Abstract
The regulatory gate hypothesis considers that soil organic C mineralization is a two-step process, where stable C is firstly transformed abiotically and is only then a microbially available substrate. The mechanisms involved in the abiotic conversion of non-microbially available to available soil organic C remain largely unknown. We conducted a perfusion experiment using a repeated fumigated-incubated soil and the corresponding fresh soil. We found that repeated fumigation-incubation significantly decreased soil microbial ATP to 0.22 nmol g−1 soil, 10% of that in the fresh soil, and significantly destroyed microbial composition and diversity. However, it had little influence on the soil CO2-C evolution rate after the flush of fumigant-killed dead biomass (8 μg CO2-C g−1 soil day−1) or dissolved organic C (DOC) concentration (about 7 μg C g−1 soil) and composition during long-term perfusion. We conclude that soil CO2 evolution rate and DOC generation were not regulated by the size or composition of the soil microbial communities. This is in support of the regulatory gate hypothesis. We suggest that abiotic processes in soil organic C mineralization need to be considered more and studied further.
Similar content being viewed by others
Change history
04 March 2020
The original version of this article was published with open access. With the author(s)’ decision to step back from Open Choice, the copyright of the article changed on 04 March 2020 to © Springer-Verlag GmbH Germany, part of Springer Nature 2020 and the article is forthwith distributed under the terms of copyright.
References
Ahmed I, Yokota A, Yamazoe A, Fujiwara T (2007) Proposal of Lysinibacillus boronitolerans gen. nov. sp. nov., and transfer of Bacillus fusiformis to Lysinibacillus fusiformis comb. nov. and Bacillus sphaericus to Lysinibacillus sphaericus comb. nov. Int J Syst Evol Microbiol 57:1117–1125. https://doi.org/10.1099/ijs.0.63867-0
Ben Salah I, Drancourt M (2010) Surviving within the amoebal exocyst: the Mycobacterium avium complex paradigm. BMC Microbiol 10:99–99. https://doi.org/10.1186/1471-2180-10-99
Bengtson P, Bengtsson G (2007) Rapid turnover of DOC in temperate forests accounts for increased CO2 production at elevated temperatures. Ecol Lett 10:783–790. https://doi.org/10.1111/j.1461-0248.2007.01072.x
Bolger AM, Lohse M, Usadel B (2014) Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30:2114–2120. https://doi.org/10.1093/bioinformatics/btu170
Brookes PC, YanFeng C, Lin C, Gaoyang Q, Yu L, Jianming X (2017) Is the rate of mineralization of soil organic carbon under microbiological control? Soil Biol Biochem 112:127–139. https://doi.org/10.1016/j.soilbio.2017.05.003
Burns RG (1978) Enzyme activity in soil: some theoretical and practical considerations. In: Burns RG (ed) Soil enzymes. Academic Press, London, pp 295–340
Chen L, Xu J, Feng Y, Wang J, Yu Y, Brookes PC (2015) Responses of soil microeukaryotic communities to short-term fumigation-incubation revealed by MiSeq amplicon sequencing. Front Microbiol 6:1–13. https://doi.org/10.3389/fmicb.2015.01149
Chen L, Luo Y, Xu J, Yu Z, Zhang K, Brookes PC (2016) Assessment of bacterial communities and predictive functional profiling in soils subjected to short-term fumigation-incubation. Soil Microbiol 72:240–251. https://doi.org/10.1007/s00248-016-0766-0
Cressey E, Hill P, Farrar J, Jones D (2007) Fast turnover of low molecular weight components of the dissolved organic carbon pool of temperate grassland field soils. Soil Biol Biochem 39(825–835):827–835. https://doi.org/10.1016/j.soilbio.2006.09.030
Diaz-Raviña M, Prieto A, Acea MJ, Carballas T (1992) Fumigation-extraction method to estimate microbial biomass in heated soils. Soil Biol Biochem 24:259–264. https://doi.org/10.1016/0038-0717(92)90227-O
Dungait J, Hopkins D, Gregory AS, Whitemore AP (2012) Soil organic matter turnover is governed by accessibility not recalcitrance. Glob Chang Biol 18:1781–1796. https://doi.org/10.1111/j.1365-2486.2012.02665.x
Edgar RC, Haas BJ, Clemente JC, Quince C, Knight R (2011) UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27:2194–2200. https://doi.org/10.1093/bioinformatics/btr381
Foster RC (1988) Microenvironments of soil microorganisms. Biol Fertil Soils 6:189–203. https://doi.org/10.1007/BF00260816
Glaeser SP, Dott W, Busse HJ, Kӓmpfer P (2013) Fictibacillus phosphorivorans gen. nov., sp. nov. and proposal to reclassify Bacillus arsenicus, Bacillus barbaricus, Bacillus macauensis, Bacillus nanhaiensis, Bacillus rigui, Bacillus solisalsi and Bacillus gelatini in the genus Fictibacillus. Int J Syst Evol Microbiol 63:2934–2944. https://doi.org/10.1099/ijs.0.049171-0
Guigue J, Harir M, Mathieu O, Lucio M, Ranjard L, Lévêque J, Schmitt-Kopplin P (2016) Ultrahigh-resolution FT-ICR mass spectrometry for molecular characterisation of pressurised hot water-extractable organic matter in soils. Biogeochemistry 128:307–326. https://doi.org/10.1007/s10533-016-0209-5
Haberhauer G, Gerzabek MH (1999) Drift and transmission FT-IR spectroscopy of forest soils: an approach to determine decomposition processes of forest litter. Vib Spectrosc 19:413–417. https://doi.org/10.1016/S0924-2031(98)00046-0
Jenkinson DS, Oades JM (1979) A method for measuring adenosine triphosphate in soil. Soil Biol Biochem 11:193–199. https://doi.org/10.1016/0038-0717(79)90100-7
Jenkinson DS, Powlson DS (1976) Effects of biocidal treatments on metabolism in soil. 5. Method for measuring soil biomass. Soil Biol Biochem 8:209–213. https://doi.org/10.1016/0038-0717(76)90005-5
Juarez S, Nunan N, Duday AC, Pouteau V, Chenu C (2013) Soil carbon mineralisation responses to alterations of microbial diversity and soil structure. Biol Fertil Soils 49:939–948. https://doi.org/10.1007/s00374-013-0784-8
Kaiser K, Kalbitz K (2012) Cycling downwards – dissolved organic matter in soils. Soil Biol Biochem 52:29–32. https://doi.org/10.1016/j.soilbio.2012.04.002
Keith FC (1984) Morphological and physiological differentiation in Streptomyces. In: Losick R, Shapiro L (eds) Microbial Development. Cold Spring Harbor, New York, pp 89–115. https://doi.org/10.1101/087969172.16.89
Kemmitt SJ, Lanyon CV, Waite IS, Wen Q, Addiscott TM, Bird NRA, O'Donnell AG, Brookes PC (2008) Mineralization of native soil organic matter is not regulated by the size, activity or composition of the soil microbial biomass - a new perspective. Soil Biol Biochem 40:61–73. https://doi.org/10.1016/j.soilbio.2007.06.021
Kindler R, Siemens J, Kaiser K, Walmsley DC, Bernhofer C, Buchmann N, Cellier P, Eugster W, Gleixner G, Grunwald T, Heim A, Ibrom A, Jones SK, Jones M, Klumpp K, Kutsch W, Larsen KS, Lehuger S, Loubet B, McKenzie R, Moors E, Osborne B, Pilegaard K, Rebmann C, Saunders M, Schmidt MWI, Schrumpf M, Seyfferth J, Skiba U, Soussana JF, Sutton MA, Tefs C, Vowinckel B, Zeeman MJ, Kaupenjohann M (2011) Dissolved carbon leaching from soil is a crucial component of the net ecosystem carbon balance. Glob Chang Biol 17:1167–1185. https://doi.org/10.1111/j.1365-2486.2010.02282.x
Knight TR, Dick RP (2004) Differentiating microbial and stabilized β-glucosidase activity relative to soil quality. Soil Biol Biochem 36:2089–2096. https://doi.org/10.1016/j.soilbio.2004.06.007
Kroppenstedt RM, Mayilraj S, Wink JM, Kallow W, Schumann P, Secondini C, Stackebrandt E (2005) Eight new species of the genus Micromonospora, Micromonospora citrea sp. nov., Micromonospora echinaurantiaca sp. nov., Micromonospora echinofusca sp. nov. Micromonospora fulviviridis sp. nov., Micromonospora inyonensis sp. nov., Micromonospora peucetia sp. nov., Micromonospora sagamiensis sp. nov., and Micromonospora viridifaciens sp. nov. Syst Appl Microbiol 28:328–339. https://doi.org/10.1016/j.syapm.2004.12.011
Kuzyakov Y, Blagodatskaya E, Blagodatsky S (2009) Comments on the paper by Kemmitt et al. (2008) ‘mineralization of native soil organic matter is not regulated by the size, activity or composition of the soil microbial biomass – a new perspective’ [Soil Biology & Biochemistry 40, 61–73]: the biology of the regulatory gate. Soil Biol Biochem 41:435–439. https://doi.org/10.1016/j.soilbio.2008.07.023
Magoc T, Salzberg SL (2011) FLASH: fast length adjustment of short reads to improve genome assemblies. Bioinformatics 27:2957–2963. https://doi.org/10.1093/bioinformatics/btr507
Margon A, Fornasier F (2008) Determining soil enzyme location and related kinetics using rapid fumigation and high-yield extraction. Soil Biol Biochem 40:2178–2181. https://doi.org/10.1016/j.soilbio.2008.02.006
Mendoza CA, Bello-López JM, Navarro-Noya YE, León-Lorenzana ASd, Delgado-Balbuena L, Gómez-Acata S, Ruíz-Valdiviezo VM, Ramirez-Villanueva DA, Luna-Guido M, Dendooven L (2014) Bacterial community structure in fumigated soil. Soil Biol Biochem 73:122–129. https://doi.org/10.1016/j.soilbio.2014.02.012
Miltner A, Bombach P, Schmidt-brücken B, Kästner M (2012) SOM genesis: microbial biomass as a significant source. Biogeochemistry 111:41–55. https://doi.org/10.1007/s10533-011-9658-z
Nannipieri P (2006) Role of stabilised enzymes in microbial ecology and enzyme extraction from soil with potential applications in soil proteomics. In: Nannipieri P, Smalla K (eds) Nucleic acids and proteins in soil. Springer, Berlin Heidelberg, pp 75–94. https://doi.org/10.1007/3-540-29449-X_4
Nannipieri P, Giagnoni L, Landi L, Renella G (2011) Role of phosphatase enzymes in soil. In: Bünemann E, Oberson A, Frossard E (eds) Phosphorus in action. Soil biology, vol 26. Springer, Berlin, Heidelberg, pp 215–243. https://doi.org/10.1007/978-3-642-15271-9_9
Nannipieri P, Trasar-Cepeda C, Dick RP (2018) Soil enzyme activity: a brief history and biochemistry as a basis for appropriate interpretations and meta-analysis. Biol Fertil Soils 54:11–19. https://doi.org/10.1007/s00374-017-1245-6
Neff JC, Asner GP (2001) Dissolved organic carbon in terrestrial ecosystems: synthesis and a model. Ecosyetems 4:29–48. https://doi.org/10.1007/s100210000058
Qiu GY, Chen YF, Luo Y, Xu JM, Brookes PC (2016) The microbial ATP concentration in aerobic and anaerobic Chinese soils. Soil Biol Biochem 92:38–40. https://doi.org/10.1016/j.soilbio.2015.09.009
Renella G, Landi L, Nannipieri P (2002) Hydrolase activities during and after the chloroform fumigation affected by protease activity. Soil Biol Biochem 34:51–60. https://doi.org/10.1016/S0038-0717(01)00152-3
Ridge EH (1976) Studies on soil fumigation - II: Effects on bacteria. Soil Biol Bioch 8:249–253. https://doi.org/10.1016/0038-0717(76)90052-3
Setia R, Verma SL, Marschner P (2012) Measuring microbial biomass carbon by direct extraction - comparison with chloroform fumigation-extraction. Eur J Soil Biol 53:103–106. https://doi.org/10.1016/j.ejsobi.2012.09.005
Sollins P, Homann P, Caldwell B (1996) Stabilization and destabilization of soil organic matter: mechanisms and controls. Geoderma 74:65–105. https://doi.org/10.1016/S0016-7061(96)00036-5
Swenson TL, Jenkins S, Bowen BP, Northen TR (2015) Untargeted soil metabolomics methods for analysis of extractable organic matter. Soil Biol Biochem 80:189–198. https://doi.org/10.1016/j.soilbio.2014.10.007
Tabatabai MA (1994) Soil enzymes. In: Bottomley PS, Angle JS, Weaver RW (eds) Methods of soil analysis: part 2-microbiological and biochemical properties. Soil Science Society of America, Madison, WI, pp 775–833. https://doi.org/10.2136/sssabookser5.2.c37
Toosi ER, Doane TA, Horwath WR (2012) Abiotic solubilization of soil organic matter, a less-seen aspect of dissolved organic matter production. Soil Biol Biochem 50:12–21. https://doi.org/10.1016/j.soilbio.2012.02.033
Toosi ER, Schmidt JP, Castellano MJ (2014) Soil temperature is an important regulatory control on dissolved organic carbon supply and uptake of soil solution nitrate. Eur J Soil Biol 61:68–71. https://doi.org/10.1016/j.ejsobi.2014.01.003
Toyota K, Ritz K, Young IM (1996) Survival of bacterial and fungal populations following chloroform-fumigation: effects of soil matric potential and bulk density. Soil Biol Biochem 28:1545–1547. https://doi.org/10.1016/S0038-0717(96)00162-9
Ultee E, Ramijan K, Dame RT, Briegel A, Claessen D (2019) Chapter two - stress-induced adaptive morphogenesis in bacteria. In: Poole RK (ed) Advances in microbial physiology. Academic Press, Sheffield, pp 97–141. https://doi.org/10.1016/bs.ampbs.2019.02.001
Van Hees PAW, Jones DL, Finlay R, Godbold DL, Lundström US (2005) The carbon we do not see - the impact of low molecular weight compounds on carbon dynamics and respiration in forest soils: a review. Soil Biol Biochem 37:1–13. https://doi.org/10.1016/j.soilbio.2004.06.010
Vance EC, Brookes PS, Jenkinson D (1987) An extraction method for measuring soil microbial biomass C. Soil Biol Biochem 19:703–707. https://doi.org/10.1016/0038-0717(87)90052-6
Von Lützow M, Kögel-Knabner I, Ekschmitt K, Flessa H, Guggenberger G, Matzner E, Marschner B (2007) SOM fractionation methods: relevance to functional pools and to stabilization mechanisms. Soil Biol Biochem 39:2183–2207. https://doi.org/10.1016/j.soilbio.2007.03.007
Wagner JK, Brun YV (2007) Out on a limb: how the Caulobacter stalk can boost the study of bacterial cell shape. Mol Microbiol 64:28–33. https://doi.org/10.1111/j.1365-2958.2007.05633.x
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. https://doi.org/10.1016/j.scitotenv.2016.04.201
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
Xu N, Tan G, Wang H, Gai X (2016) Effect of biochar additions to soil on nitrogen leaching, microbial biomass and bacterial community structure. Eur J Soil Biol 74:1–8. https://doi.org/10.1016/j.ejsobi.2016.02.004
Zhou Z, Cao X, Schmidt-Rohr K, Olk DC, Zhuang S, Zhou J, Cao Z, Mao J (2014) Similarities in chemical composition of soil organic matter across a millennia-old paddy soil chronosequence as revealed by advanced solid-state NMR spectroscopy. Biol Fertil Soils 50:571–581. https://doi.org/10.1007/s00374-013-0875-6
Acknowledgments
We thank Msc Yanfeng Chen, Professor David Powlson, Rothamsted Research, for helpful discussion.
Funding
This work was supported by the National Natural Science Foundation of China (41671233, 41721001, 41807017, 41671237). P. C. Brookes received funding under The Chinese Government 1000 Talents Program.
Author information
Authors and Affiliations
Corresponding author
Additional information
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
The original version of this article was revised: The original version of this article was published with open access. With the author(s)’ decision to step back from Open Choice, the copyright of the article changed on 04 March 2020 to © Springer-Verlag GmbH Germany, part of Springer Nature 2020 and the article is forthwith distributed under the terms of copyright.
Electronic supplementary material
ESM 1
(DOCX 2589 kb)
Rights and permissions
About this article
Cite this article
Zhou, X., Chen, L., Xu, J. et al. Soil biochemical properties and bacteria community in a repeatedly fumigated-incubated soil. Biol Fertil Soils 56, 619–631 (2020). https://doi.org/10.1007/s00374-020-01437-0
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00374-020-01437-0