Succession of bacterial and fungal 4-chloro-2-methylphenoxyacetic acid degraders at the soil–litter interface
Corresponding Author
Franziska Ditterich
Institute of Soil Science and Land Evaluation, Soil Biology Section, University of Hohenheim, Stuttgart, Germany
Correspondence: Franziska Ditterich, Institute of Soil Science and Land Evaluation, Soil Biology Section, University of Hohenheim, Emil Wolff-Straße 27, 70599 Stuttgart, Germany. Tel.: +49 0711 459 24252; fax: +49 0711 459 23117; e-mail: [email protected]Search for more papers by this authorChristian Poll
Institute of Soil Science and Land Evaluation, Soil Biology Section, University of Hohenheim, Stuttgart, Germany
Search for more papers by this authorHolger Pagel
Institute of Soil Science and Land Evaluation, Biogeophysics Section, University of Hohenheim, Stuttgart, Germany
Search for more papers by this authorDoreen Babin
Julius Kühn-Institut, Federal Research Centre for Cultivated Plants, Institute for Epidemiology and Pathogen Diagnostics, Braunschweig, Germany
Search for more papers by this authorKornelia Smalla
Julius Kühn-Institut, Federal Research Centre for Cultivated Plants, Institute for Epidemiology and Pathogen Diagnostics, Braunschweig, Germany
Search for more papers by this authorMarcus A. Horn
Department of Ecological Microbiology, University of Bayreuth, Bayreuth, Germany
Search for more papers by this authorThilo Streck
Institute of Soil Science and Land Evaluation, Biogeophysics Section, University of Hohenheim, Stuttgart, Germany
Search for more papers by this authorEllen Kandeler
Institute of Soil Science and Land Evaluation, Soil Biology Section, University of Hohenheim, Stuttgart, Germany
Search for more papers by this authorCorresponding Author
Franziska Ditterich
Institute of Soil Science and Land Evaluation, Soil Biology Section, University of Hohenheim, Stuttgart, Germany
Correspondence: Franziska Ditterich, Institute of Soil Science and Land Evaluation, Soil Biology Section, University of Hohenheim, Emil Wolff-Straße 27, 70599 Stuttgart, Germany. Tel.: +49 0711 459 24252; fax: +49 0711 459 23117; e-mail: [email protected]Search for more papers by this authorChristian Poll
Institute of Soil Science and Land Evaluation, Soil Biology Section, University of Hohenheim, Stuttgart, Germany
Search for more papers by this authorHolger Pagel
Institute of Soil Science and Land Evaluation, Biogeophysics Section, University of Hohenheim, Stuttgart, Germany
Search for more papers by this authorDoreen Babin
Julius Kühn-Institut, Federal Research Centre for Cultivated Plants, Institute for Epidemiology and Pathogen Diagnostics, Braunschweig, Germany
Search for more papers by this authorKornelia Smalla
Julius Kühn-Institut, Federal Research Centre for Cultivated Plants, Institute for Epidemiology and Pathogen Diagnostics, Braunschweig, Germany
Search for more papers by this authorMarcus A. Horn
Department of Ecological Microbiology, University of Bayreuth, Bayreuth, Germany
Search for more papers by this authorThilo Streck
Institute of Soil Science and Land Evaluation, Biogeophysics Section, University of Hohenheim, Stuttgart, Germany
Search for more papers by this authorEllen Kandeler
Institute of Soil Science and Land Evaluation, Soil Biology Section, University of Hohenheim, Stuttgart, Germany
Search for more papers by this authorAbstract
Phenoxyacetic acids can be degraded by diverse soil microorganisms. Nevertheless, we miss information about the succession of 4-chloro-2-methylphenoxyacetic acid (MCPA) degraders in micro-environments of soils as well as specific functions of different microbial groups during MCPA degradation. We studied MCPA degradation at the soil–litter interface in a microcosm experiment and followed the succession of different degrader populations by quantifying the abundance of 16S rRNA genes as well as, the fungal ITS fragment and the functional genes tfdA (in total and divided into three classes) and cadA. Adjacent to the litter layer, a dynamic depletion zone of MCPA indicated that the litter effect on MCPA degradation depends on substrate availability and the affected soil volume. The increase of the tfdA class III and cadA genes was linked to MCPA mineralisation. Total abundance of tfdA genes was dominated by class I MCPA degraders and did not reflect MCPA degradation potential of the soil. Litter addition induced the development of pioneer and late-stage fungal communities, which were probably both involved in MCPA degradation. The results underline the importance of the ecological behaviour of different degrader populations for the understanding of herbicide degradation in soils.
Supporting Information
Filename | Description |
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fem12131-sup-0001-TableS1.docWord document, 135.5 KB | Table S1. Mean and standard deviation (SD) of measured gene abundances in treatments without litter addition at different sampling dates. |
fem12131-sup-0002-TableS2.docWord document, 136 KB | Table S2. Mean and standard deviation (SD) of measured gene abundances in treatments with litter addition at different sampling dates. |
Please note: The publisher is not responsible for the content or functionality of any supporting information supplied by the authors. Any queries (other than missing content) should be directed to the corresponding author for the article.
References
- Anderson IC & Cairney JWG (2004) Diversity and ecology of soil fungal communities: increased understanding through the application of molecular techniques. Environ Microbiol 6: 769–779.
- Bælum J & Jacobsen CS (2009) TaqMan probe-based real-time PCR assay for detection and discrimination of class I, II, and III tfdA genes in soils treated with phenoxy acid herbicides. Appl Environ Microbiol 75: 2969–2972.
- Bælum J, Henriksen T, Hansen HCB & Jacobsen CS (2006) Degradation of 4-chloro-2-methylphenoxyacetic acid in top and sub-soil is quantitatively linked to the class III tfdA gene. Appl Environ Microbiol 72: 1476–1486.
- Bælum J, Nicolaisen MH, Holben WE, Strobel BW, Sorensen J & Jacobsen CS (2008) Direct analysis of tfdA gene expression by indigenous bacteria in phenoxy acid amended agricultural soil. ISME J 2: 677–687.
- Bælum J, Jacobsen CS & Holben WE (2010) Comparison of 16S rRNA gene phylogeny and functional tfdA gene distribution in thirty-one different 2,4-dichlorophenoxyacetic acid and 4-chloro-2-methylphenoxyacetic acid degraders. Syst Appl Microbiol 33: 67–70.
- Batıoğlu-Pazarbaşı M, Bælum J, Johnsen AR, Sørensen SR, Albrechtsen HJ & Aamand J (2012) Centimetre-scale vertical variability of phenoxy acid herbicide mineralization potential in aquifer sediment relates to the abundance of tfdA genes. FEMS Microbiol Ecol 80: 331–341.
- Beadle CA & Smith ARW (1982) The purification and properties of 2,4-dichlorophenol hydroxylase from a strain of Acinetobacter species. Eur J Biochem 123: 323–332.
- Castillo MDP, Andersson A, Ander P, Stenström J & Torstensson L (2001) Establishment of the white rot fungus Phanerochaete chrysosporium on unsterile straw in solid substrate fermentation systems intended for degradation of pesticides. World J Microbiol Biotechnol 17: 627–633.
- Cederlund H, Börjesson E, Önneby K & Stenström J (2007) Metabolic and cometabolic degradation of herbicides in the fine material of railway ballast. Soil Biol Biochem 39: 473–484.
- Danganan CE, Ye RW, Daubaras DL, Xun L & Chakrabarty AM (1994) Nucleotide sequence and functional analysis of the genes encoding 2,4,5-trichlorophenoxyacetic acid oxygenase in Pseudomonas cepacia AC1100. Appl Environ Microbiol 60: 4100–4106.
- Don RH & Pemberton JM (1981) Properties of six pesticide degradation plasmids isolated from Alcaligenes paradoxus and Alcaligenes eutrophus. J Bacteriol 145: 681–686.
- Don RH, Weightman AJ, Knackmuss HJ & Timmis KN (1985) Transposon mutagenesis and cloning analysis of the pathways for degradation of 2,4-dichlorophenoxyacetic acid and 3-chlorobenzoate in Alcaligenes eutrophus JMP134(pJP4). J Bacteriol 161: 85–90.
- Duah-Yentumi S & Kuwatsuka S (1980) Effect of organic matter and chemical fertilizers on the degradation of benthiocarb and MCPA herbicides in the soil. Soil Sci Plant Nutr 26: 541–549.
- Duah-Yentumi S & Kuwatsuka S (1982) Microbial degradation of benthiocarb, MCPA and 2,4-D herbicides in perfused soils amended with organic matter and chemical fertilizers. Soil Sci Plant Nutr 28: 19–26.
- Fierer N, Jackson JA, Vilgalys R & Jackson RB (2005) Assessment of soil microbial community structure by use of taxon-specific quantitative PCR Assays. Appl Environ Microbiol 71: 4117–4120.
- Fredslund L, Vinther FP, Brinch UC, Elsgaard L, Rosenberg P & Jacobsen CS (2008) Spatial variation in 2-methyl-4-chlorophenoxyacetic acid mineralization and sorption in a sandy soil at field level. J Environ Qual 37: 1918–1928.
- Fukumori F & Hausinger RP (1993) Alcaligenes eutrophus JMP134 “2,4-dichlorophenoxyacetate monooxygenase” is an α-ketoglutarate-dependent dioxygenase. J Bacteriol 175: 2083–2086.
- Fulthorpe RR, McGowan C, Maltseva OV, Holben WE & Tiedje JM (1995) 2,4-Dichlorophenoxyacetic acid-degrading bacteria contain mosaics of catabolic genes. Appl Environ Microbiol 61: 3274–3281.
- Gonod VL, Martin-Laurent M & Chenu C (2006) 2,4-Dimpacton bacterial communities, and the activity and genetic potential of 2,4-D degrading communities in soil. FEMS Microbiol Ecol 58: 529–537.
- Greer LE & Shelton DR (1992) Effect of inoculant strain and organic matter content on kinetics of 2,4-dichlorophenoxyacetic acid degradation in soil. Appl Environ Microbiol 61: 1459–1465.
- Heuer H, Wieland G, Schönfeld J, Schönwälder A, Gomes NCM & Smalla K (2001) Bacterial community profiling using DGGE or TGGE analysis. Environmental Molecular Microbiology: Protocols and Applications ( PA Rochelle, ed), pp. 177–190. Horizon Scientific Press, Wymondham, UK.
- Hotopp JC & Hausinger RP (2001) Alternative substrates of 2,4-dichlorophenoxyacetate/α-ketoglutarate dioxygenase. J Mol Catal B Enzym 15: 155–162.
- Ingwersen J, Poll C, Streck T & Kandeler E (2008) Micro-scale modelling of carbon turnover driven by microbial succession at a biogeochemical interface. Soil Biol Biochem 40: 864–878.
- Itoh K, Kanda R, Sumita Y, Kim H, Kamagata Y, Suyama K, Yamamoto H, Hausinger RP & Tiedje JM (2002) tfdA-like genes in 2,4-dichlorophenoxyacetic acid-degrading bacteria belonging to the Bradyrhizobium-Agromonas-Nitrobacter-Afipia cluster in α-Proteobacteria. Appl Environ Microbiol 68: 3449–3454.
- Itoh K, Tashiro Y, Uobe K, Kamagata Y, Suyama K & Yamamoto H (2004) Root nodule Bradyrhizobium spp. harbor tfdAα and cadA, homologous with genes encoding 2,4-dichlorophenoxyacetic acid degrading proteins. Appl Environ Microbiol 70: 2110–2118.
- Ka JO, Holben WE & Tiedje JM (1994) Genetic and phenotypic diversity of 2,4- dichlorophenoxyacetic acid (2,4-D)-degrading bacteria isolated from 2,4-D treated field soils. Appl Environ Microbiol 60: 1106–1115.
- Kamagata Y, Fulthorpe R, Tamura K, Takami H, Forney LJ & Tiedje JM (1997) Pristine environments harbor a new group of oligotrophic 2,4-dichlorophenoxyacetic acid-degrading bacteria. Appl Environ Microbiol 63: 2266–2272.
- Kitagawa W, Takami S, Miyauchi K, Masai E, Kamagata Y, Tiedje JM & Fukuda M (2002) Novel 2,4- dichlorophenoxyacetic acid degradation genes from oligotrophic Bradyrhizobium sp. strain HW13 isolated from a pristine environment. J Bacteriol 184: 509–518.
- Lerch TZ, Dignac MF, Nunan N, Bardoux G, Barriuso E & Mariotti A (2009) Dynamics of soil microbial populations involved in 2,4-D biodegradation revealed by FAME-based stable isotope probing. Soil Biol Biochem 41: 77–85.
- Liu YJ, Zaprasis A, Liu SJ, Drake HL & Horn MA (2011a) The earthworm Aporrectodea caliginosa stimulates abundance and activity of phenoxyalkanoic acid herbicide degraders. ISME J 5: 473–485.
- Liu YJ, Liu SJ, Drake HL & Horn MA (2011b) Alphaproteobacteria dominate active 2-methyl-4-chlorophenoxyacetic acid herbicide degraders in agricultural soil and drilosphere. Environ Microbiol 13: 991–1009.
- López-Gutiérrez JC, Henry S, Hallet S, Martin-Laurent F, Catroux G & Philippot L (2004) Quantification of a novel group of nitrate-reducing bacteria in the environment by real-time PCR. J Microbiol Methods 57: 399–407.
- Manerkar MA, Seen S & Bärlocher F (2008) Q-RT-PCR for assessing archaea, bacteria, and fungi during leaf decomposition in a stream. Microb Ecol 56: 467–473.
- McGowan C, Fulthorpe R, Wright A & Tiedje JM (1998) Evidence for interspecies gene transfer in the evolution of 2,4-dichlorophenoxyacetic acid degraders. Appl Environ Microbiol 64: 4089–4092.
- Moret S, Hidalgo M & Sánchez JM (2006) Development of an ion-pairing liquid chromatography method for the determination of phenoxyacetic herbicides and their main metabolites: application to the analysis of soil samples. Chromatographia 63: 109–115.
- Mortensen SK & Jacobsen CS (2004) Influence of frozen storage on herbicide degradation capacity in surface and subsurface sandy soils. Environ Sci Technol 38: 6625–6632.
- Müller RH & Babel W (2000) A theoretical study on the metabolic requirements resulting from a-ketoglutarate-dependent cleavage of phenoxyalkanoates. Appl Environ Microbiol 66: 339–344.
- Müller RH & Babel W (2001) Pseudo-recalcitrance of chlorophenoxyalkanoate herbicides – correlation to the availability of α-ketoglutarate. Acta Biotechnol 21: 227–242.
- Nielsen MS, Bælum J, Jensen MB & Jacobsen CS (2011) Mineralization of the herbicide MCPA in urban soils is linked to presence and growth of class III tfdA genes. Soil Biol Biochem 43: 984–990.
- Nikolcheva LG, Bourque T & Bärlocher F (2005) Fungal diversity during initial stages of leaf decomposition in a stream. Mycol Res 109: 246–253.
- Pagel H, Ingwersen J, Poll C, Kandeler E & Streck T (2013) Micro-scale modeling of pesticide degradation coupled to carbon turnover in the detritusphere - model description and sensitivity analysis. Biogeochemistry: doi: 10.1007/s10533-013-9851-3.
- Poll C, Ingwersen J, Stemmer M, Gerzabek MH & Kandeler E (2006) Mechanisms of solute transport affect small-scale abundance and function of soil microorganisms in the detritusphere. Eur J Soil Sci 57: 583–595.
- Poll C, Marhan S, Ingwersen J & Kandeler E (2008) Dynamics of litter carbon turnover and microbial abundance in a rye detritusphere. Soil Biol Biochem 40: 1306–1321.
- Poll C, Pagel H, Devers-Lamrani M, Martin-Laurent F, Ingwersen J, Streck T & Kandeler E (2010a) Regulation of bacterial and fungal MCPA degradation at the soil-litter interface. Soil Biol Biochem 42: 1879–1887.
- Poll C, Brune T, Begerow D & Kandeler E (2010b) Small-scale diversity and succession of fungi in the detritusphere of rye residues. Microb Ecol 59: 130–140.
- Reddy GVB, Joshi DK & Gold MH (1997) Degradation of chlorophenoxyacetic acids by the lignin-degrading fungus Dichomitus squalens. Microbiology 43: 2353–2360.
10.1099/00221287-143-7-2353 Google Scholar
- Rodriguez-Cruz MS, Bælum J, Shawc LJ, Sørensen SR, Shi S, Aspray T, Jacobsen CS & Bending GD (2010) Biodegradation of the herbicide mecoprop-p with soil depth and its relationship with class III tfdA genes. Soil Biol Biochem 42: 32–39.
- Shailubhai K, Sahasrabudhe SR, Vora KA & Modi VV (1983) Degradation of chlorinated derivatives of phenoxyacetic acid and benzoic acid by Aspergillus niger. FEMS Microbiol Lett 18: 279–282.
- Shishido M & Chanway CP (1998) Storage effects on indigenous soil microbial communities and PGPR efficacy. Soil Biol Biochem 30: 939–947.
- Streber WR, Timmis KN & Zenk MH (1987) Analysis, cloning, and high-level expression of 2,4-dichlorophenoxyacetate monooxygenase gene tfdA of Alcaligenes eutrophus JMP134. J Bacteriol 169: 2950–2955.
- Tonso NL, Matheson VG & Holben WE (1995) Polyphasic characterization of a suite of bacterial isolates capable of degrading 2,4-D. Microb Ecol 30: 3–24.
- Top EM, Maltseva OV & Forney LJ (1996) Capture of a catabolic plasmid that encodes only 2,4-dichlorophenoxyacetic acid: α-ketoglutaric acid dioxygenase (TfdA) by genetic complementation. Appl Environ Microbiol 62: 2470–2476.
- Vallaeys T, Fulthorpe RR, Wright AM & Soulas G (1996) The metabolic pathway of 2,4-dichlorophenoxyacetic acid degradation involves different families of tfdA and tJdB genes according to PCR-RFLP analysis. FEMS Microbiol Ecol 20: 163–172.
- Vieublé Gonod L, Chenu C & Soulas G (2003) Spatial variability of 2,4-dichlorophenoxyacetic acid (2,4-D) mineralisation potential at a millimetre scale in soil. Soil Biol Biochem 35: 373–382.
- Vroumsia T, Steiman R, Seigle-Murandi F & Benoit-Guyod JL (1999) Effects of culture parameters on the degradation of 2,4-dichlorophenoxyacetic acid (2,4-D) and 2,4-dichlorophenol (2,4-DCP) by selected fungi. Chemosphere 39: 1397–1405.
- Vroumsia T, Steiman R, Seigle-Murandi F & Benoit-Guyod JL (2005) Fungal bioconversation of 2,4-dichlorophenoxyacetic acid (2,4-D) and 2,4-dichlorophenol (2,4-DCP). Chemosphere 60: 1471–1480.
- Weinert N, Meincke R, Gottwald C, Heuer H, Gomes NC, Schloter M, Berg G & Smalla K (2009) Rhizosphere communities of genetically modified zeaxanthin-accumulating potato plants and their parent cultivar differ less than those of different potato cultivars. Appl Environ Microbiol 75: 3859–3865.
- White TJ, Bruns T, Lee S & Taylor J (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. PCR Protocols: A Guide to Methods and Applications ( MA Innis, DH Gelfand, JJ Sninsky & TJ White, eds), pp. 315–322. Academic Press, San Diego, CA, USA.
- Zakaria D, Lappin-Scott H, Burton S & Whitby C (2007) Bacterial diversity in soil enrichment cultures amended with 2 (2-methyl-4-chlorophenoxy) propionic acid (mecoprop). Environ Microbiol 9: 2575–2587.
- Zaprasis A, Liu YJ, Liu SJ, Drake HL & Horn MA (2010) Abundance of novel and diverse tfdA-like genes, encoding putative phenoxyalkanoic acid herbicide-degrading dioxygenases, in soil. Appl Environ Microbiol 76: 119–128.
- Zelles L, Adrian P, Bai QY, Stepper K, Adrian MV, Fischer K, Maier A & Ziegle A (1991) Microbial activity measured in soils stored under different temperature and humidity conditions. Soil Biol Biochem 23: 955–961.