Abstract
Purpose
Microalgae, biochar, or organic manure (OM) can be used as soil amendments to enhance soil organic carbon (OC) content. In the present study, a mixture of all three was used to test whether they could further improve soil OC content and the soil’s ability to retain and fix carbon.
Materials and methods
A laboratory incubation study was carried out to evaluate the efficacy of using microalgae, biochar, OM, or their mixture, as a soil amendment to improve OC in soil extract. Metabolic processes and soil microbial community structuring were analyzed to explore the mechanism by which the mixture increased the capacity of soil to act as a carbon sink.
Results and discussion
OC increased markedly (2.9 times its initial level) following the amendment of the soil with a treatment comprising microalgae, biochar, and the highest dose of OM. Microalgal metabolites were utilized by soil microorganisms as a carbon source. Biochar reduced the concentration of extracellular polysaccharides, whereas OM increased extracellular protein concentration. These metabolites affected the relative proportions of different groups of soil microorganisms, thereby increasing the proportion of Rhodobacter and Runella, which exerted a positive synergistic effect on soil OC and increased the soil’s capacity to fix carbon.
Conclusions
A mixture including microalga, biochar, and OM as a soil amendment improved the OC of soil extract, and its effect was greater than that of any of its components alone. The findings of this study can help in devising ways to increase the OC content and the CO2-fixing capacity of the soil.





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References
Bamminger C, Poll C, Sixt C, Högy P, Wüst D, Kandeler E, Marhan S (2016) Short-term response of soil microorganisms to biochar addition in a temperate agroecosystem under soil warming. Agric Ecosyst Environ 233:308–317
Cardozo KHM, Guaratini T, Barros MP, Falcão VR, Tonon AP, Lopes NP, Campos S, Torres MA, Souza AO, Colepicolo P, Pinto E (2007) Metabolites from algae with economical impact. Comp Biochem Physiol, Part C: Toxicol Pharmacol 146:60–78
Claesson MJ, O'Sullivan O, Wang Q, Nikkilä J, Marchesi JR, Smidt H, de Vos WM, Ross RP, O'Toole PW (2009) Comparative analysis of pyrosequencing and a phylogenetic microarray for exploring microbial community structures in the human distal intestine. PLoS One 4:e6669. https://doi.org/10.1371/journal.pone.0006669
de la Rosa JM, Rosado M, Paneque M, Miller AZ, Knicker H (2018) Effects of aging under field conditions on biochar structure and composition: implications for biochar stability in soils. Sci Total Environ 613-614:969–976
Deb D, Kloft M, Lässig J, Walsh S (2016) Variable effects of biochar and P solubilizing microbes on crop productivity in different soil conditions. Agroecol Sustain Food Syst 40:145–168
DuBois M, Gilles KA, Hamilton JK, Rebers PA, Smith F (1956) Colorimetric method for determination of sugars and related substances. Anal Chem 28:350–356
Eswaran H, Van Den Berg E, Reich P (1993) Organic carbon in soils of the world. Soil Sci Soc Am J 57:192–194
Foster EJ, Hansen N, Wallenstein M, Cotrufo MF (2016) Biochar and manure amendments impact soil nutrients and microbial enzymatic activities in a semi-arid irrigated maize cropping system. Agric Ecosyst Environ 233:404–414
Garrity G, Boone DR, Castenholz RW (2001) Bergey’s manual of systematic bacteriology vol 1. Springer-Verlag New York, New York doi:https://doi.org/10.1007/978-0-387-21609-6
Gascó G, Paz-Ferreiro J, Cely P, Plaza C, Méndez A (2016) Influence of pig manure and its biochar on soil CO2 emissions and soil enzymes. Ecol Eng 95:19–24
Geisseler D, Scow KM (2014) Long-term effects of mineral fertilizers on soil microorganisms – a review. Soil Biol Biochem 75:54–63
Hu J, Guo H, Wang X, Gao MT, Yao G, Tsang YF, Li J, Yan J, Zhang S (2019) Utilization of the saccharification residue of rice straw in the preparation of biochar is a novel strategy for reducing CO2 emissions. Sci Total Environ 650:1141–1148
Hu J, Xue Y, Li J, Wang L, Zhang S, Wang Y-n, Gao M-t (2016) Characterization of a designed synthetic autotrophic-heterotrophic consortia for fixing CO2 without light. RSC Adv 6:78161–78169
Kozich JJ, Westcott SL, Baxter NT, Highlander SK, Schloss PD (2013) Development of a dual-index sequencing strategy and curation pipeline for analyzing amplicon sequence data on the MiSeq illumina sequencing platform. Appl Environ Microbiol 79:5112–5120
Lal R (2004) Soil carbon sequestration impacts on global climate change and food security. Science 304:1623–1627
Langille MGI, Zaneveld J, Caporaso JG, McDonald D, Knights D, Reyes JA, Clemente JC, Burkepile DE, Vega Thurber RL, Knight R, Beiko RG, Huttenhower C (2013) Predictive functional profiling of microbial communities using 16S rRNA marker gene sequences. Nat Biotechnol 31:814–821
Li S, Liang C, Shangguan Z (2017) Effects of apple branch biochar on soil C mineralization and nutrient cycling under two levels of N. Sci Total Environ 607-608:109–119
Miltner A, Richnow H-H, Kopinke F-D, Kästner M (2004) Assimilation of CO2 by soil microorganisms and transformation into soil organic matter. Org Geochem 35:1015–1024
Mullen RW, Thomason WE, Raun WR (1999) Estimated increase in atmospheric carbon dioxide due to worldwide decrease in soil organic matter. Commun Soil Sci Plant Anal 30:1713–1719
Nayak M, Karemore A, Sen R (2016) Performance evaluation of microalgae for concomitant wastewater bioremediation, CO2 biofixation and lipid biosynthesis for biodiesel application. Algal Res 16:216–223
Nicoloso RS, Rice CW, Amado TJC, Costa CN, Akley EK (2018) Carbon saturation and translocation in a no-till soil under organic amendments. Agric Ecosyst Environ 264:73–84
Pruvost J, Van Vooren G, Le Gouic B, Couzinet-Mossion A, Legrand J (2011) Systematic investigation of biomass and lipid productivity by microalgae in photobioreactors for biodiesel application. Bioresour Technol 102:150–158
Raya-Moreno I, Cañizares R, Domene X, Carabassa V, Alcañiz JM (2017) Comparing current chemical methods to assess biochar organic carbon in a Mediterranean agricultural soil amended with two different biochars. Sci Total Environ 598:604–618
Šantrůčková H, Bird MI, Elhottová D, Novák J, Picek T, Šimek M, Tykva R (2005) Heterotrophic fixation of CO2 in soil. Microb Ecol 49:218–225
Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB, Lesniewski RA, Oakley BB, Parks DH, Robinson CJ, Sahl JW, Stres B, Thallinger GG, van Horn DJ, Weber CF (2009) Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 75:7537–7541
Schmidt MWI, Torn MS, Abiven S, Dittmar T, Guggenberger G, Janssens IA, Kleber M, Kögel-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
Solovchenko A, Solovchenko O, Khozin-Goldberg I, Didi-Cohen S, Pal D, Cohen Z, Boussiba S (2013) Probing the effects of high-light stress on pigment and lipid metabolism in nitrogen-starving microalgae by measuring chlorophyll fluorescence transients: studies with a Δ5 desaturase mutant of Parietochloris incisa (Chlorophyta, Trebouxiophyceae). Algal Res 2:175–182
Usman ARA et al (2016) Conocarpus biochar induces changes in soil nutrient availability and tomato growth under saline irrigation. Pedosphere 26:27–38
Venkata S, Rajvanshi M, Navish K, Govindachary S, Prasad V, Dasgupta S (2017) Carbon streaming in microalgae: extraction and analysis methods for high value compounds. Bioresour Technol 244:1304–1316
Wang R, Peng B, Huang K (2015) The research progress of CO2 sequestration by algal bio-fertilizer in China. J CO2 Util 11:67–70
Wang Y-n, Tsang YF, Wang L, Fu X, Li H, Hu J, Le Y (2017) Influence of reduced sulfur on carbon fixation efficiency of Halothiobacillus neapolitanus and its mechanism. Chem Eng J 326:249–256
Wu Y, Jiang Y (2016) A case study on the method-induced difference in the chemical properties and biodegradability of soil water extractable organic carbon of a granitic forest soil. Sci Total Environ 565:656–662
Xu X, Kan Y, Zhao L, Cao X (2016) Chemical transformation of CO2 during its capture by waste biomass derived biochars. Environ Pollut 213:533–540
Zhang S, Wang L, Wei W, Hu J, Mei S, Zhao Q, Tsang YF (2018) Enhanced roles of biochar and organic fertilizer in microalgae for soil carbon sink. Biodegradation 29:313–321
Zheng J, Han J, Liu Z, Xia W, Zhang X, Li L, Liu X, Bian R, Cheng K, Zheng J, Pan G (2017) Biochar compound fertilizer increases nitrogen productivity and economic benefits but decreases carbon emission of maize production. Agric Ecosyst Environ 241:70–78
Zhou Z, Gan Z, Shangguan Z, Zhang F (2013) Effects of long-term repeated mineral and organic fertilizer applications on soil organic carbon and total nitrogen in a semi-arid cropland. Eur J Agron 45:20–26
Acknowledgments
This work was supported by the Natural Science Foundation of Shanghai (No. 16ZR1440000); the Youth Innovation Fund for Interdisciplinary Research of SARI (No. Y526453235); the National Natural Science Foundation of China (No. 51878646 and No. 21577101); the Scientific Research Projects of Shanghai Science and Technology Committee (No. 16391902000); the Research Grants Council of the Hong Kong SAR, China (No. 28300015); the Youth Innovation Promotion Association, CAS (No. 2017353); and the Internal Research Grant (NO. DSRAF-6 SP1, RG78/2015-2016R, and RG50/2017-2018R) of the Education University of Hong Kong.
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Hu, J., Guo, H., Xue, Y. et al. Using a mixture of microalgae, biochar, and organic manure to increase the capacity of soil to act as carbon sink. J Soils Sediments 19, 3718–3727 (2019). https://doi.org/10.1007/s11368-019-02337-z
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DOI: https://doi.org/10.1007/s11368-019-02337-z


