambridge University Press, Cambridge

    Google Scholar 

  • Jassey VEJ, Chiapusio G, Gilbert D, Buttler A, Toussaint ML, Binet P (2011) Experimental climate effect on seasonal variability of polyphenol/phenoloxidase interplay along a narrow fen-bog ecological gradient in Sphagnum fallax. Glob Chang Biol 17:2945–2957. doi:10.1111/j.1365-2486.2011.02437.x

    Article  Google Scholar 

  • Leifeld J, Fuhrer J (2005) The temperature response of CO2 production from bulk soils and soil fractions is related to soil organic matter quality. Biogeochemistry 75:433–453. doi:10.1007/s10533-005-2237-4

    Article  CAS  Google Scholar 

  • Li Z, Luo Y, Teng Y (2008) Soil and environmental Microbiology research. Science Press, Beijing

    Google Scholar 

  • Ma L, Huang W, Guo C, Wang R, Xiao C (2012) Soil microbial properties and plant growth responses to carbon and water addition in a temperate steppe: the importance of nutrient availability. PLoS One 7:e35165. doi:10.1371/journal.pone.0035165

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mack MC, Schuur EAG, Bret-Harte MS, Shaver GR, Chapin FS (2004) Ecosystem carbon storage in arctic tundra reduced by long-term nutrient fertilization. Nature 431:440–443. doi:10.1038/Nature02887

    Article  CAS  PubMed  Google Scholar 

  • Mandal UK, Yadav SK, Sharma KL, Ramesh V, Venkanna K (2011) Estimating permanganate-oxidizable active carbon as quick indicator for assessing soil quality under different land-use system of rainfed Alfisols. Indian J Agric Sci 81:927–931

    CAS  Google Scholar 

  • Marin-Spiotta E, Silver WL, Swanston CW, Ostertag R (2009) Soil organic matter dynamics during 80 years of reforestation of tropical pastures. Glob Chang Biol 15:1584–1597. doi:10.1111/j.1365-2486.2008.01805.x

    Article  Google Scholar 

  • Melillo JM, Steudler PA, Aber JD, Newkirk K, Lux H, Bowles FP, Catricala C, Magill A, Ahrens T, Morrisseau S (2002) Soil warming and carbon-cycle feedbacks to the climate system. Science 298:2173–2176

    Article  CAS  PubMed  Google Scholar 

  • Mirsky SB, Lanyon LE, Needelman BA (2008) Evaluating soil management using particulate and chemically labile soil organic matter fractions. Soil Sci Soc Am J 72:180–185. doi:10.2136/sssaj2005.0279

    Article  CAS  Google Scholar 

  • Reddy KR, D’angelo EM, Harris WG (1998) Biogeochemistry of wetlands. In: Summer ME (ed) Handbook of soil Science. CRC Press, Boca Raton, pp. 89–119

    Google Scholar 

  • Rinnan R, Michelsen A, Baath E, Jonasson S (2007) Fifteen years of climate change manipulations alter soil microbial communities in a subarctic heath ecosystem. Glob Chang Biol 13:28–39

    Article  Google Scholar 

  • Schmidt MWI, Torn MS, Abiven S, Dittmar T, Guggenberger G, Janssens IA, Kleber M, Kogel-Knabner I, Lehmann J, Manning DAC, Nannipieri P, Rasse DP, Weiner S, Trumbore SE (2011) Persistence of soil organic matter as an ecosystem property. Nature 478:49–56. doi:10.1038/nature10386

    Article  CAS  PubMed  Google Scholar 

  • Schuur EAG, Vogel JG, Crummer KG, Lee H, Sickman JO, Osterkamp TE (2009) The effect of permafrost thaw on old carbon release and net carbon exchange from tundra. Nature 459:556–559

    Article  CAS  PubMed  Google Scholar 

  • Sierra CA (2012) Temperature sensitivity of organic matter decomposition in the Arrhenius equation: some theoretical considerations. Biogeochemistry 108:1–15

    Article  Google Scholar 

  • Sowerby A, Emmett B, Beier C, Tietema A, Penuelas J, Estiarte M, Van Meeteren MJM, Hughes S, Freeman C (2005) Microbial community changes in heathland soil communities along a geographical gradient: interaction with climate change manipulations. Soil Biol Biochem 37:1805–1813. doi:10.1016/j.soilbio.2005.02.023

    Article  CAS  Google Scholar 

  • Trasar-Cepeda C, Gil-Sotres F, Leiros MC (2007) Thermodynamic parameters of enzymes in grassland soils from Galicia, NW Spain. Soil Biol Biochem 39:311–319. doi:10.1016/j.soilbio.2006.08.002

    Article  CAS  Google Scholar 

  • Verhoeven JTA, Arheimer B, Yin CQ, Hefting MM (2006) Regional and global concerns over wetlands and water quality. Trends Ecol Evol 21:96–103. doi:10.1016/j.tree.2005.11.015

    Article  PubMed  Google Scholar 

  • von Luetzow M, Koegel-Knabner I (2009) Temperature sensitivity of soil organic matter decomposition-what do we know? Biol Fertil Soils 46:1–15. doi:10.1007/s00374-009-0413-8

    Article  Google Scholar 

  • Waldrop MP, Firestone MK (2004) Altered utilization patterns of young and old soil C by microorganisms caused by temperature shifts and N additions. Biogeochemistry 67:235–248. doi:10.1023/B:Biog.0000015321.51462.41

    Article  CAS  Google Scholar 

  • Wallenstein MD, Weintraub MN (2008) Emerging tools for measuring and modeling the in situ activity of soil extracellular enzymes. Soil Biol Biochem 40:2098–2106. doi:10.1016/j.soilbio.2008.01.024

    Article  CAS  Google Scholar 

  • Wang H, He ZL, Lu ZM, Zhou JZ, Van Nostrand JD, Xu XH, Zhang ZJ (2012) Genetic linkage of soil carbon pools and microbial functions in subtropical freshwater wetlands in response to experimental warming. Appl Environ Microbiol 78:7652–7661. doi:10.1128/aem.01602-12

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang H, Holden J, Zhang ZJ, Li M, Li X (2014) Concentration dynamics and biodegradability of dissolved organic matter in wetland soils subjected to experimental warming. Sci Total Environ 470:907–916. doi:10.1016/j.scitotenv.2013.10.049

    Article  PubMed  Google Scholar 

  • Winton RS, Richardson CJ (2015) The effects of organic matter Amendments on Greenhouse Gas emissions from a Mitigation wetland in Virginia's Coastal Plain (vol 35, pg 969, 2015). Wetlands 35:981–981. doi:10.1007/s13157-015-0689-4

    Article  Google Scholar 

  • Wright AL, Reddy KR, Corstanje R (2009) Patterns of heterotrophic microbial activity in eutrophic and oligotrophic peatlands. Eur J Soil Biol 45:131–137

    Article  CAS  Google Scholar 

  • Wu J, Joergensen RG, Pommerening B, Chaussod R, Brookes PC (1990) Measurement of soil microbial biomass C by fumigation extraction - an automated procedure. Soil Biol Biochem 22:1167–1169

    Article  CAS  Google Scholar 

  • Yoshitake S, Tabei N, Mizuno Y, Yoshida H, Sekine Y, Tatsumura M, Koizumi H (2015) Soil microbial response to experimental warming in cool temperate semi-natural grassland in Japan. Ecol Res 30:235–245. doi:10.1007/s11284-014-1209-3

    Article  CAS  Google Scholar 

  • Zhang W, Parker KM, Luo Y, Wan S, Wallace LL, Hu S (2005) Soil microbial responses to experimental warming and clipping in a tallgrass prairie. Glob Chang Biol 11:266–277. doi:10.1111/j.1365-2486.2005.00902.x

    Article  CAS  Google Scholar 

  • Zhang ZJ, Wang ZD, Holden J, Xu XH, Wang H, Ruan JH, Xu X (2012) The release of phosphorus from sediment into water in subtropical wetlands: a warming microcosm experiment. Hydrol Process 26:15–26. doi:10.1002/hyp.8105

    Article  Google Scholar 

  • Zhang B, Chen SY, Zhang JF, He XY, Liu WJ, Zhao Q, Zhao L, Tian CJ (2015) Depth-related responses of soil microbial communities toexperimental warming in an alpine meadow on the Qinghai-Tibet Plateau. Eur J Soil Sci 66:496–504. doi:10.1111/ejss.12240

    Article  CAS  Google Scholar 

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Acknowledgments

This work was supported by the National Natural Science Foundation of China (41373074, 31500409), National Departments of Science and Technology, and Water Resource (2013GB23600658, 201301092), and Zhejiang Science and Technology Innovation Program (2015F50002).

Author information

Authors and Affiliations

  1. National Plateau Wetlands Research Center, Southwest Forestry University, Kunming, People’s Republic of China

    Hang Wang

  2. College of Environmental and Resource Sciences, Zhejiang University, Hangzhou, People’s Republic of China

    Hang Wang, HongYi Li, Fan Ping & ZhiJian Zhang

  3. Institute of Ecology, Zhejiang Forestry Academy, Liu He Ave 399, Hangzhou, 310020, People’s Republic of China

    ChunLei Yue

  4. China Academy of West Region Development, Zhejiang University, Hangzhou, People’s Republic of China

    ZhiJian Zhang

Authors
  1. Hang Wang
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  2. HongYi Li
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  3. Fan Ping
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Correspondence to Hang Wang or ZhiJian Zhang.

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Responsible Editor: Per Ambus.

Electronic supplementary material

Online Resource 1

Descriptions of experimental warming scenario. A ) Schematic of the experimental wetland microcosm system under the current climate condition (Left: ambient temperature, control) and the simulated climate warming condition (Right: ambient temperature + 5 °C, warmed). B ) Photographs of the microcosm temperature control system represented in this study. Six wetland columns for each study site were put in stainless steel boxes and operated outdoors since 2008. C ) Manipulated temperature variations in the overlying water of incubated wetland columns and field precipitation obtained from Hangzhou meteorological station records during a study year of 2010 as an example. Lines represent daily temperature (black squares for control, red circles for warmed) and bars represent daily precipitation. The temperature data from Jan., 15 to Apr, 20 is missing. (DOCX 579 kb)

Online Resource 2

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Online Resource 3

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Online Resource 4

Degree of similarity for the responses of three variables, including labile organic carbon (LOC), recalcitrant organic carbon (REC), and total soil organic carbon (SOC) to experimental warming. Percentages (%) in these variables between treatments (control versus warmed) for six wetlands over 6 years (2009–2013, inclusive) were used for analyses. A ) Linear model distance-based principal component analysis (PCA). The dissimilarity between samples (n = 6) on a PCA is reflected by their distances. B ) Hierarchical clustering analysis for these samples (expressed as mean values from six replicates) determined by squared Euclidian distance based on Ward’s clustering method. (DOCX 166 kb)

Online Resource 5

The extended information for redundancy analysis illustrated in Fig. 4. A) and B) The Monte Carlo permutation test with 499 random permutations was performed to show the relative importance of environmental variables with F values and p-values in a decreasing order. Data with significant p-values (0.05 or 0.01) are in bold. All observed environmental variables (significant or not) were incorporated in our redundancy analysis in order to show their relative importance in reshaping microbial properties in a more visual way. Based on our RDA model, a total of 62.1 % and 74.5 % variance of microbial properties could be explained by our selected environmental variables for summer and winter samples, respectively. C) Variation partitioning based on redundancy analysis. The environmental variables were classified into three common sets according to their different ecological properties: temperature, soil nutrient content, and warming-induced other environmental variables (water table level, dissolved oxygen, water moisture, and pH). A partial redundancy analysis was used to differentiate the effects of environmental variables and their interactions on the shifts of microbial properties. (DOCX 414 kb)

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Wang, H., Li, H., Ping, F. et al. Microbial acclimation triggered loss of soil carbon fractions in subtropical wetlands subjected to experimental warming in a laboratory study. Plant Soil 406, 101–116 (2016). https://doi.org/10.1007/s11104-016-2868-3

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