Abstract
Purpose
The study of interactions between humic substances (HSs) and soil filamentous fungi is the key to understanding the sustainable soil functioning. The present work aims to examine the decomposition of HSs by filamentous dark-pigmented fungus Alternaria alternatа under the laboratory conditions and to determine the effect of easily assimilable organic carbon on this process. Analyzing such polydisperse substances like HSs by a complex integrated methodology makes it possible to explore the data on their decomposition by microorganisms.
Materials and methods
To achieve the aforementioned goals, we used chromatographic and spectroscopic approaches: low-pressure size-exclusion and hydrophobic interaction chromatography accompanied by absorption and fluorescence spectroscopy. To determine the effect cometabolism conditions produced on HS decomposition, two types of carbon substrates were added to the nutrient media: easily assimilable organic carbon (standard 0.3% or reduced 0.03% sucrose content) and hardly assimilable organic carbon (HSs), as well as their combinations. Five HS samples of different organic matter origin have been inspected: potassium humates (HPs) and humic acids (HAs) from coal, peat, and lignosulfonate. Correlation matrix and principal component analysis (PCA) were calculated for comprehensive data analysis.
Results and discussion
Transformations of the investigated HSs under fungal cultivation lead to the increase in the low molecular weight fraction, rise of hydrophilic fraction, enlargement of absorbance ratio A250/A365, shortening of the emission wavelength of the humic-type fluorescence, and growth in the fluorescence quantum yield measured with excitation at 355 nm. A positive correlation was observed between the accumulation of fungal biomass and the degree of HS decomposition. PCA analysis confirms that the difference in the results of HS decomposition largely depends on the sucrose content and the nature of HSs. We divided all the HS samples into four groups according to the degree of HS decomposition: original HS solutions, HPs altered using fungal cultivation at 0.03% sucrose, HAs after fungal cultivation at 0.03% sucrose, and finally, HSs (both HPs and HAs) after fungal cultivation at 0.3% sucrose.
Conclusions
In the laboratory experiments, we showed that (1) the isolated HAs were more effectively degraded than the parent HPs, and this process was more pronounced at a reduced sucrose content, and (2) the decomposition of stable organic compounds (HSs) was activated by the easily assimilable carbon sources (especially 0.3% sucrose) being present. We assume that it is the easily assimilable organic carbon that most likely triggers the HS degradation working as the priming effect in natural environments.
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Change history
17 January 2019
Incorrect and incomplete wording: Funding information. The study was funded by the RFBR research project no. 18–016-00078. Correct and complete wording: Funding information. The study was funded by the RFBR research projects no. 18–016-00078, 18–04-01218.
Abbreviations
- A250/A365 :
-
Absorbance ratio at 250 nm and 365 nm
- CDOM:
-
Chromophoric dissolved organic matter
- FAs:
-
Fulvic acids
- HAcoal :
-
Humic acid isolated from HPcoal
- HApeat :
-
Humic acid isolated from HPpeat
- HAs:
-
Humic acids
- HIC:
-
Hydrophobic interaction chromatography
- HPcoal :
-
Potassium humates produced from coal
- HPlingo :
-
Potassium humates produced from lignosulfonate
- HPpeat :
-
Potassium humates produced from peat
- HPs:
-
Potassium humates
- HSs:
-
Humic substances
- LPSEC:
-
Low-pressure size-exclusion chromatography
- PCA:
-
Principal component analysis
- QY355 :
-
Fluorescence quantum yield at 355 nm
- RP-HIC:
-
Reversed-phase hydrophobic interaction chromatography
References
Bingeman CW, Varner JE, Martin WP (1953) The effect of the addition of organic materials on the decomposition of an organic soil. Soil Sci Soc Am Proc 29:692–696
Boyle E, Guerriero N, Thiallet A, Del Vecchio R, Blough N (2009) Optical properties of humic substances and CDOM: relation to structure. Environ Sci Technol 43(7):2262–2268
Carzaniga R, Fiocco D, Bowyer P, O’Connell RJ (2002) Localization of melanin in conidia of Alternaria alternata using phage display antibodies. Mol Plant-Microbe Interact 15:216–224
Coble P (1996) Characterization of marine and terrestrial DOM in seawater using excitation-emission matrix spectroscopy. Mar Chem 51(4):325–346
Dang HX, Pryor B, Peever T, Lawrence CB (2015) The Alternaria genomes database: a comprehensive resource for a fungal genus comprised of saprophytes, plant pathogens, and allergenic species. BMC Genomics 16:239
Debska B, Drag M, Banach-Szott M (2007) Molecular size distribution and hydrophilic and hydrophobic properties of humic acids isolated from forest soil. Soil Water Res 2(2):45–53
Fedoseeva E, Khundzhua D, Terekhova V, Patsaeva S (2018) Use of absorption spectra and their second-order derivative to quantify degradation of lignohumate by filamentous fungi. Proc SPIE 106142B:1–7
Fichot CG, Benner R (2012) The spectral slope coefficient of chromophoric dissolved organic matter (S275-295) as a tracer of terrigenous dissolved organic carbon in river-influenced ocean margins. Limnol Oceanogr 57(5):1453–1466
Gramss G, Ziegenhagen D, Sorge S (1999) Degradation of soil humic extract by wood- and soil associated fungi, bacteria, and commercial enzymes. Microb Ecol 37:140–151
Grinhut T, Hadar Y, Chen Y (2007) Degradation and transformation of humic substances by saprotrophic fungi: processes and mechanisms. Fungal Biol Rev 21:179–189
Hardie AG, Dynes JJ, Kozak LM, Huang PM (2009) The role of glucose in abiotic humification pathways as catalyzed by birnessite. J Mol Catal A Cheml 308:114–126
Helms JR, Stubbins A, Ritchie JD, Minor EC, Kieber DJ, Mopper K (2008) Absorption spectral slopes and slope ratios as indicators of molecular weight, source, and photobleaching of chromophoric dissolved organic matter. Limnol Oceanogr 53(3):955–969
Kirk PM, Cannon PF, Minter DW, Stalpers JA (2008) Dictionary of the fungi (10th ed). CABI, Wallingford
Kudryavtsev AV, Perminova IV, Petrosyan VS (2000) Size-exclusion chromatographic descriptors of humic substances. Anal Chim Acta 407(1–2):193–202
Kuzyakov Y (2010) Priming effects: interactions between living and dead organic matter. Soil Biol Biochem 42:1363–1371
Lindahl BD, Ihrmark K, Boberg J, Trumbore SE, Hogberg P, Stenlid J, Finlay RD (2007) Spatial separation of litter decomposition and mycorrhizal nitrogen uptake in a boreal forest. New Phytol 173:611–620
McKay G, Couch KD, Mezyk SP, Rosario-Ortiz FL (2016) Investigation of the coupled effects of molecular weight and chargetransfer interactions on the optical and photochemical properties of dissolved organic matter. Environ Sci Technol 50(15):8093–8102
Milanovskii EYu (2006) Humus substances as a system of hydrophobic-hydrophilic compounds. Dissertation, Lomonosov Moscow State University
Milyukov AS, Patsaeva SV, Yuzhakov VI, Gorshkova OM, Prashchikina EM (2007) Fluorescence of nanoparticles of organic matter dissolved in natural water. Mosc Univ Phys Bull 62(6):368–372
Moliszewska E, Pisarek I (1996) Influence of humic substances on the growth of two phytopathogenic soil fungi. Environ Int 22(5):579–584
Osterman LA (1985) Chromatography of proteins and nucleic acids, Russia, Moscow
Patsaeva S, Khundzhua D, Trubetskoj OA, Trubetskaya OE (2018) Excitation-dependent fluorescence quantum yield for freshwater chromophoric dissolved organic matter from northern Russian lakes. J Spectroscopy 3168320:3168320–1–3168320–7
Patsayeva S, Reuter R (1995) Spectroscopic study of major components of dissolved organic matter naturally occurring in water. Proc SPIE 2586:151–160
Perminova IV, Frimmel FH, Kudryavtsev AV, Kulikova NA, Abbt-Braun G, Hesse S, Petrosyan VS (2003) Molecular weight characteristics of humic substances from different environments as determined by size exclusion chromatography and their statistical evaluation. Environ Sci Technol 37(11):2477–2485
Rezacova V, Hrselova H, Gryndlerova H, Miksik I, Gryndler M (2006) Modifications of degradation-resistant soil organic matter by soil saprobic microfungi. Soil Biol Biochem 38:2292–2299
Shubina D, Fedoseeva E, Gorshkova O, Patsaeva S, Terekhova V, Timofeev M, Yuzhakov V (2010) The “blue shift” of emission maximum and the fluorescence quantum yield as quantitative spectral characteristics of dissolved humic substances. EARSeL eProceedings 9(1):13–21
Silva-Stenico ME, Vengadajellum CJ, Janjua HA, Harrison STL, Burton SG, Cowan DA (2007) Degradation of low rank coal by Trichoderma atroviride ES11. J Ind Microbiol Biotechnol 34(9):625–631
Stepanov AA (2005) Structural features of amphiphilic humic acid fractions from a southern chernozem. Eurasian Soil Sci 38(8):843–847
Stepanov AA (2008) Separation and characterization of amphiphilic humic acid fractions. Mosc Univ Soil Sci Bull 63(3):125–129
Tikhonov VV, Yakushev AV, Zavgorodnyaya YA, Bam B, Demin VV (2010) Effects of humic acids on the growth of bacteria. Eurasian Soil Sci 43(3):305–313
Trubetskoj OA, Richard C, Voyard G, Marchenkov VV, Trubetskaya OE (2018) Molecular size distribution of fluorophores in aquatic natural organic matter: application of HPSEC with multi-wavelength absorption and fluorescence detection following LPSEC-PAGE fractionation. Environ Sci Technol 52(9):5287–5295
Valmaseda M, Martinez AT, Almendros D (1989) Contribution by pigmented fungi to P-type humic acid formation in two forest soils. Soil Biol Biochem 21:23–28
Wünsch U, Murphy KR, Stedmon C (2015) Fluorescence quantum yields of natural organic matter and organic compounds: implications for the fluorescence-based interpretation of organic matter composition. Front Mar Sci 2:98
Wünsch UJ, Stedmon CA, Tranvik LJ, Guillemette F (2018) Unraveling the size-dependent optical properties of dissolved organic matter. Limnol Oceanogr 63:588–601
Yakimenko OS, Terekhova VA (2011) Humic preparations and the assessment of their biological activity for certification purposes. Eurasian Soil Sci 44(11):1222–1230
Yakimenko O, Khundzhua DA, Izosimov A, Yuzhakov V, Patsaeva S (2018) Source indicator of commercial humic products: UV-Vis and fluorescence proxies. J Soils Sediments 18(4):1279–1291
Zavarzina AG, Demin VV, Nifant’eva TI, Shkinev VM, Danilova TV, Spivakov BY (2002) Extraction of humic acids and their fractions in polyethylene glycol-based aqueous biphasic systems. Anal Chim Acta 452(1):95–103
Zavarzina AG, Vanifatova NG, Stepanov AA (2008) Fractionation of humic acids according to their hydrophobicity, size, and charge-dependent mobility by the salting-out method. Eurasian Soil Sci 41(12):1294–1301
Zavarzina AG, Lisov AA, Zavarzin AA, Leontievsky AA (2011) Fungal oxidoreductases and humification in forest soils. In: Shukla G, Varma A (eds) Soil enzymology, (Vol. 22 of Soil Biology), pp 207–229
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The study was funded by the RFBR research project no. 18-016-00078.
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Fedoseeva, E., Stepanov, A., Yakimenko, O. et al. Biodegradation of humic substances by microscopic filamentous fungi: chromatographic and spectroscopic proxies. J Soils Sediments 19, 2676–2687 (2019). https://doi.org/10.1007/s11368-018-2209-7
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DOI: https://doi.org/10.1007/s11368-018-2209-7