Skip to main content
Log in

Microbes in a neutral-alkaline paddy soil react differentially to intact and acid washed biochar

  • Soils, Sec 5 • Soil and Landscape Ecology • Research Article
  • Published:
Journal of Soils and Sediments Aims and scope Submit manuscript

Abstract

Purpose

The effects of biochar additions on soil nutrients and biotic processes have been studied extensively. However, the impact of intact and acid washed biochar on the microbial community assembly process in a neutral-alkaline paddy soil remains unknown.

Materials and methods

A microcosm experiment with six treatments (CK: control; CB: CK-added intact biochar; CWB: CK-added acid washed biochar; NPK: N, P, and K fertilizer application; NPKB: NPK-added intact biochar; NPKWB: NPK-added acid washed biochar) was conducted using soil samples from a long-term rice–wheat rotation ecosystem. Soil microbial phospholipid fatty acids (PLFAs) and high-throughput sequencing were utilized to evaluate microbial biomass and community structure.

Results and discussion

Less than 24% of PLFA biomass dropped in CB and CWB treatments whereas 27% decreased in NPKB and NPKWB treatments. Archaeal diversity in NPK soils was lower than in CK soils but rose in NPKB and NPKWB soils. However, only intact biochar reduced bacterial diversity, whereas acid washed biochar reduced fungal diversity. Acidobacteria, Chloroflexi, Firmicutes, Nitrospirota, and Planctomycetota behaved differentially to both intact and acid washed biochar treatments. Biochar was more responsive to saprophytic than pathotrophic and symbiotrophic fungi. The soil pH and available P content influenced fungi community structure, whereas DOC, DON, NH4+-N, and NO3-N influenced bacteria community structure. Archaeal taxa were dominated by ammonia oxidizing and methane cycling species, which were susceptible to biochar treatment.

Conclusions

Our findings suggest that intact or acid washed biochar has a different effect on soil microbial sublineages (archaea, bacteria, and fungus) community, and then in turn modulated soil carbon and nitrogen cycling in the neutral-alkaline paddy soil.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Al-Wabel MI, Hussain Q, Usman ARA et al (2018) Impact of biochar properties on soil conditions and agricultural sustainability: a review. Land Degrad Dev 29:2124–2161

    Article  Google Scholar 

  • Ameloot N, Sleutel S, Case SDC et al (2014) C mineralization and microbial activity in four biochar field experiments several years after incorporation. Soil Biol Biochem 78:195–203

    Article  CAS  Google Scholar 

  • Anderson CR, Condron LM, Clough TJ et al (2011) Biochar induced soil microbial community change: implications for biogeochemical cycling of carbon, nitrogen and phosphorus. Pedobiologia 54:309–320

    Article  CAS  Google Scholar 

  • Andert J, Mumme J (2015) Impact of pyrolysis and hydrothermal biochar on gas-emitting activity of soil microorganisms and bacterial and archaeal community composition. Appl Soil Ecol 96:225–239

    Article  Google Scholar 

  • Andrés P, Rosell-Melé A, Colomer-Ventura F et al (2019) Belowground biota responses to maize biochar addition to the soil of a Mediterranean vineyard. Sci Total Environ 660:1522–1532

    Article  Google Scholar 

  • Bååth E, Anderson TH (2003) Comparison of soil fungal/bacterial ratios in a pH gradient using physiological and PLFA-based techniques. Soil Biol Biochem 35:955–963

    Article  Google Scholar 

  • Bai N, Zhang H, Zhou S et al (2020) Long-term effects of straw return and straw-derived biochar amendment on bacterial communities in soil aggregates. Sci Rep-UK 10:7891

    Article  CAS  Google Scholar 

  • Bai N, Zhang HL, Li S et al (2019) Long-term effects of straw and straw-derived biochar on soil aggregation and fungal community in a rice–wheat rotation system. PeerJ 6:e6171

    Article  Google Scholar 

  • Baker BJ, De Anda V, Seitz KW et al (2020) Diversity, ecology and evolution of Archaea. Nat Microbiol 5:887–900

    Article  CAS  Google Scholar 

  • Bates ST, Berg-Lyons D, Caporaso JG et al (2011) Examining the global distribution of dominant archaeal populations in soil. ISME J 5:908–917

    Article  CAS  Google Scholar 

  • Bi Y, Cai S, Wang Y et al (2020) Structural and microbial evidence for different soil carbon sequestration after four-year successive biochar application in two different paddy soils. Chemosphere 254:126881

    Article  CAS  Google Scholar 

  • Bligh EG, Dyer WJ (1959) A rapid method of total lipid extraction and purification. Can J Biochem Physiol 37:911–917

    Article  CAS  Google Scholar 

  • Bossolani JW, Crusciol CAC, Leite MFA et al (2021) Modulation of the soil microbiome by long-term Ca-based soil amendments boosts soil organic carbon and physicochemical quality in a tropical no-till crop rotation system. Soil Biol Biochem 156:108188

    Article  CAS  Google Scholar 

  • Callahan BJ, McMurdie PJ, Rosen MJ et al (2016) DADA2: High-resolution sample inference from Illumina amplicon data. Nat Methods 13:581–583

    Article  CAS  Google Scholar 

  • Chen J, Liu X, Zheng JW et al (2013) Biochar soil amendment increased bacterial but decreased fungal gene abundance with shifts in community structure in a slightly acid rice paddy from southwest China. Appl Soil Ecol 71:33–44

    Article  Google Scholar 

  • Chen LM, Zhang GL, Effland WR (2011) Soil characteristic response times and pedogenic thresholds during the 1000-year evolution of a paddy soil chronosequence. Soil Sci Soc Am J 75:1807–1820

    Article  CAS  Google Scholar 

  • Chen S, Zhou Y, Chen Y et al (2018) fastp: an ultra-fast all-in-one FASTQ preprocessor. Bioinformatics 34:884–890

    Article  Google Scholar 

  • Chen W, Meng J, Han X et al (2019) Past, present, and future of biochar. Biochar 1:75–87

    Article  Google Scholar 

  • Dai Z, Enders A, Rodrigues JLM et al (2018) Soil fungal taxonomic and functional community composition as affected by biochar properties. Soil Biol Biochem 126:159–167

    Article  CAS  Google Scholar 

  • Dai Z, Xiong X, Zhu H et al (2021) Association of biochar properties with changes in soil bacterial, fungal and fauna communities and nutrient cycling processes. Biochar 3:39–254

    Article  Google Scholar 

  • Doilom M, Guo JW, Phookamsak R et al (2020) Screening of phosphate-solubilizing fungi from air and soil in Yunnan, China: four novel species in Aspergillus, Gongronella, Penicillium, and Talaromyces. Front Microbiol 11:2443

    Article  Google Scholar 

  • Dutta T, Kwon E, Bhattacharya SS et al (2017) Polycyclic aromatic hydrocarbons and volatile organic compounds in biochar and biochar-amended soil: a review. GCB Bioenergy 9:990–1004

    Article  CAS  Google Scholar 

  • Evans PN, Parks DH, Chadwick GL et al (2015) Methane metabolism in the archaeal phylum Bathyarchaeota revealed by genome-centric metagenomics. Science 350:434–438

    Article  CAS  Google Scholar 

  • Fernández-Calviño D, Bååth E (2010) Growth response of the bacterial community to pH in soils differing in pH. FEMS Microbiol Ecol 73:149–156

    Google Scholar 

  • Fierer N (2017) Embracing the unknown: disentangling the complexities of the soil microbiome. Nat Rev Microbiol 15:579–590

    Article  CAS  Google Scholar 

  • Friedman J, Alm EJ (2012) Inferring correlation networks from genomic survey data. PLoS Comput Biol 8:e1002687

    Article  CAS  Google Scholar 

  • Frostegård Å, Tunlid A, Bååth E (2011) Use and misuse of PLFA measurements in soils. Soil Biol Biochem 43:1621–1625

    Article  Google Scholar 

  • Fu L, Lu Y, Tang L et al (2021) Dynamics of methane emission and archaeal microbial community in paddy soil amended with different types of biochar. Appl Soil Ecol 162:103892

    Article  Google Scholar 

  • Guo HJ, Ma L, Liang Y et al (2020a) Response of ammonia-oxidizing bacteria and archaea to long-term saline water irrigation in alluvial grey desert soils. Sci Rep-UK 10:489

    Article  CAS  Google Scholar 

  • Guo HN, Shi X, Ma L et al (2020b) Long-term irrigation with saline water decreases soil nutrients, diversity of bacterial communities, and cotton yields in a gray desert soil in china. Pol J Environ Stud 29:4077–4088

    Article  CAS  Google Scholar 

  • Harter J, Weigold P, El-Hadidi M et al (2016) Soil biochar amendment shapes the composition of N2O-reducing microbial communities. Sci Total Environ 562:379–390

    Article  CAS  Google Scholar 

  • He M, Xiong X, Wang L et al (2021) A critical review on performance indicators for evaluating soil biota and soil health of biochar-amended soils. J Hazard Mater 414:125378

    Article  CAS  Google Scholar 

  • Herbold CW, Lebedeva E, Palatinszky M et al (2016) Candidatus Nitrosotenuis, in: Bergey’s manual of systematics of archaea and bacteria. John Wiley & Sons, Ltd, pp 1–9

  • Hu HW, Zhang LM, Yuan CL et al (2013) Contrasting euryarchaeota communities between upland and paddy soils exhibited similar ph-impacted biogeographic patterns. Soil Biol Biochem 64:18–27

    Article  CAS  Google Scholar 

  • Jiang Y, Liang Y, Li C et al (2016) Crop rotations alter bacterial and fungal diversity in paddy soils across East Asia. Soil Biol Biochem 95:250–261

    Article  CAS  Google Scholar 

  • Jiang Z, Yang S, Pang Q et al (2021) Biochar improved soil health and mitigated greenhouse gas emission from controlled irrigation paddy field: insights into microbial diversity. J Clean Prod 318:128595

    Article  CAS  Google Scholar 

  • Kaiser C, Frank A, Wild B et al (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

    Article  CAS  Google Scholar 

  • Kaur A, Chaudhary A, Kaur A et al (2005) Phospholipid fatty acid – a bioindicator of environment monitoring and assessment in soil ecosystem. Curr Sci India 89:1103–1112

    CAS  Google Scholar 

  • Kerou M, Schleper C (2016) Nitrososphaera, in: Bergey’s manual of systematics of archaea and bacteria. John Wiley & Sons, Ltd, pp 1–10

  • Kohl M, Wiese S, Warscheid B (2011) Cytoscape: software for visualization and analysis of biological networks. In: Data mining in proteomics. Springer, pp 291–303

  • Lammel DR, Barth G, Ovaskainen O et al (2018) Direct and indirect effects of a pH gradient bring insights into the mechanisms driving prokaryotic community structures. Microbiome 6:106

    Article  Google Scholar 

  • Lawson CE, Wu S, Bhattacharjee AS et al (2017) Metabolic network analysis reveals microbial community interactions in anammox granules. Nat Commun 8:15416

    Article  CAS  Google Scholar 

  • Lehmann J, Rillig MC, Thies J et al (2011) Biochar effects on soil biota – a review. Soil Biol Biochem 43:1812–1836

    Article  CAS  Google Scholar 

  • Li F, Chen L, Zhang J et al (2017a) Bacterial community structure after long-term organic and inorganic fertilization reveals important associations between soil nutrients and specific taxa involved in nutrient transformations. Front Microbiol 8:187

    Google Scholar 

  • Li M, Li D, Tang Y et al (2017b) CytoCluster: a cytoscape plugin for cluster analysis and visualization of biological networks. Int J Mol Sci 18:1880

    Article  Google Scholar 

  • Liu Q, Li YH, Liu SL et al (2021) Anaerobic primed CO2 and CH4 in paddy soil are driven by Fe reduction and stimulated by biochar. Sci Total Environ 808:151911

    Article  Google Scholar 

  • Liu X, Li M, Castelle CJ et al (2018) Insights into the ecology, evolution, and metabolism of the widespread Woesearchaeotal leineages. Microbiome 6:102

    Article  Google Scholar 

  • Long XE, Yao H (2020) Phosphorus input alters the assembly of rice (oryza sativa l.) root-associated communities. Microb Ecol 79:357–366

    Article  Google Scholar 

  • Long XE, Yao H, Wang J et al (2015) Community structure and soil pH determine chemoautotrophic carbon dioxide fixation in drained paddy soils. Environ Sci Technol 49:7152–7160

    Article  CAS  Google Scholar 

  • Louca S, Parfrey LW, Doebeli M (2016) Decoupling function and taxonomy in the global ocean microbiome. Science 353:1272–1277

    Article  CAS  Google Scholar 

  • Lu H, Bian R, Xia X et al (2020) Legacy of soil health improvement with carbon increase following one time amendment of biochar in a paddy soil – a rice farm trial. Geoderma 376:114567

    Article  CAS  Google Scholar 

  • Lu W, Ding W, Zhang J et al (2014) Biochar suppressed the decomposition of organic carbon in a cultivated sandy loam soil: a negative priming effect. Soil Biol Biochem 76:12–21

    Article  CAS  Google Scholar 

  • Luo Y, Durenkamp M, De Nobili M et al (2011) Short term soil priming effects and the mineralisation of biochar following its incorporation to soils of different pH. Soil Biol Biochem 43:2304–2314

    Article  CAS  Google Scholar 

  • Magoč T, Salzberg SL (2011) FLASH: fast length adjustment of short reads to improve genome assemblies. Bioinformatics 27:2957–2963

    Article  Google Scholar 

  • Megyes M, Borsodi AK, Árendás T et al (2021) Variations in the diversity of soil bacterial and archaeal communities in response to different long-term fertilization regimes in maize fields. Appl Soil Ecol 168:104120

    Article  Google Scholar 

  • Minasny B, Hong SY, Hartemink AE et al (2016) Soil pH increase under paddy in South Korea between 2000 and 2012. Agric Ecosyst Environ 221:205–213

    Article  Google Scholar 

  • Nguyen NH, Song Z, Bates ST et al (2016) FUNGuild: an open annotation tool for parsing fungal community datasets by ecological guild. Fungal Ecol 20:241–248

    Article  Google Scholar 

  • Ning Q, Chen L, Jia Z et al (2020) Multiple long-term observations reveal a strategy for soil pH-dependent fertilization and fungal communities in support of agricultural production. Agric Ecosyst Environ 293:106837

    Article  CAS  Google Scholar 

  • Oksanen J, Blanchet FG, Friendly M et al (2020) Vegan: Community Ecology Package. R Package Version 2(5–6):2019

    Google Scholar 

  • Pan F, Li Y, Chapman SJ et al (2016) Microbial utilization of rice straw and its derived biochar in a paddy soil. Sci Total Environ 559:15–23

    Article  CAS  Google Scholar 

  • Paterson E, Thornton B, Midwood AJ et al (2008) Atmospheric CO2 enrichment and nutrient additions to planted soil increase mineralisation of soil organic matter, but do not alter microbial utilisation of plant- and soil C-sources. Soil Biol Biochem 40:2434–2440

    Article  CAS  Google Scholar 

  • Puissant J, Jones B, Goodall T et al (2019) The pH optimum of soil exoenzymes adapt to long term changes in soil pH. Soil Biol Biochem 138:107601

    Article  CAS  Google Scholar 

  • Samaddar S, Truu J, Chatterjee P et al (2021) Long-term inorganic nitrogen application changes the ammonia-oxidizing archaeal community composition in paddy soils. Eur J Soil Sci 72:2246–2260

    Article  CAS  Google Scholar 

  • Segata N, Izard J, Waldron L et al (2011) Metagenomic biomarker discovery and explanation. Genome Biol 12:1–18

    Article  Google Scholar 

  • Sheng Y, Cong W, Yang L et al (2019) Forest soil fungal community elevational distribution pattern and their ecological assembly processes. Front Microbiol 10:2226

    Article  Google Scholar 

  • Song Y, Zhang X, Ma B et al (2014) Biochar addition affected the dynamics of ammonia oxidizers and nitrification in microcosms of a coastal alkaline soil. Biol Fertil Soils 50:321–332

    Article  CAS  Google Scholar 

  • Soriano-Disla JM, Janik LJ, Viscarra Rossel RA et al (2014) The performance of visible, near-, and mid-infrared reflectance spectroscopy for prediction of soil physical, chemical, and biological properties. Appl Spectrosc Rev 49:139–186

    Article  CAS  Google Scholar 

  • Tang Z, Zhang L, He N et al (2021) Soil bacterial community as impacted by addition of rice straw and biochar. Sci Rep-UK 11:22185

    Article  CAS  Google Scholar 

  • Tian J, Wang J, Dippold M et al (2016) Biochar affects soil organic matter cycling and microbial functions but does not alter microbial community structure in a paddy soil. Sci Total Environ 556:89–97

    Article  CAS  Google Scholar 

  • Tolar BB, Mosier AC, Lund MB et al (2019) Nitrosarchaeum, in: Bergey’s manual of systematics of archaea and bacteria. John Wiley & Sons, Ltd, pp 1–9

  • Tripathi BM, Kim M, Tateno R et al (2015) Soil pH and biome are both key determinants of soil archaeal community structure. Soil Biol Biochem 88:1–8

    Article  CAS  Google Scholar 

  • Tripathi BM, Stegen JC, Kim M et al (2018) Soil pH mediates the balance between stochastic and deterministic assembly of bacteria. ISME J 12:1072–1083

    Article  CAS  Google Scholar 

  • Verbaendert I, Boon N, De Vos P et al (2011) Denitrification is a common feature among members of the genus Bacillus. Syst Appl Microbiol 34:385–391

    Article  CAS  Google Scholar 

  • Wang C, Chen D, Shen J et al (2021) Biochar alters soil microbial communities and potential functions 3–4 years after amendment in a double rice cropping system. Agric Ecosyst Environ 311:107291

    Article  CAS  Google Scholar 

  • Wang C, Shen J, Liu J et al (2019) Microbial mechanisms in the reduction of CH4 emission from double rice cropping system amended by biochar: a four-year study. Soil Biol Biochem 135:251–263

    Article  CAS  Google Scholar 

  • Wang N, Chang ZZ, Xue XM et al (2017) Biochar decreases nitrogen oxide and enhances methane emissions via altering microbial community composition of anaerobic paddy soil. Sci Total Environ 581–582:689–696

    Article  Google Scholar 

  • Wang YQ, Bai R, Di HJ et al (2018) Differentiated mechanisms of biochar mitigating straw-induced greenhouse gas emissions in two contrasting paddy soils. Front Microbiol 9:025066

    Article  Google Scholar 

  • Watzinger A (2015) Microbial phospholipid biomarkers and stable isotope methods help reveal soil functions. Soil Biol Biochem 86:98–107

    Article  CAS  Google Scholar 

  • Watzinger A, Feichtmair S, Kitzler B et al (2014) Soil microbial communities responded to biochar application in temperate soils and slowly metabolized 13C-labelled biochar as revealed by 13C PLFA analyses: results from a short-term incubation and pot experiment. Eur J Soil Sci 65:40–51

    Article  CAS  Google Scholar 

  • Wei L, Ge TD, Zhu ZK et al (2022) Paddy soils have a much higher microbial biomass content than upland soils: a review of the origin, mechanisms, and drivers. Agric Ecosyst Environ 326:107798

    Article  CAS  Google Scholar 

  • Xie F, Ma A, Zhou H et al (2020) Niche differentiation of denitrifying anaerobic methane oxidizing bacteria and archaea leads to effective methane filtration in a Tibetan alpine wetland. Environ Int 140:105764

    Article  CAS  Google Scholar 

  • Yan S, Niu Z, Yan H et al (2019) Biochar application significantly affects the N pool and microbial community structure in purple and paddy soils. PeerJ 7:e7576

    Article  Google Scholar 

  • Yang Q, Zhao N, Wang H et al (2020) Electrochemical and biochemical profiling of the enhanced hydrogenotrophic denitrification through cathode strengthening using bioelectrochemical system (BES). Chem Eng J 381:122686

    Article  CAS  Google Scholar 

  • Yin D, Li H, Wang H et al (2021) Impact of different biochars on microbial community structure in the rhizospheric soil of rice grown in albic soil. Molecules 26:4783

    Article  CAS  Google Scholar 

  • Yu Z, Ling L, Singh BP et al (2020) Gain in carbon: deciphering the abiotic and biotic mechanisms of biochar-induced negative priming effects in contrasting soils. Sci Total Environ 746:141057

    Article  CAS  Google Scholar 

  • Yuan CL, Zhang LM, Wang JT et al (2019a) Distributions and environmental drivers of archaea and bacteria in paddy soils. J Soils Sediments 19:23–37

    Article  CAS  Google Scholar 

  • Yuan HZ, Zhu ZK, Wei XM et al (2019b) Straw and biochar strongly affect functional diversity of microbial metabolism in paddy soils. J Integr Agric 18:1474–1485

    Article  CAS  Google Scholar 

  • Zelles L (1999) Fatty acid patterns of phospholipids and lipopolysaccharides in the characterisation of microbial communities in soil: a review. Biol Fertil Soils 29:111–129

    Article  CAS  Google Scholar 

  • Zhang H, Sun H, Zhou S et al (2019) Effect of straw and straw biochar on the community structure and diversity of ammonia-oxidizing bacteria and archaea in rice-wheat rotation ecosystems. Sci Rep-UK 9:9367

    Article  Google Scholar 

  • Zhang H, Wu X, Li G et al (2011) Interactions between arbuscular mycorrhizal fungi and phosphate-solubilizing fungus (Mortierella sp.) and their effects on Kostelelzkya virginica growth and enzyme activities of rhizosphere and bulk soils at different salinities. Biol Fertil Soils 47:543

    Article  CAS  Google Scholar 

  • Zhang L, Jing Y, Xiang Y et al (2018) Responses of soil microbial community structure changes and activities to biochar addition: a meta-analysis. Sci Total Environ 643:926–935

    Article  CAS  Google Scholar 

  • Zhang X, Liao X, Huang L et al (2021) Soil profile rather than reclamation time drives the mudflat soil microbial community in the wheat-maize rotation system of Nantong, China. J Soils Sediments 21:1672–1687

    Article  Google Scholar 

  • Zhou Z, Gao T, Zhu Q et al (2019) Increases in bacterial community network complexity induced by biochar-based fertilizer amendments to karst calcareous soil. Geoderma 337:691–700

    Article  CAS  Google Scholar 

  • Zhou Z, Pan J, Wang F et al (2018) Bathyarchaeota: globally distributed metabolic generalists in anoxic environments. FEMS Microbiol Rev 42:639–655

    Article  CAS  Google Scholar 

Download references

Acknowledgements

This research was supported by the National Natural Science Foundation of China (41773079).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Xi-En Long.

Ethics declarations

Competing interests

The authors declare no competing interests.

Additional information

Responsible editor: Bin Ma

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (PDF 430 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Wu, Y., Lu, S., Zhu, Y. et al. Microbes in a neutral-alkaline paddy soil react differentially to intact and acid washed biochar. J Soils Sediments 22, 3137–3150 (2022). https://doi.org/10.1007/s11368-022-03277-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11368-022-03277-x

Keywords

Navigation