Skip to main content
Log in

Effect of volatile organic compounds absorbed to fresh biochar on survival of Bacillus mucilaginosus and structure of soil microbial communities

  • SOILS, SEC 1 • SOIL ORGANIC MATTER DYNAMICS AND NUTRIENT CYCLING • RESEARCH ARTICLE
  • Published:
Journal of Soils and Sediments Aims and scope Submit manuscript

An Erratum to this article was published on 14 December 2014

Abstract

Purpose

Biochar is considered difficult for microorganisms to decompose, and volatile organic compounds (VOCs) sorbed to fresh biochar may affect the survival rate of inoculants or the structure of soil microbial communities. We tested the hypotheses that VOCs on fresh biochar may play a vital role in shaping the structure of soil microbial communities and determined if they inhibited or supported the growth of inoculants.

Materials and methods

We examined the growth of Bacillus mucilaginosus in mushroom medium-based biochar (MM-biochar), corn stalk-based biochar (CS-biochar), and rice straw-based biochar (RS-biochar) in comparison with peat. The composition of VOCs before and after the incubation was characterized by pyrolysis-gas chromatography/mass spectroscopy (GC-MS). The structure of a soil microbial community incubated in biochar was examined via denaturing gradient gel electrophoresis (DGGE). Canonical correspondence analysis (CCA) was applied to reveal the contribution of pH, K and Na, and diversity indices from VOC fingerprints to diversity indices in DGGE profiles.

Results and discussion

In the present study, all biochars were able to support B. mucilaginosus at population densities analogous to peat. Phenols comprise a fraction of the VOCs that potentially could be toxic to some microbes and inhibit their growth in the short time. The structure of the inoculated soil microbial communities in terms of the diversity indices calculated from 16S ribosomal DNA (16S rDNA) and 18S rDNA DGGE profiles was greatly affected by biochar. Besides, CCA revealed the role of VOCs in shaping the structure of soil microbial communities.

Conclusions

VOCs absorbed to biochar, despite their short life spans, could support the survival of B. mucilaginosus, demonstrating the potential of biochars as carriers for inoculants. The changes in the soil microbial communities induced by fresh biochar may not represent the long-term “biochar effect.” Therefore, future work needs to appreciate mechanisms underlying aged biochar on the structure of soil microbial communities.

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
Fig. 6
Fig. 7
Fig. 8
Fig. 9
Fig. 10

Similar content being viewed by others

References

  • Anderson CR, Condron LM, Clough TJ, Fiers M, Stewart A, Hill RA, Sherlock RR (2011) Biochar induced soil microbial community change: implications for biogeochemical cycling of carbon, nitrogen and phosphorus. Pedobiologia 54:309–320

    Article  CAS  Google Scholar 

  • Bao S (1999) Soil agricultural chemistry analysis. China Agriculture Press, Beijing

    Google Scholar 

  • Brockwell J (1977) Application of legume seed inoculants. Treatise on Dinitrogen Fixation (USA)

  • Bruun EW, Ambus P, Egsgaard H, Hauggaard NH (2012) Effects of slow and fast pyrolysis biochar on soil C and N turnover dynamics. Soil Biol Biochem 46:73–79

    Article  CAS  Google Scholar 

  • Chen J, Liu X, Zheng J, Zhang B, Lu H, Chi Z, Yu X (2013a) 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 WF, Zhang WM, Meng J (2013b) Advances and prospects in research of biochar utilization in agriculture. Sci Agric Sin 46:3324–3333

    CAS  Google Scholar 

  • Farrell M, Kuhn TK, Macdonald LM, Maddern TM, Murphy DV, Hall PA, Baldock JA (2013) Microbial utilisation of biochar-derived carbon. Sci Total Environ 465:288–297

    Article  CAS  Google Scholar 

  • Fritze H, Pennanen T, Kitunen V (1998) Characterization of dissolved organic carbon from burned humus and its effects on microbial activity and community structure. Soil Biol Biochem 30:687–693

    Article  CAS  Google Scholar 

  • Gardes M, Bruns TD (1993) ITS primers with enhanced specificity for basidiomycetes-application to the identification of mycorrhizae and rusts. Mol Ecol 2:113–118

    Article  CAS  Google Scholar 

  • Glaser B (2007) Prehistorically modified soils of Central Amazonia: a model for sustainable agriculture in the 21st century? Philos T Roy Soc B 362:187–196

    Article  CAS  Google Scholar 

  • Glaser B, Birk JJ (2012) State of the scientific knowledge on properties and genesis of Anthropogenic Dark Earths in Central Amazonia (terra preta de Índio). Geochim Cosmochim Acta 82:39–51

    Article  CAS  Google Scholar 

  • Glaser B, Lehmann J, Zech W (2002) Ameliorating physical and chemical properties of highly weathered soils in the tropics with charcoal. Biol Fertil Soils 35:219–230

    Article  CAS  Google Scholar 

  • Graber ER, Harel YM, Kolton M, Cytryn E, Silber A, David DR, Elad Y (2010) Biochar impact on development and productivity of pepper and tomato grown in fertigated soilless media. Plant Soil 337:481–496

    Article  CAS  Google Scholar 

  • Grandy AS, Sinsabaugh RL, Neff JC, Stursova M, Zak DR (2008) Nitrogen deposition effects on soil organic matter chemistry are linked to variation in enzymes, ecosystems and size fractions. Biogeochemistry 91:37–49

    Article  CAS  Google Scholar 

  • Grossman JM, O’Neill BE, Tsai SM, Liang B, Neves E, Lehmann J, Thies JE (2010) Amazonian anthrosols support similar microbial communities that differ distinctly from those extant in adjacent, unmodified soils of the same mineralogy. Microb Ecol 60:192–205

    Article  CAS  Google Scholar 

  • Gurtler JB, Boateng AA, Han Y, Douds DD Jr (2014) Inactivation of E. coli O157:H7 in cultivable soil by fast and slow pyrolysis-generated biochar. Foodborne Pathog Dis 11:215–223

    Article  Google Scholar 

  • Hale SE, Lehmann J, Rutherford D, Zimmerman AR, Bachmann RT, Shitumbanuma V, Cornelissen G (2012) Quantifying the total and bioavailable polycyclic aromatic hydrocarbons and dioxins in biochars. Appl Microbiol Biot 46:2830–2838

    CAS  Google Scholar 

  • Herrmann L, Lesueur D (2013) Challenges of formulation and quality of biofertilizers for successful inoculation. Appl Microbiol Biot 97:8859–8873

    Article  CAS  Google Scholar 

  • Insam H, Seewald SA (2010) Volatile organic compounds (VOCs) in soils. Biol Fertil Soils 46:199–213

    Article  CAS  Google Scholar 

  • Jin H (2010) Characterization of microbial life colonizing biochar and biochar amended soils. PhD Dissertation, Cornell University

  • Kaal J, Rumpel C (2009) Can pyrolysis-GC/MS be used to estimate the degree of thermal alteration of black carbon? Org Geochem 40:1179–1187

    Article  CAS  Google Scholar 

  • Kim JS, Sparovek G, Longo RM, Melo WJ, Crowley D (2007) Bacterial diversity of terra preta and pristine forest soil from the western Amazonia. Soil Biol Biochem 39:684–690

    Article  CAS  Google Scholar 

  • Kuwatsova S, Shindo H (1973) Behavior of phenolic substances in the decaying process of plants. Identification and quantitative determination of phenolic acids in rice straw and its decayed products by gas chromatography. Soil Sci Plant Nutr 19:219–227

    Article  Google Scholar 

  • Lehmann J (2007) A handful of carbon. Nature 447:143–144

    Article  CAS  Google Scholar 

  • Luo Y, Durenkamp M, De Nobili M, Lin Q, Devonshire BJ, Brookes PC (2012) Microbial biomass growth, following incorporation of biochars produced at 350 °C or 700 °C, in a silty-clay loam soil of high and low pH. Soil Biol Biochem 57:513–523

    Article  Google Scholar 

  • McClellan AT, Deenik J, Uehara G, Antal M (2007) Effects of Flashed Carbonized© Macadamia Nutshell charcoal on plant growth and soil chemical properties. a a, 80(100), 120

  • Muyzer G, De Waal EC, Uitterlinden AG (1993) Profiling of complex microbial populations by denaturing gradient gel electrophoresis analysis of polymerase chain reaction-amplified genes coding for 16S rRNA. Appl Environ Microbiol 59:695–700

    CAS  Google Scholar 

  • Neves EG, Petersen JB, Bartone RN, Augusto DSC (2003) Historical and socio-cultural origins of Amazonian dark earths. In: Lehmann J, Kern D, Glaser B, Woods WI (eds) Amazonian dark earths: origin, properties, management. Kluwer Academic Publishers, London, pp 29–50

    Google Scholar 

  • Ng EL, Patti AF, Rose MT, Schefe CR, Wilkinson K, Smernik RJ, Cavagnaro TR (2013) Does the chemical nature of soil carbon drive the structure and functioning of soil microbial communities? Soil Biol Biochem 70:54–61

    Article  Google Scholar 

  • O’Neill B, Grossman J, Tsai SM, Gomes JE, Peterson J, Lehmann J, Neves EG, Thies JE (2009) Bacterial community composition in Brazilian Anthrosols and adjacent soils characterized using culturing and molecular identification. Microb Ecol 58:23–35

    Article  Google Scholar 

  • Pietikäinen J, Kiikkilä O, Fritze H (2000) Charcoal as a habitat for microbes and its effect on the microbial community of the underlying humus. Oikos 89:231–242

    Article  Google Scholar 

  • Prayogo C, Jones JE, Baeyens J, Bending GD (2013) Impact of biochar on mineralisation of C and N from soil and willow litter and its relationship with microbial community biomass and structure. Biol Fertil Soils 50:695–702

    Article  Google Scholar 

  • Ruivo MLP, Amarante CB, Oliveira MLS, Muniz ICM, Santos DAM (2009) Microbial population and biodiversity in Amazonian Dark Earth soils. In: Amazonian Dark Earths: Wim Sombroek’s Vision (ed) Springer, Berlin, pp 351–362

  • Rutigliano FA, Romano M, Marzaioli R, Baglivo I, Baronti S, Miglietta F, Castaldi S (2014) Effect of biochar addition on soil microbial community in a wheat crop. Eur J Soil Biol 60:9–15

    Article  CAS  Google Scholar 

  • Saranya K, Santhana P, Kumutha K, French J (2011) Potential for biochar as an alternate carrier to lignite for the preparation of biofertilizers in India. Int J Agri Environ Biot 4:167–172

    Google Scholar 

  • Spokas KA, Novak JM, Stewart CE, Cantrell KB, Uchimiya M, DuSaire MG, Ro KS (2011) Qualitative analysis of volatile organic compounds on biochar. Chemosphere 85:869–882

    Article  CAS  Google Scholar 

  • Sun D, Meng J, Chen W (2013) Effects of abiotic components induced by biochar on microbial communities. Acta Agr Scand B-S P 63:1–9

    Google Scholar 

  • Taketani RG, Lima AB, da Conceição Jesus E, Teixeira WG, Tiedje JM, Tsai SM (2013) Bacterial community composition of anthropogenic biochar and Amazonian anthrosols assessed by 16S rRNA gene 454 pyrosequencing. Anton Leeuw 104:233–242

    Article  CAS  Google Scholar 

  • Villar MC, González-Prieto SJ, Carballas T (1997) Evaluation of three organic wastes for reclaiming burnt soils: improvement in the recovery of vegetation cover and soil fertility in pot experiments. Biol Fertil Soils 26:122–129

    Article  Google Scholar 

  • Watzinger A, Feichtmair S, Kitzler B, Zehetner F, Kloss S, Wimmer B, Soja G (2013) 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  Google Scholar 

  • White TJ, Buns TD, Lee S, Taylor J (1990) Analysis of phylogenetic relationships by amplification and direct sequencing of ribosomal RNA genes. In: Innis MA, Gefland DH, Sninsky JJ, White TJ (eds) PCR protocols: a guide to methods and applications. Academic, New York, pp 315–322

    Chapter  Google Scholar 

  • Woods WI, Denevan WM (2009) Amazonian Dark Earths: the first century of reports, in: Amazonian Dark Earths: Wim Sombroek’s Vision (eds) Springer, Berlin, pp 1–14

Download references

Acknowledgments

The authors would like to acknowledge funding from Special Fund for Agro-scientific Research in Public Interest (201303095), National Key Technology R&D Program of the Ministry of Science and Technology (2012BAD14B01), and Research and Application of the Soil Amelioration Technology upon Tobacco Cultivation & Biochar Incorporation. Also, this work was supported by Graduate Student Innovation Cultivation Program, Shenyang Agricultural University. We would like to express our gratitude to Lauren Hale for her assistance to the language polishing.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Wenfu Chen.

Additional information

Responsible editor: Leo Condron

Daquan Sun and Jun Meng contributed equally to this work.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Sun, D., Meng, J., Liang, H. et al. Effect of volatile organic compounds absorbed to fresh biochar on survival of Bacillus mucilaginosus and structure of soil microbial communities. J Soils Sediments 15, 271–281 (2015). https://doi.org/10.1007/s11368-014-0996-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11368-014-0996-z

Keywords

Navigation