Abstract
Dark microbial CO2 fixation plays a crucial role in soil organic carbon (SOC) sequestration, but the fungus contributions to this process in varying agroecosystems remain unclear. This study investigated fungal CO2 fixation in 29 soil samples collected from the major agricultural regions across China. Phospholipid fatty analysis-stable isotope probing revealed variations in fungal fixation by 2.2 to 65.5% of the total microbial CO2 fixation. CO2 assimilation of ten fungal strains belonging to the phyla Ascomycota and Basidiomycota was determined in three different media using an isotope labeling experiment. Trichocladium uniseriatum had the highest CO2 fixation capacity. T. uniseriatum had the reductive tricarboxylic acid cycle (rTCA) for CO2 assimilation associated with sulfite metabolism. T. uniseriatum was thus selected for use in soil inoculation experiments, aimed to trace the fractionation of its fixed carbon in SOC. The CO2 fixation rate of T. uniseriatum was 0.07–0.09 μg C per g of soil per day. Notably, 77–82% of the fixed C was partitioned into the mineral-associated soil organic carbon. This study highlights the significance of fungal CO2 fixation in soil carbon sequestration.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Akinyede R, Taubert M, Schrumpf M, Trumbore S, Küsel K (2022) Dark CO2 fixation in temperate beech and pine forest soils. Soil Biol Biochem 165:108526. https://doi.org/10.1016/j.soilbio.2021.108526
Atomi H (2002) Microbial enzymes involved in carbon dioxide fixation. J Biosci Bioeng 94:497–505. https://doi.org/10.1016/S1389-1723(02)80186-4
Bastos A, Fleischer K (2021) Fungi are key to CO2 response of soil. Nature 591:532–534. https://doi.org/10.1038/d41586-021-00737-1
Berg I (2011) Ecological aspects of the distribution of different autotrophic CO2 fixation pathways. Appl Environ Microbiol 77:1925–1936. https://doi.org/10.1128/AEM.02473-10
Braun A, Spona-Friedl M, Avramov M, Elsner M, Baltar F, Reinthaler T, Herndl GJ, Griebler C (2021) Reviews and syntheses: heterotrophic fixation of inorganic carbon – significant but invisible flux in environmental carbon cycling. Biogeosciences 18:3689–3700. https://doi.org/10.5194/bg-18-3689-2021
Buyanovsky GA, Wagner GH (1983) Annual cycles of carbon dioxide level in soil air. Soil Sci Soc Am J 47:1139–1145. https://doi.org/10.2136/sssaj1983.03615995004700060016x
Camenzind T, Mason-Jones K, Mansour I, Rillig MC, Lehmann J (2023) Formation of necromass-derived soil organic carbon determined by microbial death pathways. Nat Geosci 16:115–122. https://doi.org/10.1038/s41561-022-01100-3
Castellani A (1939) Viability of some pathogenic fungi in distilled water. AM J Trop Med Hyg 42:225–226
Chen H, Wang F, Kong W, Jia H, Zhou T, Xu R, Wu G, Wang J, Wu J (2021) Soil microbial CO2 fixation plays a significant role in terrestrial carbon sink in a dryland ecosystem: a four-year small-scale field-plot observation on the Tibetan Plateau. Sci Total Environ 761:143282. https://doi.org/10.1016/j.scitotenv.2020.143282
Fang Y, Singh BP, Collins D, Armstrong R, Van Zwieten L, Tavakkoli E (2020) Nutrient stoichiometry and labile carbon content of organic amendments control microbial biomass and carbon-use efficiency in a poorly structured sodic-subsoil. Biol Fert Soils 56:219–233. https://doi.org/10.1007/s00374-019-01413-3
Figueroa IA, Barnum TP, Somasekhar PY, Carlstrom CI, Engelbrektson AL, Coates JD (2018) Metagenomics-guided analysis of microbial chemolithoautotrophic phosphite oxidation yields evidence of a seventh natural CO2 fixation pathway. PNAS 115:E92–E101. https://doi.org/10.1073/pnas.1715549114
Fuchs G (2011) Alternative pathways of carbon dioxide fixation: insights into the early evolution of life? In: Gottesman S, Harwood CS (Eds). Rev Microbiol 65:631–659. https://doi.org/10.1146/annurev-micro-090110-102801
Garland G, Bunemann EK, Oberson A, Frossard E, Snapp S, Chikowo R, Six J (2018) Phosphorus cycling within soil aggregate fractions of a highly weathered tropical soil: a conceptual model. Soil Biol Biochem 116:91–98. https://doi.org/10.1016/j.soilbio.2017.10.007
Ge T, Wu X, Chen X, Yuan H, Zou Z, Li B, Zhou P, Liu S, Tong C, Brookes P, Wu J (2013) Microbial phototrophic fixation of atmospheric CO2 in China subtropical upland and paddy soils. Geoc Cosmoc 113:70–78. https://doi.org/10.1016/j.gca.2013.03.020
He L, Mazza Rodrigues JL, Soudzilovskaia NA, Barceló M, Olsson PA, Song C, Tedersoo L, Yuan F, Yuan F, Lipson DA, Xu X (2020) Global biogeography of fungal and bacterial biomass carbon in topsoil. Soil Biol Biochem 151:108024. https://doi.org/10.1016/j.soilbio.2020.108024
Hoff KJ, Stanke M (2013) WebAUGUSTUS-a web service for training AUGUSTUS and predicting genes in eukaryotes. Nuc Ac Res 41:W123–W128. https://doi.org/10.1093/nar/gkt418
Jiang JR, Cai L, Liu F (2017) Oligotrophic fungi from a carbonate cave, with three new species of Cephalotrichum. Mycology 8:164–177. https://doi.org/10.1080/21501203.2017.1366370
Joergensen RG (2022) Phospholipid fatty acids in soil—drawbacks and future prospects. Biol Fert Soils 58:1–6. https://doi.org/10.1007/s00374-021-01613-w
Kaiser C, Frank A, Wild B, Koranda M, Richter A (2010) Negligible contribution from roots to soil-borne phospholipid fatty acid fungal biomarkers 18:2ω6,9 and 18:1ω9. Soil Biol Biochem 42:1650–1652. https://doi.org/10.1016/j.soilbio.2010.05.019
Kanehisa M, Sato Y, Kawashima M, Furumichi M, Tanabe M (2016) KEGG as a reference resource for gene and protein annotation. Nuc Ac Res 44:D457–D462. https://doi.org/10.1093/nar/gkv1070
Kleber M, Eusterhues K, Keiluweit M, Mikutta C, Mikutta R, Nico PS (2015) Mineral–organic associations: formation, properties, and relevance in soil environments. In: Sparks DL (Ed). Adv Agron 130:1–140. https://doi.org/10.1016/bs.agron.2014.10.005
Koechli C, Campbell A, Pepe-Ranney C, Buckley D (2018) Assessing fungal contributions to cellulose degradation in soil by using high-throughput stable isotope probing. Soil Biol Biochem 130:150–158. https://doi.org/10.1016/j.soilbio.2018.12.013
Larmour R, Marchant R (1977) Carbon dioxide fixation and conidiation in Fusarium culmorum grown in continuous culture. Microbiology 99:59–68. https://doi.org/10.1099/00221287-99-1-59
Li PP, Han YL, He JZ, Zhang SQ, Zhang LM (2019) Soil aggregate size and long- term fertilization effects on the function and community of ammonia oxidizers. Geoderma 338:107–117. https://doi.org/10.1016/j.geoderma.2018.11.033
Li F, Chen L, Zhao ZH, Li Y, Yu HY, Wang Y, Zhang JB, Han YL (2023) The changes of chemical molecular components in soil organic matter are associated with fungus Mortierella capitata K. Soil Till Res 227:105598. https://doi.org/10.1016/j.still.2022.105598
Liang C, Balser TC (2011) Microbial production of recalcitrant organic matter in global soils: implications for productivity and climate policy. Nat Rev Microbiol 9:2386. https://doi.org/10.1038/nrmicro2386-c1
Liao H, Hao X, Qin F, Delgado-Baquerizo M, Liu Y, Zhou J, Cai P, Chen W, Huang Q (2022) Microbial autotrophy explains large-scale soil CO2 fixation. Global Change Biol 00:1–12. https://doi.org/10.1111/gcb.16452
Liao JD, Boutton TW, Jastrow JD (2006) Organic matter turnover in soil physical fractions following woody plant invasion of grassland: evidence from natural 13C and 15N. Soil Biol Biochem 38:3197–3210. https://doi.org/10.1016/j.soilbio.2006.04.004
Liu L, Gunina A, Zhang F, Cui Z, Tian J (2023) Fungal necromass increases soil aggregation and organic matter chemical stability under improved cropland management and natural restoration. Sci Total Environ 858:159953. https://doi.org/10.1016/j.scitotenv.2022.159953
Lukaszkiewicz Z, Paszewski A (1976) Hyper-repressible operator-type mutant in sulphate permease gene of Aspergillus nidulans. Nature 259:337–338. https://doi.org/10.1038/259337a0
Luo R, Liu B, Xie Y, Li Z, Huang W, Yuan J, He G, Chen Y, Pan Q, Liu Y, Tang J, Wu G, Zhang H, Shi Y, Liu Y, Yu C, Wang B, Lu Y, Han C et al (2012) SOAPdenovo2: an empirically improved memory-efficient short-read de novo assembler. Gigascience 1:18. https://doi.org/10.1186/2047-217x-1-18
Lynn TM, Ge T, Yuan H, Wei X, Wu X, Xiao K, Kumaresan D, Yu SS, Wu J, Whiteley AS (2017) Soil carbon-fixation rates and associated bacterial diversity and abundance in three natural ecosystems. Microb Ecol 73:645–657. https://doi.org/10.1007/s00248-016-0890-x
Manirakiza E, Ziadi N, St Luce M, Hamel C, Antoun H, Karam A (2019) Nitrogen mineralization and microbial biomass carbon and nitrogen in response to co-application of biochar and paper mill biosolids. Appl Soil Ecol 142:90–98. https://doi.org/10.1016/j.apsoil.2019.04.025
Miltner A, Bombach P, Schmidt-Bruecken B, Kaestner M (2012) SOM genesis: microbial biomass as a significant source. Biogeochemistry 111:41–55. https://doi.org/10.1007/s10533-011-9658-z
Mirocha CJ, DeVay JE (1971) Growth of fungi on an inorganic medium. Can J Microbiol 17:1373–1378. https://doi.org/10.1139/m71-219
Nel JA, Cramer MD (2019) Soil microbial anaplerotic CO2 fixation in temperate soils. Geoderma 335:170–178. https://doi.org/10.1016/j.geoderma.2018.08.014
Olsen SR, Cole CV, Watanabe FS, Dean LA (1954) Estimation of available phosphorus in soils by extraction with sodium bicarbonate. In: USDA Cricular 939. U.S. Government Printing Office, Washington DC
Parkinson SM, Killham K, Wainwright M (1990) Assimilation of 14CO2 by Fusarium oxysporum grown under oligotrophic conditions. Mycol Res 94:959–964. https://doi.org/10.1016/S0953-7562(09)81312-9
Parkinson SM, Wainwright M, Killham K (1989) Observations on oligotrophic growth of fungi on silica gel. Mycol Res 93:529–534. https://doi.org/10.1016/S0953-7562(89)80048-6
Paul EA, Morris SJ, Conant RT, Plante AF (2006) Does the acid hydrolysis–incubation method measure meaningful soil organic carbon pools? Soil Sci Soc Am J 70:1023–1035. https://doi.org/10.2136/sssaj2005.0103
Pilsyk S, Mieczkowski A, Golan MP, Wawrzyniak A, Kruszewska JS (2020) Internalization of the Aspergillus nidulans AstA transporter into mitochondria depends on growth conditions, and affects ATP levels and sulfite oxidase activity. Int J Mol Sci 21:7727. https://doi.org/10.3390/ijms21207727
Quideau SA, McIntosh ACS, Norris CE, Lloret E, Swallow MJB, Hannam K (2016) Extraction and analysis of microbial phospholipid fatty acids in soils. J Vis Exp 114:54360. https://doi.org/10.3791/54360
Šantrůčková H, Kotas P, Bárta J, Urich T, Čapek P, Palmtag J, Eloy Alves RJ, Biasi C, Diáková K, Gentsch N, Gittel A, Guggenberger G, Hugelius G, Lashchinsky N, Martikainen PJ, Mikutta R, Schleper C, Schnecker J, Schwab C et al (2018) Significance of dark CO2 fixation in arctic soils. Soil Biol Biochem 119:11–21. https://doi.org/10.1016/j.soilbio.2017.12.021
Šantrůčková H, Šimek M (1997) Effect of soil CO2 concentration on microbial biomass. Biol Fert Soils 25:269–273. https://doi.org/10.1007/s003740050313
Seah BKB, Antony CP, Huettel B, Zarzycki J, von Borzyskowski LS, Erb TJ, Kouris A, Kleiner M, Liebeke M, Dubilier N, Gruber-Vodicka HR (2019) Sulfur-oxidizing symbionts without canonical genes for autotrophic CO2 fixation. Mbio 10:540435. https://doi.org/10.1128/mBio.01112-19
Shi M, Li J, Gao R, Song X, Wang G, Gao Y, Yan S (2023) Contrasting effects of elevated CO2 on autotrophic prokaryotes with different CO2 fixation strategies in tea plantation soil. Biol Fert Soils 59:205–215. https://doi.org/10.1007/s00374-023-01700-0
Siletti CE, Zeiner CA, Bhatnagar JM (2017) Distributions of fungal melanin across species and soils. Soil Biol Biochem 113:285–293. https://doi.org/10.1016/j.soilbio.2017.05.030
Smith KR, Desai MA, Rogers JV, Houghton RA (2013) Joint CO2 and CH4 accountability for global warming. PNAS 110:E2865–E2874. https://doi.org/10.1073/pnas.1308004110
Sokol NW, Bradford MA (2019) Microbial formation of stable soil carbon is more efficient from belowground than aboveground input. Nat Geosci 12:46–54. https://doi.org/10.1038/s41561-018-0258-6
Spohn M, Müller K, Höschen C, Mueller CW, Marhan S (2019) Dark microbial CO2 fixation in temperate forest soils increases with CO2 concentration. Global Change Biol 00:1–10. https://doi.org/10.1111/gcb.14937
Twining CW, Taipale SJ, Ruess L, Bec A, Martin-Creuzburg D, Kainz MJ (2020) Stable isotopes of fatty acids: current and future perspectives for advancing trophic ecology. Philos T R Soc B: Biol Sci 375:20190641. https://doi.org/10.1098/rstb.2019.0641
Wainwright M, Grayston SJ (1988) Fungal growth and stimulation by thiosulphate under oligocarbotrophic conditions. Trans Brit Mycol Soc 91:149–156. https://doi.org/10.1016/S0007-1536(88)80016-0
Willers C, Jansen van Rensburg PJ, Claassens S (2015) Phospholipid fatty acid profiling of microbial communities–a review of interpretations and recent applications. J Appl Microbiol 119:1207–1218. https://doi.org/10.1111/jam.12902
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. https://doi.org/10.1016/0038-0717(90)90046-3
Wu X, Ge T, Yuan H, Li B, Zhu H, Zhou P, Sui F, O’Donnell AG, Wu J (2014) Changes in bacterial CO2 fixation with depth in agricultural soils. Appl Microbiol Biotechnol 98:2309–2319. https://doi.org/10.1007/s00253-013-5179-0
Xiao H, Li Z, Chang X, Deng L, Nie X, Liu C, Liu L, Jiang J, Chen J, Wang D (2018) Microbial CO2 assimilation is not limited by the decrease in autotrophic bacterial abundance and diversity in eroded watershed. Biol Fert Soils 54:595–605. https://doi.org/10.1007/s00374-018-1284-7
Yuan H, Ge T, Chen C, O'Donnell AG, Wu J (2012) Significant role for microbial autotrophy in the sequestration of soil carbon. Appl Environ Microb 78:2328–2336. https://doi.org/10.1128/aem.06881-11
Zelle RM, Trueheart J, Harrison JC, Pronk JT, van Maris AJA (2010) Phosphoenolpyruvate carboxykinase as the sole anaplerotic enzyme in Saccharomyces cerevisiae. Appl Environ Microb 76:5383–5389. https://doi.org/10.1128/aem.01077-10
Funding
National Key Research and Development Program of China (2022YFD1500203), The National Natural Science Foundation of China (42007005), the Strategic Priority Research Program of the Chinese Academy of Sciences (XDA24020104). B.K.S works on microbial function that is supported by the Australian Research Council (DP190103714).
Author information
Authors and Affiliations
Contributions
J.B.Z and Z.J.J conceived the idea. F. L. and L.C. performed all the experiments. Y.L.H collected soil samples, determined soil physiochemical properties, and cultivated the strain in this study. Y.F.C contributed to data analysis. Experimental design was further modified by Z.J.J and B.K.S. F.L. wrote the first draft of the manuscript with inputs from Z.J.J and B.K.S., and all authors discussed the results, critically reviewed the manuscript, and approved its publication.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare no competing interests
Additional information
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary information
ESM 1
(DOCX 671 kb)
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Li, F., Jia, ZJ., Chen, L. et al. Fixation of CO2 by soil fungi: contribution to organic carbon pool and destination of fixed carbon products. Biol Fertil Soils 59, 791–802 (2023). https://doi.org/10.1007/s00374-023-01750-4
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00374-023-01750-4