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Conversion of organic carbon from decayed native and invasive plant litter in Jiuduansha wetland and its implications for SOC formation and sequestration

  • Jianfang Yan
  • Lei WangEmail author
  • Yiu Fai TsangEmail author
  • Liwei Qian
  • Xiaohua Fu
  • Ying Sun
  • Pengfei Wu
Soils, Sec 1 • Soil Organic Matter Dynamics and Nutrient Cycling • Research Article
  • 56 Downloads

Abstract

Purpose

It is still controversial which type of plant litter is conducive to soil organic carbon (SOC) formation. Here we are to explore the conversion of organic carbon (OC) from decayed plant litter in soil and its influence on final SOC sequestration.

Materials and methods

In situ investigation combined with laboratory soil incubation experiments were conducted in mixing zones dominated by halophytes of Phragmites communis and Spartina alterniflora in the Jiuduansha wetland of the Yangtze River estuary to investigate differences in conversion patterns of OC from two decayed plant litters of different characteristics using traditional physicochemical indicators and stable isotope tracing. Additionally, the mechanism of biotransformation was investigated through analysis of soil microbial community structure.

Results and discussion

Due to the higher content of lignin and cellulose in P. communis litter, the associated soil microbial community was more conducive to the formation of soil humus (HS). By contrast, more easily decomposable S. alterniflora litter induced its related soil microbial community more amenable to mineralization. Consequently, OC from decayed S. alterniflora litter remained in soil for less time than that from decayed P. communis, and the lost OC was more readily converted into CO2. OC from decayed P. communis was degraded very slowly during the early stage of conversion (November), and its longer duration in soil was favorable for HS formation.

Conclusions

Analysis of the conversion of intermediates derived from different types of decayed plants can provide insight into plant litter input and SOC formation, and indicate the whereabouts of lost OC. From the perspective of plant biomass and conversion of plant litter-derived OC, P. communis is more conducive to soil carbon sequestration than S. alterniflora.

Keywords

Biotransformation Phragmites communis Plant litter Soil microbial community Soil organic carbon Spartina alterniflora 

Notes

Acknowledgments

We thanked the International Science Editing for editing the paper.

Funding information

This work was supported by the National Natural Science Foundation of China (no. 21876127); National Key Research and Development Project of China (no. 2017YFC0506004); Research Grants Council of the Hong Kong SAR, China (nos. 28300015 and 18202116); the Internal Research Grant (RG 34/2017-2018R and RG 50/2017-2018R) of The Education University of Hong Kong; Science and Technology Developmental Fund Project of Pudong District (no. PKJ2015-C11); and Research Projects of City Environmental Protection Bureau of Pudong District (no. 2016012).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

11368_2019_2464_MOESM1_ESM.docx (220 kb)
ESM 1 (DOCX 219 kb)

References

  1. Berg B, McClaugherty C (2014) Plant litter: decomposition, humus formation, carbon sequestration, third ed. Springer, Berlin HeidelbergCrossRefGoogle Scholar
  2. Bergey DH, Holt JG (1994) Bergey’s manual of determinative bacteriology, ninth ed. Lippincott Williams & Wilkins, BaltimoreGoogle Scholar
  3. Caesar-Tonthat TC, Cochran VL (2000) Soil aggregate stabilization by a saprophytic lignin-decomposing basidiomycete fungus I. Microbiological aspects. Biol Fertil Soils 32:374–380CrossRefGoogle Scholar
  4. Carter MR, Gregorich EG (2008) Soil sampling and methods of analysis. CRC Press, FloridaGoogle Scholar
  5. Chen L, Xu J, Feng Y, Wang J, Yu Y, Brookes PC (2015) Responses of soil microeukaryotic communities to short-term fumigation-incubation revealed by MiSeq amplicon sequencing. Front Microbiol 6:1149Google Scholar
  6. Cheng X, Luo Y, Chen J, Lin G, Chen J, Li B (2006) Short-term C4 plant Spartina alterniflora invasions change the soil carbon in C3 plant-dominated tidal wetlands on a growing estuarine island. Soil Biol Biochem 38:3380–3386CrossRefGoogle Scholar
  7. Cheng X, Luo Y, Xu Q, Lin G, Zhang Q, Chen J, Li B (2010) Seasonal variation in CH4 emission and its 13C-isotopic signature from Spartina alterniflora and Scirpus mariqueter soils in an estuarine wetland. Plant Soil 327:85–94CrossRefGoogle Scholar
  8. Chomel M, Guittonny-Larchevêque M, Fernandez C, Gallet C, DesRochers A, Paré D, Jackson BG, Baldy V (2016) Plant secondary metabolites: a key driver of litter decomposition and soil nutrient cycling. J Ecol 104:1527–1541CrossRefGoogle Scholar
  9. Cotrufo MF, Wallenstein MD, Boot CM, Denef K, Paul E (2013) The Microbial Efficiency-Matrix Stabilization (MEMS) framework integrates plant litter decomposition with soil organic matter stabilization: do labile plant inputs form stable soil organic matter? Glob Chang Biol 19:988–995CrossRefGoogle Scholar
  10. Currin CA, Newell SY, Paerl HW (1995) The role of standing dead Spartina alterniflora and benthic microalgae in salt marsh food webs: considerations based on multiple stable isotope analysis. Mar Ecol-Prog Ser 121:99–116CrossRefGoogle Scholar
  11. Duan H, Wang L, Zhang Y, Fu X, Tsang YF, Wu J, Le Y (2018) Variable decomposition of two plant litters and their effects on the carbon sequestration ability of wetland soil in the Yangtze River estuary. Geoderma 319:230–238CrossRefGoogle Scholar
  12. Duarte CM, Middelburg JJ, Caraco N (2005) Major role of marine vegetation on the oceanic carbon cycle. Biogeosciences 2:1–8CrossRefGoogle Scholar
  13. Ertel JR, Hedges JI (1984) The lignin component of humic substances: distribution among soil and sedimentary humic, fulvic, and base-insoluble fractions. Geochim Cosmochim AC 48:2065–2074CrossRefGoogle Scholar
  14. Fan F, Li Z, Wakelin SA, Yu W, Liang Y (2012) Mineral fertilizer alters cellulolytic community structure and suppresses soil cellobiohydrolase activity in a long-term fertilization experiment. Soil Biol Biochem 55:70–77CrossRefGoogle Scholar
  15. Fernandez I, Cadisch G (2003) Discrimination against 13C during degradation of simple and complex substrates by two white rot fungi. Rapid Commun Mass Spectrom 17:2614–2620CrossRefGoogle Scholar
  16. Fukushima M, Yamamoto K, Ootsuka K, Komai T, Aramaki T, Ueda S, Horiya S (2009) Effects of the maturity of wood waste compost on the structural features of humic acids. Bioresour Technol 100:791–797CrossRefGoogle Scholar
  17. Goering HK, Van Soest PJ (1970) Forage fiber analysis. Agriculture Handbook No. 379, US Government Printing Office, Washington, DC (USDA-ARS)Google Scholar
  18. Graysston SJ, Wang S, Campbell CD, Edwards AC (1998) Selective influence of plant species on microbial diversity in the rhizosphere. Soil Biol Biochem 30:369–378CrossRefGoogle Scholar
  19. Han SI (2016) Phylogenetic characteristics of bacterial populations and isolation of aromatic compounds utilizing bacteria from humus layer of oak forest. Korean J Microbiol 52:175–182CrossRefGoogle Scholar
  20. Hu Y, Wang L, Tang Y, Li Y, Chen J, Xi X, Zhang Y, Fu X, Wu J, Sun Y (2014) Variability in soil microbial community and activity between coastal and riparian wetlands in the Yangtze River estuary—potential impacts on carbon sequestration. Soil Biol Biochem 70:221–228CrossRefGoogle Scholar
  21. Jex C, Pate G, Blyth A, Spencer R, Hernes P, Khan S, Baker A (2014) Lignin biogeochemistry: from modern processes to quaternary archives. Quat Sci Rev 87:46–59CrossRefGoogle Scholar
  22. José Luis M-M, María EH, Patricia M-C (2014) Comparing soil carbon sequestration in coastal freshwater wetlands with various geomorphic features and plant communities in Veracruz, Mexico. Plant Soil 378:189–203CrossRefGoogle Scholar
  23. Kelleher BP, Simpson AJ (2006) Humic substances in soils: are they really chemically distinct? Environ Sci Technol 40:4605–4611CrossRefGoogle Scholar
  24. Kutsch WL, Bahn M, Heinemeyer A (2010) Soil carbon dynamics. Cambridge University Press, New YorkCrossRefGoogle Scholar
  25. Lehmann J, Kleber M (2015) The contentious nature of soil organic matter. Nature 528:60–68CrossRefGoogle Scholar
  26. Lehmann J, Solomon D, Kinyangi J, Dathe L, Wirick S, Jacobsen C (2008) Spatial complexity of soil organic matter forms at nanometre scales. Nat Geosci 1:238–242CrossRefGoogle Scholar
  27. Li X, Liu JP, Tian B (2016) Evolution of the Jiuduansha wetland and the impact of navigation works in the Yangtze estuary, China. Geomorphology 253:328–339CrossRefGoogle Scholar
  28. Li X, Rui J, Mao Y, Yannarell A, Mackie R (2014) Dynamics of the bacterial community structure in the rhizosphere of a maize cultivar. Soil Biol Biochem 68:392–401CrossRefGoogle Scholar
  29. Li Y, Chen N, Harmon ME, Li Y, Cao X, Chappell MA, Mao J (2015) Plant species rather than climate greatly alters the temporal pattern of litter chemical composition during long-term decomposition. Sci Rep 5:15783CrossRefGoogle Scholar
  30. Liao C, Luo Y, Jiang L, Zhou X, Wu X, Fang C, Chen J, Li B (2007) Invasion of Spartina alterniflora enhanced ecosystem carbon and nitrogen stocks in the Yangtze estuary, China. Ecosystems 10:1351–1361CrossRefGoogle Scholar
  31. Liao C, Peng R, Luo Y, Zhou X, Wu X, Fang C, Chen J, Li B (2008) Altered ecosystem carbon and nitrogen cycles by plant invasion: a meta-analysis. New Phytol 177:706–714CrossRefGoogle Scholar
  32. Loya WM, Johnson LC, Nadelhoffer KJ (2004) Seasonal dynamics of leaf- and root-derived C in arctic tundra mesocosms. Soil Biol Biochem 36:655–666CrossRefGoogle Scholar
  33. Lundell TK, Mäkelä MR, de Vries RP, Hildén KS (2014) Chapter eleven—genomics, lifestyles and future prospects of wood-decay and litter-decomposing basidiomycota. Adv Bot Res 70:329–370CrossRefGoogle Scholar
  34. Lundell TK, Mäkelä MR, Hildén K (2010) Lignin-modifying enzymes in filamentous basidiomycetes—ecological, functional and phylogenetic review. J Basic Microbiol 50:5–20CrossRefGoogle Scholar
  35. Mazzilli S, Kemanian A, Ernst O, Jackson R, Pineiro G (2015) Greater humification of belowground than aboveground biomass carbon into particulate soil organic matter in no-till corn and soybean crops. Soil Biol Biochem 85:22–30CrossRefGoogle Scholar
  36. Mendes R, Kruijt M, de Bruijn I, Dekkers E, van der Voort M, Schneider JHM, Piceno YM, DeSantis TZ, Andersen GL, Bakker PAHM, Raaijmakers JM (2011) Deciphering the rhizosphere microbiome for disease-suppressive bacteria. Science 332:1097–1100CrossRefGoogle Scholar
  37. Millard P, Midwood AJ, Hunt JE, Whitehead D, Boutton TW (2008) Partitioning soil surface CO2 efflux into autotrophic and heterotrophic components, using natural gradients in soil δ13C in an undisturbed savannah soil. Soil Biol Biochem 40:1575–1582CrossRefGoogle Scholar
  38. Moorhead DL, Sinsabaugh RL (2006) A theoretical model of litter decay and microbial interaction. Ecol Monogr 76:151–174CrossRefGoogle Scholar
  39. Orellana R, Chaput G, Markillie LM, Mitchell H, Gaffrey M, Orr G, DeAngelis KM (2017) Multi-time series RNA-seq analysis of Enterobacter lignolyticus SCF1 during growth in lignin-amended medium. PLoS One 12:e0186440CrossRefGoogle Scholar
  40. Paul EA (2016) The nature and dynamics of soil organic matter: plant inputs, microbial transformations, and organic matter stabilization. Soil Biol Biochem 98:109–126CrossRefGoogle Scholar
  41. Peršoh D (2015) Plant-associated fungal communities in the light of meta’omics. Fungal Divers 75:1–25CrossRefGoogle Scholar
  42. Phillips DL, Gregg JW (2001) Uncertainty in source partitioning using stable isotopes. Oecologia 127:171–179CrossRefGoogle Scholar
  43. Quintino V, Sangiorgio F, Ricardo F, Mamede R, Pires A, Freitas R, Rodrigues AM, Basset A (2009) In situ experimental study of reed leaf decomposition along a full salinity gradient. Estuar Coast Shelf Sci 85:497–506CrossRefGoogle Scholar
  44. Ravit B, Ehrenfeld JG, Haggblom MM (2003) A comparison of sediment microbial communities associated with Phragmites australis and Spartina alterniflora in two brackish wetlands of New Jersey. Estuar Coasts 26:465–474CrossRefGoogle Scholar
  45. Šárka A, Tomáš C, Gerrit A, Hana Š, Jiří B, Jan F (2017) Retention of dead standing plant biomass (marcescence) increases subsequent litter decomposition in the soil organic layer. Plant Soil 418:571–579CrossRefGoogle Scholar
  46. Schmidt MW, Torn MS, Abiven S, Dittmar T, Guggenberger G, Janssens IA, Kleber M, Kogel-Knabner I, Lehmann J, Manning DA, Nannipieri P, Rasse DP, Weiner S, Trumbore SE (2011) Persistence of soil organic matter as an ecosystem property. Nature 478:49–56CrossRefGoogle Scholar
  47. Semenov AV, Pereira e Silva MC, Szturc-Koestsier AE, Schmitt H, Falcão Salles J, van Elsas JD (2012) Impact of incorporated fresh 13C potato tissues on the bacterial and fungal community composition of soil. Soil Biol Biochem 49:88–95CrossRefGoogle Scholar
  48. Sinsabaugh RL (2010) Phenol oxidase, peroxidase and organic matter dynamics of soil. Soil Biol Biochem 42:391–404CrossRefGoogle Scholar
  49. Sinsabaugh RL, Carreiro MM, Repert DA (2002) Allocation of extracellular enzymatic activity in relation to litter composition, N deposition, and mass loss. Biogeochemistry 60:1–24CrossRefGoogle Scholar
  50. Šnajdr J, Cajthaml T, Valášková V, Merhautová V, Petránková M, Spetz P, Leppänen K, Baldrian P (2011) Transformation of Quercus petraea litter: successive changes in litter chemistry are reflected in differential enzyme activity and changes in the microbial community composition. FEMS Microbiol Ecology 75:291–303CrossRefGoogle Scholar
  51. Strope PK, Nickerson KW, Harris SD, Moriyama EN (2011) Molecular evolution of urea amidolyase and urea carboxylase in fungi. BMC Evol Biol 11:1–15CrossRefGoogle Scholar
  52. Sun J, Steindler L, Thrash JC, Halsey KH, Smith DP, Carter AE, Landry ZC, Giovannoni SJ (2011) One carbon metabolism in SAR11 pelagic marine bacteria. PLoS One 6:e23973.  https://doi.org/10.1371/journal.pone.0023973 CrossRefGoogle Scholar
  53. Tang YS, Wang L, Jia JW, Fu XH, Le YQ, Xz C, Sun Y (2011) Response of soil microbial community in Jiuduansha wetland to different successional stages and its implications for soil microbial respiration and carbon turnover. Soil Biol Biochem 43:638–646CrossRefGoogle Scholar
  54. Vandenkoornhuyse P, Baldauf SL, Leyval C, Straczek J, Young JPW (2002) Extensive fungal diversity in plant roots. Science 295:2051CrossRefGoogle Scholar
  55. Vida C, Bonilla N, de Vicente A, Cazorla FM (2016) Microbial profiling of a suppressiveness-induced agricultural soil amended with composted almond shells. Front Microbiol 7:1–14CrossRefGoogle Scholar
  56. Waldrop MP, Firestone MK (2004) Microbial community utilization of recalcitrant and simple carbon compounds: impact of oak-woodland plant communities. Oecologia 138:275–284CrossRefGoogle Scholar
  57. Wang M, Wang Q, Sha C, Chen J (2018) Spartina alterniflorainvasion affects soil carbon in a C3 plant-dominated tidal marsh. Sci Rep 8(628).  https://doi.org/10.1038/s41598-017-19111-1
  58. Woo HL, Utturkar S, Klingeman D, Simmons BA, DeAngelis KM, Brown SD, Hazen TC (2014) Draft genome sequence of the lignin-degrading Burkholderia sp. strain LIG30, isolated from wet tropical forest soil. Genome Announc 2:e00637–e00614.  https://doi.org/10.1128/genomeA.00637-14 CrossRefGoogle Scholar
  59. Xia Y, Wang Y, Wang Y, Chin FY, Zhang T (2016) Cellular adhesiveness and cellulolytic capacity in Anaerolineae revealed by omics-based genome interpretation. Biotechnol Biofuels 9:111CrossRefGoogle Scholar
  60. Yan J, Wang L, Hu Y, Tsang YF, Zhang Y, Wu J, Fu X, Sun Y (2018) Plant litter composition selects different soil microbial structures and in turn drives different litter decomposition pattern and soil carbon sequestration capability. Geoderma 319:194–203CrossRefGoogle Scholar
  61. Yang W, An S, Zhao H, Xu L, Qiao Y, Cheng X (2016) Impacts of Spartina alterniflora invasion on soil organic carbon and nitrogen pools sizes, stability, and turnover in a coastal salt marsh of eastern China. Ecol Eng 86:174–182CrossRefGoogle Scholar
  62. Zhang WW, Lu ZT, Yang K, Zhu JJ (2017) Impacts of conversion from secondary forests to larch plantations on the structure and function of microbial communities. Appl Soil Ecol 111:73–83CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Key Laboratory of Yangtze River Water Environment, Ministry of Education, College of Environmental Science and EngineeringTongji UniversityShanghaiChina
  2. 2.Department of Science and Environmental StudiesThe Education University of Hong KongHong KongChina
  3. 3.Research Institute for Shanghai Pollution Control and Ecological SecurityShanghaiChina
  4. 4.Shanghai Jiuduansha Wetland Nature Reserve AdministrationShanghaiChina

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