Enhanced mineralization of sedimentary organic carbon induced by excess carbon from phytoplankton in a eutrophic plateau lake

Abstract

Purpose

Large additions of organic carbon (OC) have been introduced into the carbon cycle of lakes from algae during the process of lake eutrophication. The impact of eutrophication on OC burial and CO2 fixing has been widely studied; however, there is still a gap regarding the impact of excess OC from algae on sedimentary OC mineralization. In this study, we aim to fill this gap by analyzing in situ measurements.

Materials and methods

Three pairs of sediment cores collected from a plateau lake (Dianchi Lake) in 2006 and 2014 were used to estimate the accumulation loss rate (ALR) of OC (and thus the total mineralization rate) in the sediment. n-Alkanes, measured from the same sedimentary cores, were used to identify the source of OC. An OC mineralization experiment in a laboratory was used to confirm the enhanced effect of excess phytoplankton carbon on ALR and reveal the potential influence of microorganisms.

Results and discussion

The results indicate that the sedimentary core (core 3), with high excess OC from algae (located in an algal bloom area), possessed a higher ALR (85.66%) and a higher attenuation coefficient (0.078), indicating the low burial efficiency and short mineralization duration of OC. Sedimentary core 1, controlled by terrestrial OC, had a relatively lower ALR (64.60%) and lower attenuation coefficient (0.029), indicating a high burial efficiency and long period of OC mineralization. The mineralization of OC in core 2 was impacted by terrestrial and endogenous OC, with an ALR of 72.00% and attenuation coefficient of 0.064, which is between that of cores 1 and 3. Excess OC from algae corresponded to an increase in ALR by 32.60% when comparing core 1 to core 3. The increased ALR and attenuation coefficient could be caused by excess OC from algae.

Conclusions

Sedimentary OC mineralization indicates that the ALR with dominantly allochthonous OC (64.60%) is much lower than that controlled by autochthonous OC (85.66%). Excess OC from phytoplankton increases the mineralization of OC: not only via increased ALR but also increased mineralization speed. The laboratory experiment on the mixture of algae and sediment suggested that excess phytoplankton OC increased the emission of CO2 by 20–70% (mineralization rate).

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References

  1. Almeida RM, Nóbrega GN, Junger PC, Figueiredo AV, Andrade AS, de Moura CGB, Tonetta D, Oliveira JES, Araújo F, Rust F, Piñeiro-Guerra JM, Mendonça JJR, Medeiros LR, Pinheiro L, Miranda M, Costa MRA, Melo ML, Nobre RLG, Benevides T, Roland F, de Klein J, Barros NO, Mendonça R, Becker V, Huszar VLM, Kosten S (2016) High primary production contrasts with intense carbon emission in a eutrophic tropical reservoir. Front Microbiol 7(717). https://doi.org/10.3389/fmicb.2016.00717

  2. Algesten G, Sobek S, Bergström AK, Ågren A, Tranvik LJ, Jansson M (2003) Role of lakes for organic carbon cycling in the boreal zone. Glob Change Biol 10:141–147. https://doi.org/10.1046/j.1529-8817.2003.00721.x

    Article  Google Scholar 

  3. Anderson NJ, Bennion H, Lotter AF (2014) Lake eutrophication and its implications for organic carbon sequestration in Europe. Glob Change Biol 20:2741–2751

    Article  CAS  Google Scholar 

  4. Anderson NJ, Dietz RD, Engstrom DR (2013) Land-use change, not climate, controls organic carbon burial in lakes. P Roy Soc B-Biol Sci 280:3907–3910

    Article  CAS  Google Scholar 

  5. Baines SB, Pace ML, Karl DM (1994) Why does the relationship between sinking flux and plank tonic primary production differ between lakes and oceans? Limnol Oceanogr 39:213–226. https://doi.org/10.4319/lo.1994.39.2.0213

    Article  Google Scholar 

  6. Bastviken D, Tranvik LJ, Downing JA, Crill PM, Prast EA (2011) Freshwater methane emissions off set the continental carbon sink. Science 331:50–50

    Article  CAS  Google Scholar 

  7. Battin TJ, Kaplan LA, Findlay S, Hopkinson CS, Marti E, Aaron IP, Denis NJ, Francesc S (2008) Biophysical controls on organic carbon fluxes in fluvial networks. Nat Geosci 1:95–100

    Article  CAS  Google Scholar 

  8. Bengtsson MM, Wagner K, Burns NR, Herberg ER, Wanek W, Kaplan LA, Battin TJ (2014) No evidence of aquatic priming effects in hyporheic zone microcosms. Sci Rep-UK 4:5187. https://doi.org/10.1038/srep05187

    Article  CAS  Google Scholar 

  9. Benoy G, Cash K, McCauley E, Wrona F (2007) Carbon dynamics in lakes of the boreal forest under a changing climate. Environ Rev 15:175–189

    Article  CAS  Google Scholar 

  10. Bianchi TS (2011) The role of terrestrially derived organic carbon in the coastal ocean: a changing paradigm and the priming effect. Proc Natl Acad Sci U S A 108(49):19473–19481

    Article  Google Scholar 

  11. Blagodatskaya E, Kuzyakov Y (2008) Mechanisms of real and apparent priming effects and their dependence on soil microbial biomass and community structure: critical review. Biol Fertil Soils 45:115–131

    Article  Google Scholar 

  12. Borges AV, Darchambeau F, Teodoru CR, Marwick TR, Tamooh F, Geeraert N, Omengo FO, Guérin F, Lambert T, Morana C, Okuku E, Bouillon S (2015) Globally significant greenhouse-gas emissions from African inland waters. Nat Geosci 8:637–642. https://doi.org/10.1038/ngeo2486

    Article  CAS  Google Scholar 

  13. Butman D, Raymond PA (2011) Significant efflux of carbon dioxide from streams and rivers in the United States. Nat Geosci 4:839–842

    Article  CAS  Google Scholar 

  14. Butman D, Stackpoole S, Stets E, McDonald CP, Clow DW, Striegl RG (2016) Aquatic carbon cycling in the conterminous United States and implications for terrestrial carbon accounting. Proc Natl Acad Sci U S A 113:58–63. https://doi.org/10.1073/pnas.1512651112

    Article  CAS  Google Scholar 

  15. Butman DE, Wilson HF, Barnes RT, Xenopoulos MA, Raymond PA (2015) Increased mobilization of aged carbon to rivers by human disturbance. Nat Geosci 8(2):112–116

    Article  CAS  Google Scholar 

  16. Cardoso SJ, Vidal LO, Mendonça RF, Tranvik LJ, Sobek S, Roland F (2013) Spatial variation of sediment mineralization supports differential CO2 emissions from a tropical hydroelectric reservoir. Front Microbiol 4(101):1–7

    Google Scholar 

  17. Catalán N, Kellerman AM, Peter H, Carmona F, Tranvik LJ (2015) Absence of a priming effect on dissolved organic carbon degradation in lake water. Limnol Oceanogr 60:159–168

    Article  CAS  Google Scholar 

  18. Chmiel HE, Niggeman J, Koki J, Ferland ME, Dittmar T, Sobek S (2015) Uncoupled organic matter burial and quality in boreal lake sediments over the Holocene. J Geophys Res-Biogeo 120:1751–1763

    Article  CAS  Google Scholar 

  19. Dong X, Anderson NJ, Yang X, Chen X, Shen J (2012) Carbon burial by shallow lakes on the Yangtze floodplain and its relevance to regional carbon sequestration. Glob Change Biol 18(7):2205–2217

    Article  Google Scholar 

  20. Downing JA, Cole JJ, Middelburg JJ, Striegl RG, Duarte CM, Kortelainen P, Prairie YT, Laube KA (2008) Sediment organic carbon burial in agriculturally eutrophic impoundments over the last century. Global Biogeochem Cy 22:GB1018. https://doi.org/10.1029/2006GB002854

    Article  CAS  Google Scholar 

  21. Ferland ME, Prairie YT, Teodor C, del Giorgio PA (2014) Linking organic carbon sedimentation, burial efficiency, and long-term accumulation in boreal lakes. J Geophys Res-Biogeo 119:836–847. https://doi.org/10.1002/2013JG002345

    Article  CAS  Google Scholar 

  22. Gälman V, Rydberg J, de-Luna SS, Bindler R, Renberg I (2008) Carbon and nitrogen loss rates during aging of lake sediment: changes over 27 years studied in varved lake sediment. Limnol Oceanogr 53(3):1076–1082

    Article  Google Scholar 

  23. Galy V, Peucker-Ehrenbrink B, Eglinton T (2015) Global carbon export from the terrestrial biosphere controlled by erosion. Nature 521:204–207

    Article  CAS  Google Scholar 

  24. Gao L, Hou J, Toney J, MacDonald D, Huang Y (2011) Mathematical modeling of the aquatic macrophyte inputs of mid-chain n-alkyl lipids to lake sediments: implications for interpreting compound specific hydrogen isotopic records. Geochim Cosmochim Ac 75:3781–3791

    Article  CAS  Google Scholar 

  25. Gudasz C, Bastviken D, Premke K, Steger K, Tranvik LJ (2012) Constrained microbial processing of allochthonous organic carbon in boreal lake sediments. Limnol Oceanogr 57:163–175

    Article  CAS  Google Scholar 

  26. Gudasz C, Bastviken D, Steger K, Premke K, Sobek S, Tranvik LJ (2010) Temperature-controlled organic carbon mineralization in lake sediments. Nature 466:478–481

    Article  CAS  Google Scholar 

  27. Guenet B, Danger M, Abbadie L, Lacroix G (2010) Priming effect: bridging the gap between terrestrial and aquatic ecology. Ecology 91:2850–2861

    Article  Google Scholar 

  28. Guenet B, Juarez S, Bardoux G, Abbadie L, Chenu C (2012) Evidence that stable C is as vulnerable to priming effect as is more labile C in soil. Soil Biochem 52:43–48

    Article  CAS  Google Scholar 

  29. Guillemette F, von Wachenfeldt E, Kothawala DN, Bastviken D, Tranvik LJ (2017) Preferential sequestration of terrestrial organic matter in bore al lake sediments. J Geophys Res-Biogeo 122:863–874. https://doi.org/10.1002/2016JG003735

    Article  CAS  Google Scholar 

  30. Hastie A, Lauerwald R, Weyhenmeyer G, Sobek S, Verpoorter C, Regnier P (2017) CO2 evasion from boreal lakes: revised estimate, drivers of spatial variability, and future projections. Glob Change Biol:1–18. https://doi.org/10.1111/gcb.13.902

  31. Heathcote AJ, Anderson NJ, Prairie YT, Engstrom DR, del Giorgio PA (2015) Large increases in carbon burial in northern lakes during the Anthropocene. Nat Commun 6:10016. https://doi.org/10.1038/ncomms10016

    Article  CAS  Google Scholar 

  32. Hotchkiss ER, Hall Jr RO, Sponseller RA, Butman D, Klaminder J, Laudon H, Rosvall M, Karlsson J (2015) Sources of and processes controlling CO2 emissions change with the size of streams and rivers. Nat Geosci 8(9):696–699

    Article  CAS  Google Scholar 

  33. Huang CC, Wang XL, Yang H, Li YM, Wang YH, Chen X, Xu LJ (2014) Satellite data regarding the eutrophication response to human activities in the plateau lake Dianchi in China from 1974 to 2009. Sci Total Environ 485–486:1–11

    Article  CAS  Google Scholar 

  34. Huang CC, Yao L, Zhang YL, Huang T, Zhang ML, Zhu AX, Yang H (2017) Spatial and temporal variation in autochthonous and allochthonous contributors to increased organic carbon and nitrogen burial in a plateau lake. Sci Total Environ 603–604:390–400

    Article  CAS  Google Scholar 

  35. Huang CC, Zhang LL, Li YM, Lin C, Huang T, Zhang ML, Zhu AX, Yang H, Wang XL (2018) Carbon and nitrogen burial in a plateau lake during eutrophication and phytoplankton blooms. Sci Total Environ 616–617:296–304

    Article  CAS  Google Scholar 

  36. Isidorova A, Bravo AG, Riise G, Bouchet S, Björn E, Sobek S (2016) The effect of lake browning and respiration mode on the burial and fate of carbon and mercury in the sediment of two boreal lakes. J Geophys Res-Biogeo 121:233–245. https://doi.org/10.1002/2015JG003086

    Article  CAS  Google Scholar 

  37. Jonsson A, Meili M, Bergström AK, Jansson M (2001) Whole-lake mineralization of allochthonous and autochthonous organic carbon in a large humic lake (örträsket, N. Sweden). Limnol Oceanogr 46(7):1691–1700

    Article  CAS  Google Scholar 

  38. Kastowski M, Hinderer M, Vecsei A (2011) Long-term carbon burial in European lakes: analysis and estimate. Global Biogeochem Cy 25:GB3019

    Article  CAS  Google Scholar 

  39. Kothawala DN, Ji X, Laudon H, Agren AM, Futter MN, Kohler SJ, Tranvik LJ (2015) The relative influence of land cover, hydrology, and in-stream processing on the composition of dissolved organic matter in boreal streams. J Geophys Res-Biogeo 120:1491–1505. https://doi.org/10.1002/2015JG002946

    Article  CAS  Google Scholar 

  40. Kuzyakov Y, Bol R (2006) Sources and mechanisms of priming effect induced in two grassland soils amended with slurry and sugar. Soil Biol Biochem 38:747–758

    Article  CAS  Google Scholar 

  41. Kuzyakov Y, Friedel JK, Stahr K (2000) Review of mechanisms and quantification of priming effects. Soil Biol Biochem 32:1485–1498

    Article  CAS  Google Scholar 

  42. Kuzyakov Y (2010) Priming effects: interactions between living and dead organic matter. Soil Biol Biochem 42:1363–1371

    Article  CAS  Google Scholar 

  43. Lapierre JF, Guillemette F, Berggren M, del Giorgio PA (2013) Increases in terrestrially derived carbon stimulate organic carbon processing and CO2 emissions in boreal aqua-tic ecosystems. Nat Commun 4(1):–7

  44. Larsen S, Aanersen T, Hessen DO (2011) Climate change predicted to cause severe increase of organic carbon in lakes. Glob Change Biol 17:1186–1192

    Article  Google Scholar 

  45. Liu H, Liu WG (2016) N-alkane distributions and concentrations in algae, submerged plants and terrestrial plants from the Qinghai-Tibetan plateau. Org Geochem 99:10–22

    Article  CAS  Google Scholar 

  46. Marotta H, Duarte CM, Sobek S, Enrich-Prast A (2009) Large CO2 disequilibria in tropical lakes. Global Biochem Cy 23:GB4022. https://doi.org/10.1029/2008GB003434

    CAS  Article  Google Scholar 

  47. Marotta H, Pinho L, Gudasz C, Bastviken D, Tranvik LJ, Enrich-Prast A (2014) Greenhouse gas production in low-latitude lake sediments responds strongly to warming. Nat Clim Chang 4(6):467–470

    Article  CAS  Google Scholar 

  48. Mendonça R, Kosten S, Sobek S, Cardoso SJ, Figueiredo-Barros MP, Estrada CHD, Roland F (2016) Organic carbon burial efficiency in a subtropical hydroelectric reservoir. Biogeosciences 13:3331–3342

    Article  CAS  Google Scholar 

  49. Peter S, Isidorova A, Sobek S (2016) Enhanced carbon loss from anoxic lake sediment through diffusion of dissolved organic carbon. J Geophys Res-Biogeo 121:195–1977. https://doi.org/10.1002/2016JG003425

    Article  CAS  Google Scholar 

  50. Peter S, Agstam O, Sobek S (2017) Widespread release of dissolved organic carbon from anoxic boreal lake sediments. Inland Waters 7(2):151–163

    Article  CAS  Google Scholar 

  51. Ran L, Lu XX, Xin Z (2014) Erosion-induced massive organic carbon burial and carbon emission in the Yellow River basin, China. Biogeosciences 11:945–959

    Article  Google Scholar 

  52. Raymond PA, Hartmann J, Lauerwald R, Sobek S, McDonald C, Hoover M, Butman D, Striegl R, Mayorga E, Humborg C, Kortelainen P, Dürr H, Meybeck M, Ciais P, Guth P (2013) Global carbon dioxide emissions from inland waters. Nature 503:355–359

    Article  CAS  Google Scholar 

  53. Raymond PA, Oh NH, Turner RE, Broussard W (2008) Anthropogenically enhanced fluxes of water and carbon from the Mississippi River. Nature 451:449–452

    Article  CAS  Google Scholar 

  54. Sanchez-Cabeza JA, Ruiz-Fernández AC (2012) 210Pb sediment radio chronology: an integrated formulation and classification of dating models. Geochim Cosmoschim Ac 82:183–200

    Article  CAS  Google Scholar 

  55. Sobek S, DelSontro T, Wongfun N, Wehrli B (2012) Extreme organic carbon burial fuels intense methane bubbling in a temperate reservoir. Geophys Res Lett 39:L01401. https://doi.org/10.1029/2011GL050144

    Article  CAS  Google Scholar 

  56. Sobek S, Durisch-Kaiser E, Zurbrugg R, Wongfun N, Wessels M, Pasche N, Wehrli B (2009) Organic carbon burial efficiency in lake sediments controlled by oxygen exposure time and sediment source. Limnol Oceanogr 54:2243–2254

    Article  Google Scholar 

  57. Sobek S, Anderson NJ, Bernasconi SM, Del Sontro T (2014) Low organic carbon burial efficiency in arctic lake sediments. J Geophys res-biogeo 119, doi:10. In: 1002/2014JG002612

    Google Scholar 

  58. Sobek S, Zurbrügg R, Ostrovsky L (2011) The burial efficiency of organic carbon in the sediments of Lake Kinneret. Aquat Sci 73:355–364

    Article  CAS  Google Scholar 

  59. Spencer RG, Stubbins A, Hernes PJ, Baker A, Mopper K, Aufdenkampe AK, Dyda RY, Mwamba VL, Mangangu AM, Wabakanghanzi JN, Six J (2009) Photochemical degradation of dissolved organic matter and dissolved lignin phenols from the Congo River. J Geophys Res-Biogeo 114:G03010. https://doi.org/10.1029/2009JG000968

    CAS  Article  Google Scholar 

  60. Stackpoole SM, Butman DE, Clow DW, Verdin KL, Gaglioti BV, Genet H, Striegl RG (2017) Inland waters and their role in the carbon cycle of Alaska. Eco Appl 27(5):1403–1420

    Article  Google Scholar 

  61. Steinsberger T, Schmid M, Wüest A, Schwefel R, Wehrli B, Müller B (2017) Organic carbon mass accumulation rate regulates the flux of reduced substances from the sediments of deep lakes. Biogeosciences 14:3275–3285

    Article  CAS  Google Scholar 

  62. van Nugteren P, Moodley L, Brummer GJ, Heip CHR, Herman PMJ, Middelburg JJ (2009) Seafloor ecosystem functioning: the importance of organic matter priming. Mar Biol 156:2277–2287

    Article  Google Scholar 

  63. Ward ND, Bianchi TS, Sawakuchi HO, Gagne-Maynard W, Cunha AC, Brito DC, Neu V, de Matos Valerio A, da Silva R, Krusche AV, Richey JE, Keil RG (2016) The reactivity of plant-derived organic matter and the potential importance of priming effects along the lower Amazon River. J Geophys res-biogeo 121. In: doi:10.100 2/2016JG003342

    Google Scholar 

  64. Ward ND, Keil RG, Medeiros PM, Brito DC, Cunha AC, Dittmar T, Yager PL, Krusche AV, Richey JE (2013) Degradation of terrestrially derived macromolecules in the Amazon River. Nat Geosci 6(7):530–533

    Article  CAS  Google Scholar 

  65. Watanabe K, Kuwae T (2015) How organic carbon derived from multiple sources contributes to carbon sequestration processes in a shallow coastal system? Glob Change Biol 21:2612–2623

    Article  Google Scholar 

  66. Wehrli B (2013) Conduits of the carbon cycle. Nature 503(7476):346–347

    Article  CAS  Google Scholar 

  67. Wilkinson GM, Pace ML, Cole JJ (2013) Terrestrial dominance of organic matter in north temperate lakes. Global Biogeochem Cy 27:43–51. https://doi.org/10.1029/2012GB004453

    Article  CAS  Google Scholar 

  68. Xiong J, Liu Y, Lin X, Zhang H, Zeng J, Hou J, Yang Y, Yao T, Knight R, Chu H (2012) Geographic distance and pH drive bacterial distribution in alkaline lake sediments across Tibetan plateau. Environ Microbiol 14:2457–2466

    Article  CAS  Google Scholar 

  69. Zhang HH, Huang TL, Chen SN, Yang X, Lv K, Sekar R (2015) Abundance and diversity of bacteria in oxygen minimum drinking water reservoir sediments studied by quantitative PCR and pyrosequencing. Microb Ecol 69:618–629

    Article  Google Scholar 

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Acknowledgments

We are grateful to Nick Kleeman for the language editing. I also express my appreciation to two reviewers for their useful comments.

Funding

This study was supported by the National Natural Science Foundation of China (Grant Nos. 41773097, 41673108, and 41571324), a project funded by the Priority Academic Program Development of Jiangsu Higher Education Institutions, the Jiangsu Planned Projects for Postdoctoral Research Funds, Natural Science Research Project of Anhui Higher Education (KJ2014A280).

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Correspondence to Changchun Huang.

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Huang, C., Chen, Z., Gao, Y. et al. Enhanced mineralization of sedimentary organic carbon induced by excess carbon from phytoplankton in a eutrophic plateau lake. J Soils Sediments 19, 2613–2623 (2019). https://doi.org/10.1007/s11368-019-02261-2

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Keywords

  • Algal blooms
  • Carbon cycling
  • Dianchi Lake
  • Sources of organic carbon