Skip to main content
Log in

Microbial consumption and production of volatile organic compounds at the soil-litter interface

  • Published:
Biogeochemistry Aims and scope Submit manuscript

Abstract

Substantial amounts of volatile organic compounds (VOCs) can be released during decomposition and these compounds can affect atmospheric chemistry, belowground processes, and the structure of microbial communities in litter and soil. However, we have a limited understanding of the types, quantities and ecological impacts of VOCs emitted from litter. Here we used a closed flow-through system and proton transfer reaction mass spectrometry (PTR-MS) to characterize VOC emissions from soil and two litter types (Pinus taeda and Acer rubrum) over a 72-day incubation period. Microbial respiration rates were measured throughout the incubation, and the soils were harvested at the end of the incubation to determine how litter VOCs influenced soil C dynamics, N mineralization rates, and bacterial communities. Using the PTR-MS we identified over 100 VOCs, with 10 VOCs making up the majority of emissions. VOCs accounted for up to 2.5% of the C flux from litter. Soil was a net sink of litter VOCs, absorbing up to 80% of VOCs released by litter, and exposure of soil to litter VOCs increased microbial respiration rates in soil by up to 15%. However, we observed negligible impacts of litter VOCs on soil nutrient levels and bacterial community structure, suggesting that soils must be exposed to higher concentrations of VOCs than observed in our study, to cause effects on these soil characteristics. Overall, VOCs appear to have an important influence on C dynamics at the soil-litter interface and VOC emissions from decomposing litter may represent an understudied component of biosphere–atmosphere interactions.

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.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Amaral JA, Knowles R (1997) Inhibition of methane consumption in forest soils and pure cultures of methanotrophs by aqueous forest soil extracts. Soil Biol Biochem 29:1713–1720

    Article  Google Scholar 

  • Amaral JA, Knowles R (1998) Inhibition of methane consumption in forest soils by monoterpenes. J Chem Ecol 24:723–734

    Article  Google Scholar 

  • Asensio D, Penuelas J, Filella I, Llusia J (2007) On-line screening of soil VOCs exchange responses to moisture, temperature and root presence. Plant Soil 291:249–261

    Article  Google Scholar 

  • Bunge M, Araghipour N, Mikoviny T, Dunkl J, Schnitzhofer R, Hansel A, Schinner F, Wisthaler A, Margesin R, Mark TD (2008) On-line monitoring of microbial volatile metabolites by proton transfer reaction-mass spectrometry. Appl Environ Microbiol 74:2179–2186

    Article  Google Scholar 

  • Cleveland CC, Yavitt JB (1998) Microbial consumption of atmospheric isoprene in a temperate forest soil. Appl Environ Microbiol 64:172–177

    Google Scholar 

  • de Gouw J, Warneke C, Karl T, Eerdekens G, van der Veen C, Fall R (2003) Sensitivity and specificity of atmospheric trace gas detection by proton-transfer-reaction mass spectrometry. Int J Mass Spectrom 223:365–382

    Article  Google Scholar 

  • DeSantis TZ, Hugenholtz P, Larsen N, Rojas M, Brodie EL, Keller K, Huber T, Dalevi D, Hu P, Andersen GL (2006) Greengenes, a chimera-checked 16S rRNA gene database and workbench compatible with ARB. Appl Environ Microbiol 72:5069–5072

    Article  Google Scholar 

  • Fierer N, Schimel JP, Holden PA (2003) Variations in microbial community composition through two soil depth profiles. Soil Biol Biochem 35:167–176

    Article  Google Scholar 

  • Fierer N, Hamady M, Lauber CL, Knight R (2008) The influence of sex, handedness, and washing on the diversity of hand surface bacteria. Proc Natl Acad Sci 105:17994–17999

    Article  Google Scholar 

  • Hamady M, Walker JJ, Harris JK, Gold NJ, Knight R (2008) Error-correcting barcoded primers for pyrosequencing hundreds of samples in multiplex. Nat Methods 5:235–237. doi:10.1038/nmeth.1184

    Article  Google Scholar 

  • Isidorov V, Jdanova M (2002) Volatile organic compounds from leaves litter. Chemosphere 48:975–979. doi:PIIS0045-6535(02)00074-7

    Article  Google Scholar 

  • Jacob DJ, Field BD, Jin EM, Bey I, Li Q, Logan JA, Yantosca RM, Singh HB (2002) Atmospheric budget of acetone. J Geophys Res 107(D10):4100

    Google Scholar 

  • Kesselmeier J, Staudt M (1999) Biogenic volatile organic compounds (VOC): an overview on emission, physiology and ecology. J Atmos Chem 33:23–88

    Article  Google Scholar 

  • Lauber CL, Strickland MS, Bradford MA, Fierer N (2008) The influence of soil properties on the structure of bacterial and fungal communities across land-use types. Soil Biol Biochem 40:2407–2415. doi:10.1016/j.soilbio.2008.05.021

    Article  Google Scholar 

  • Lauber CL, Hamady M, Knight R, Fierer F (2009) Pyrosequencing-based assessment of soil pH as a predictor of soil bacterial community structure at the continental scale. Appl Environ Microbiol 75:5111–5120. doi:10.1128/AEM.00335-09

    Article  Google Scholar 

  • Leff JW, Fierer N (2008) Volatile organic compound (VOC) emissions from soil and litter samples. Soil Biol Biochem 40:1629–1636. doi:10.1016/j.soilbio.2008.01.018

    Article  Google Scholar 

  • Lindinger W, Hansel A, Jordan A (1998) On-line monitoring of volatile organic compounds at pptv levels by means of proton-transfer-reaction mass spectrometry (PTR-MS) medical applications, food control and environmental research. Int J Mass Spectrom Ion Process 173:191–241. doi:10.1016/S0168-1176(97)00281-4

    Article  Google Scholar 

  • Litvak ME, Madronich S, Monson RK (2008) Herbivore-induced monoterpene emissions from coniferous forests: Potential impact on local tropospheric chemistry. Ecol Appl 9:1147–1159

    Article  Google Scholar 

  • Lozupone CA, Knight R (2005) UniFrac: a new phylogenetic method for comparing microbial communities. Appl Environ Microbiol 71:8228–8235. doi:10.1128/AEM.71.12.8228-8235.2005

    Article  Google Scholar 

  • Lozupone CA, Knight R (2008) Species divergence and the measurement of microbial diversity. FEMS Microbiol Rev 32:557–578. doi:10.1111/j.1574-6976.2008.00111

    Article  Google Scholar 

  • Lozupone CA, Hamady M, Knight R (2006) UniFrac: an online tool for comparing microbial community diversity in a phylogenetic context. Bioinformatics 7:371. doi:10.1186/1471-2105-7-371

    Article  Google Scholar 

  • Mackie AE, Wheatley RE (1999) Effects and incidence of volatile organic compound interactions between soil bacterial and fungal isolates. Soil Biol Biochem 31:375–385

    Article  Google Scholar 

  • Mayrhofer S, Mikoviny T, Waldhuber S, Wagner AO, Innerebner G, Frank-Whittle IH, Mark TD, Hansel A, Insam H (2006) Microbial community related to volatile organic compound (VOC) mission in household biowaste. Environ Microbiol 8:1960–1974. doi:10.1111/j.1462-2920.2006.01076

    Article  Google Scholar 

  • Monson RK (2002) Volatile organic compound emissions from terrestrial ecosystems: A primary biological control over atmospheric chemistry. Isr J Chem 42:29–42

    Article  Google Scholar 

  • Monson RK, Holland EA (2003) Biospheric trace gas fluxes and their control over tropospheric chemistry. Annu Rev Ecol Syst 32:547–576

    Article  Google Scholar 

  • Neff JC, Asner GP (2001) Dissolved organic carbon in terrestrial ecosystems: synthesis and a model. Ecosystems 4:29–48. doi:10.1007/s100210000058

    Article  Google Scholar 

  • Owen SM, Clark S, Pompe M, Semple KT (2007) Biogenic volatile organic compounds as potential carbon sources for microbial communities in soil from the rhizosphere of Populus tremula. FEMS Microbiol Lett 268:34–39. doi:10.1111/j.1574-6968.2006.00602

    Article  Google Scholar 

  • Paavolainen L, Kitunen V, Smolander A (1998) Inhibition of nitrification in forest soil by monoterpenes. Plant Soil 205:147–154

    Article  Google Scholar 

  • Richter D, Markewitz D (2001) Understanding soil change. Cambridge University Press, Cambridge, UK

    Google Scholar 

  • Schade GW, Crutzen PJ (1999) CO emissions from degrading plant matter (II): estimate of a global source strength. Tellus B 51:909–918. doi:10.1034/j.1600-0889.1999.t01-4-00004

    Article  Google Scholar 

  • Schade GW, Goldstein AH (2001) Fluxes of oxygenated volatile organic compounds from a ponderosa pine plantation. J Geophys Res 106:3111–3123

    Article  Google Scholar 

  • Schink B, Zeikus J (1980) Microbial methanol formation: a major end product of pectin metabolism. Curr Microbiol 4:387–389. doi:10.1007/BF02605383

    Article  Google Scholar 

  • Smolander A, Ketola RA, Kotiaho T, Kanerva S, Suominen K, Kitunen V (2006) Volatile monoterpenes in soil atmosphere under birch and conifers: effects on soil N transformations. Soil Biol Biochem 38:3436–3442. doi:10.1016/j.soilbio.2006.05.019

    Article  Google Scholar 

  • Stahl PD, Parkin TB (1996) Microbial production of volatile organic compounds in soil microcosms. Soil Sci Soc Am J 60:821–828

    Article  Google Scholar 

  • Stotzky G, Schenck S (1976) Volatile organic compounds and microorganisms. CRC Crit Rev 4:333–381

    Article  Google Scholar 

  • Tsuji K, Tsien HC, Hanson RS, DePalma SR, Scholtz R, LaRoche S (1990) 16S ribosomal RNA sequence analysis for determination of phylogenetic relationship among methylotrophs. J Gen Microbiol 136:1–10

    Google Scholar 

  • Vespermann A, Kai M, Piechulla B (2007) Rhizobacterial volatiles affect the growth of fungi and Arabidopsis thaliana. Appl Environ Microbiol 73:5639–5641. doi:10.1128/AEM.01078-07

    Article  Google Scholar 

  • Warneke C, Karl T, Judmaier H, Hansel A, Jordan A, Lindinger W, Crutzen PJ (1999) Acetone, methanol, and other partially oxidized volatile organic emissions from dead plant matter by abiological processes: significance for atmospheric HO x chemistry. Global Biogeochem Cycles 13:9–17

    Article  Google Scholar 

  • Wheatley R (2002) The consequences of volatile organic compound mediated bacterial and fungal interactions. Antonie van Leeuwenhoek 81:357–364. doi:10.1023/A:1020592802234

    Article  Google Scholar 

  • Wheatley RE, Millar SE, Griffiths DW (1996) The production of volatile organic compounds during nitrogen transformations in soils. Plant Soil 181:163–167. doi:10.1007/BF00011303

    Article  Google Scholar 

  • Wheatley R, Hackett C, Bruce A, Kundzewicz A (1997) Effect of substrate composition on production of volatile organic compounds from Trichoderma spp. inhibitory to wood decay fungi. Int Biodeterior Biodegradation 39:199–205

    Article  Google Scholar 

  • White CS (1988) Nitrification inhibition by monoterpenoids: theoretical mode of action based on molecular structures. Ecology 69:1631–1633. doi:10.2307/1941663

    Article  Google Scholar 

  • Zhao J, Zhang R (2004) Proton transfer reaction rate constants between hydronium ion (H3O+) and volatile organic compounds. Atmos Environ 38:2177–2185. doi:10.1016/j.atmosenv.2004.01.019

    Article  Google Scholar 

Download references

Acknowledgements

We would like to thank members of the Fierer lab for their valuable comments on previous drafts of this manuscript. We would also like to thank Mark Bradford and Mike Strickland for their help with sample collection, Rob Knight and Micah Hamady for their help with the sequence analyses, Michael Wilkinson for his guidance and aide in sampling, and Russ Monson for making the PTR-MS available for our use. Finally, we thank the three anonymous reviewers for their thoughtful comments. This work was funded by grants awarded to N.F. from the National Science Foundation and the Andrew W. Mellon Foundation.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Kelly S. Ramirez.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Ramirez, K.S., Lauber, C.L. & Fierer, N. Microbial consumption and production of volatile organic compounds at the soil-litter interface. Biogeochemistry 99, 97–107 (2010). https://doi.org/10.1007/s10533-009-9393-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10533-009-9393-x

Keywords

Navigation