The earthworm Aporrectodea caliginosa stimulates abundance and activity of phenoxyalkanoic acid herbicide degraders

Research output: Contribution to journalArticleResearchpeer review

Authors

  • Ya Jun Liu
  • Adrienne Zaprasis
  • Shuang Jiang Liu
  • Harold L. Drake
  • Marcus A. Horn

External Research Organisations

  • University of Bayreuth
  • CAS - Institute of Microbiology
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Details

Original languageEnglish
Pages (from-to)473-485
Number of pages13
JournalISME Journal
Volume5
Issue number3
Publication statusPublished - Mar 2011
Externally publishedYes

Abstract

2-Methyl-4-chlorophenoxyacetic acid (MCPA) is a widely used phenoxyalkanoic acid (PAA) herbicide. Earthworms represent the dominant macrofauna and enhance microbial activities in many soils. Thus, the effect of the model earthworm Aporrectodea caliginosa (Oligochaeta, Lumbricidae) on microbial MCPA degradation was assessed in soil columns with agricultural soil. MCPA degradation was quicker in soil with earthworms than without earthworms. Quantitative PCR was inhibition-corrected per nucleic acid extract and indicated that copy numbers of tfdA-like and cadA genes (both encoding oxygenases initiating aerobic PAA degradation) in soil with earthworms were up to three and four times higher than without earthworms, respectively. tfdA-like and 16S rRNA gene transcript copy numbers in soil with earthworms were two and six times higher than without earthworms, respectively. Most probable numbers (MPNs) of MCPA degraders approximated 4 × 10 5 g dw -1 in soil before incubation and in soil treated without earthworms, whereas MPNs of earthworm-treated soils were approximately 150 × higher. The aerobic capacity of soil to degrade MCPA was higher in earthworm-treated soils than in earthworm-untreated soils. Burrow walls and 0-5 cm depth bulk soil displayed higher capacities to degrade MCPA than did soil from 5-10 cm depth bulk soil, expression of tfdA-like genes in burrow walls was five times higher than in bulk soil and MCPA degraders were abundant in burrow walls (MPNs of 5 × 10 7 g dw -1). The collective data indicate that earthworms stimulate abundance and activity of MCPA degraders endogenous to soil by their burrowing activities and might thus be advantageous for enhancing PAA degradation in soil.

Keywords

    bioconcentration, cadA, drilosphere, gene expression, mRNA, quantitative PCR, relative gene frequency ratio, tfdA-like

ASJC Scopus subject areas

Cite this

The earthworm Aporrectodea caliginosa stimulates abundance and activity of phenoxyalkanoic acid herbicide degraders. / Liu, Ya Jun; Zaprasis, Adrienne; Liu, Shuang Jiang et al.
In: ISME Journal, Vol. 5, No. 3, 03.2011, p. 473-485.

Research output: Contribution to journalArticleResearchpeer review

Liu YJ, Zaprasis A, Liu SJ, Drake HL, Horn MA. The earthworm Aporrectodea caliginosa stimulates abundance and activity of phenoxyalkanoic acid herbicide degraders. ISME Journal. 2011 Mar;5(3):473-485. doi: 10.1038/ismej.2010.140
Liu, Ya Jun ; Zaprasis, Adrienne ; Liu, Shuang Jiang et al. / The earthworm Aporrectodea caliginosa stimulates abundance and activity of phenoxyalkanoic acid herbicide degraders. In: ISME Journal. 2011 ; Vol. 5, No. 3. pp. 473-485.
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title = "The earthworm Aporrectodea caliginosa stimulates abundance and activity of phenoxyalkanoic acid herbicide degraders",
abstract = "2-Methyl-4-chlorophenoxyacetic acid (MCPA) is a widely used phenoxyalkanoic acid (PAA) herbicide. Earthworms represent the dominant macrofauna and enhance microbial activities in many soils. Thus, the effect of the model earthworm Aporrectodea caliginosa (Oligochaeta, Lumbricidae) on microbial MCPA degradation was assessed in soil columns with agricultural soil. MCPA degradation was quicker in soil with earthworms than without earthworms. Quantitative PCR was inhibition-corrected per nucleic acid extract and indicated that copy numbers of tfdA-like and cadA genes (both encoding oxygenases initiating aerobic PAA degradation) in soil with earthworms were up to three and four times higher than without earthworms, respectively. tfdA-like and 16S rRNA gene transcript copy numbers in soil with earthworms were two and six times higher than without earthworms, respectively. Most probable numbers (MPNs) of MCPA degraders approximated 4 × 10 5 g dw -1 in soil before incubation and in soil treated without earthworms, whereas MPNs of earthworm-treated soils were approximately 150 × higher. The aerobic capacity of soil to degrade MCPA was higher in earthworm-treated soils than in earthworm-untreated soils. Burrow walls and 0-5 cm depth bulk soil displayed higher capacities to degrade MCPA than did soil from 5-10 cm depth bulk soil, expression of tfdA-like genes in burrow walls was five times higher than in bulk soil and MCPA degraders were abundant in burrow walls (MPNs of 5 × 10 7 g dw -1). The collective data indicate that earthworms stimulate abundance and activity of MCPA degraders endogenous to soil by their burrowing activities and might thus be advantageous for enhancing PAA degradation in soil.",
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author = "Liu, {Ya Jun} and Adrienne Zaprasis and Liu, {Shuang Jiang} and Drake, {Harold L.} and Horn, {Marcus A.}",
note = "Funding Information: We are grateful to Stephan Schulz, Michael Schloter and Jean Charles Munch for provision of soil samples; Klaus-Holger Knorr and Julia Beer for help with scintillation counting; and Martina Gocke, Ilse Thaufelder and Yakov Kuzyakov for support with the analysis of non-extractable residues of MCPA. Support for this study was provided by the Deutsche Forschungsgemeinschaft (DFG Grant HO4020/1-1, DFG Priority Program 1315 {\textquoteleft}Biogeochemical interfaces in soil{\textquoteright}), by the University of Bayreuth and by grants from the Chinese Academy of Sciences (KSCX2-SW-G-052) and the German Academic Exchange Service (DAAD) to Y-JL. Copyright: Copyright 2012 Elsevier B.V., All rights reserved.",
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T1 - The earthworm Aporrectodea caliginosa stimulates abundance and activity of phenoxyalkanoic acid herbicide degraders

AU - Liu, Ya Jun

AU - Zaprasis, Adrienne

AU - Liu, Shuang Jiang

AU - Drake, Harold L.

AU - Horn, Marcus A.

N1 - Funding Information: We are grateful to Stephan Schulz, Michael Schloter and Jean Charles Munch for provision of soil samples; Klaus-Holger Knorr and Julia Beer for help with scintillation counting; and Martina Gocke, Ilse Thaufelder and Yakov Kuzyakov for support with the analysis of non-extractable residues of MCPA. Support for this study was provided by the Deutsche Forschungsgemeinschaft (DFG Grant HO4020/1-1, DFG Priority Program 1315 ‘Biogeochemical interfaces in soil’), by the University of Bayreuth and by grants from the Chinese Academy of Sciences (KSCX2-SW-G-052) and the German Academic Exchange Service (DAAD) to Y-JL. Copyright: Copyright 2012 Elsevier B.V., All rights reserved.

PY - 2011/3

Y1 - 2011/3

N2 - 2-Methyl-4-chlorophenoxyacetic acid (MCPA) is a widely used phenoxyalkanoic acid (PAA) herbicide. Earthworms represent the dominant macrofauna and enhance microbial activities in many soils. Thus, the effect of the model earthworm Aporrectodea caliginosa (Oligochaeta, Lumbricidae) on microbial MCPA degradation was assessed in soil columns with agricultural soil. MCPA degradation was quicker in soil with earthworms than without earthworms. Quantitative PCR was inhibition-corrected per nucleic acid extract and indicated that copy numbers of tfdA-like and cadA genes (both encoding oxygenases initiating aerobic PAA degradation) in soil with earthworms were up to three and four times higher than without earthworms, respectively. tfdA-like and 16S rRNA gene transcript copy numbers in soil with earthworms were two and six times higher than without earthworms, respectively. Most probable numbers (MPNs) of MCPA degraders approximated 4 × 10 5 g dw -1 in soil before incubation and in soil treated without earthworms, whereas MPNs of earthworm-treated soils were approximately 150 × higher. The aerobic capacity of soil to degrade MCPA was higher in earthworm-treated soils than in earthworm-untreated soils. Burrow walls and 0-5 cm depth bulk soil displayed higher capacities to degrade MCPA than did soil from 5-10 cm depth bulk soil, expression of tfdA-like genes in burrow walls was five times higher than in bulk soil and MCPA degraders were abundant in burrow walls (MPNs of 5 × 10 7 g dw -1). The collective data indicate that earthworms stimulate abundance and activity of MCPA degraders endogenous to soil by their burrowing activities and might thus be advantageous for enhancing PAA degradation in soil.

AB - 2-Methyl-4-chlorophenoxyacetic acid (MCPA) is a widely used phenoxyalkanoic acid (PAA) herbicide. Earthworms represent the dominant macrofauna and enhance microbial activities in many soils. Thus, the effect of the model earthworm Aporrectodea caliginosa (Oligochaeta, Lumbricidae) on microbial MCPA degradation was assessed in soil columns with agricultural soil. MCPA degradation was quicker in soil with earthworms than without earthworms. Quantitative PCR was inhibition-corrected per nucleic acid extract and indicated that copy numbers of tfdA-like and cadA genes (both encoding oxygenases initiating aerobic PAA degradation) in soil with earthworms were up to three and four times higher than without earthworms, respectively. tfdA-like and 16S rRNA gene transcript copy numbers in soil with earthworms were two and six times higher than without earthworms, respectively. Most probable numbers (MPNs) of MCPA degraders approximated 4 × 10 5 g dw -1 in soil before incubation and in soil treated without earthworms, whereas MPNs of earthworm-treated soils were approximately 150 × higher. The aerobic capacity of soil to degrade MCPA was higher in earthworm-treated soils than in earthworm-untreated soils. Burrow walls and 0-5 cm depth bulk soil displayed higher capacities to degrade MCPA than did soil from 5-10 cm depth bulk soil, expression of tfdA-like genes in burrow walls was five times higher than in bulk soil and MCPA degraders were abundant in burrow walls (MPNs of 5 × 10 7 g dw -1). The collective data indicate that earthworms stimulate abundance and activity of MCPA degraders endogenous to soil by their burrowing activities and might thus be advantageous for enhancing PAA degradation in soil.

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