DNA sequence variation and methylation in an arsenic tolerant earthworm population

Peter Kille, Jane Andre, Craig Anderson, Hui Na Ang, Michael W. Bruford, Jacob G. Bundy, Robert Donnelly, Mark E. Hodson, Gabriela Juma, Elma Lahive, A. John Morgan, Stephen R. Stürzenbaum, David J. Spurgeon

Research output: Contribution to journalArticle

42 Citations (Scopus)

Abstract

Evidence is emerging that earthworms can evolve tolerance to trace element enriched soils. However, few studies have sought to establish whether such tolerance is determined through adaptation or plasticity. Here we report results from a combined analysis of mitochondrial (cytochrome oxidase II, COII), nuclear (amplified fragment length polymorphism, AFLP) variation and DNA methylation in populations of the earthworm Lumbricus rubellus from sites across an abandoned arsenic and copper mine. Earthworms from the mine site population demonstrated clear arsenic tolerance in comparison to a naïve strain. COII and AFLP results suggest that L. rubellus from the unexposed and the adapted populations comprises two cryptic lineages (Lineages A and B) each of which was present across all of the sites. AFLP analysis by lineage highlighted variations associated with soil metal/metalloid concentrations (most clearly for Lineage A) suggesting a genetic component to the observed tolerance. The methylation sensitive AFLP (Me-AFLP) identified a high genome methylation content (average 13.5%) in both lineages. For Lineage A, Me-AFLP analysis did not identify a strong association with soil arsenic levels. For Lineage B, however, a clear association of methylation patterns with soil arsenic concentrations was found. This suggests that Lineage B earthworms utilise epigenetic mechanisms to adapt to the presence of contamination. These fundamentally different genetic adjustments in the two clades indicate that the two lineages employ distinct adaptive strategies (genetic or epigenetic) in response to arsenic exposure. Mechanisms driving this variation may be founded within the colonisation histories of the lineages.
LanguageEnglish
Pages524-532
Number of pages9
JournalSoil Biology and Biochemistry
Volume57
Early online date27 Oct 2012
DOIs
Publication statusPublished - Feb 2013
Externally publishedYes

Fingerprint

Oligochaeta
methylation
Arsenic
DNA Methylation
arsenic
earthworms
earthworm
amplified fragment length polymorphism
Methylation
nucleotide sequences
DNA
polymorphism
Soil
tolerance
Amplified Fragment Length Polymorphism Analysis
Lumbricus rubellus
Population
Electron Transport Complex IV
Epigenomics
epigenetics

Cite this

Kille, P., Andre, J., Anderson, C., Ang, H. N., Bruford, M. W., Bundy, J. G., ... Spurgeon, D. J. (2013). DNA sequence variation and methylation in an arsenic tolerant earthworm population. Soil Biology and Biochemistry, 57, 524-532. https://doi.org/10.1016/j.soilbio.2012.10.014
Kille, Peter ; Andre, Jane ; Anderson, Craig ; Ang, Hui Na ; Bruford, Michael W. ; Bundy, Jacob G. ; Donnelly, Robert ; Hodson, Mark E. ; Juma, Gabriela ; Lahive, Elma ; Morgan, A. John ; Stürzenbaum, Stephen R. ; Spurgeon, David J. / DNA sequence variation and methylation in an arsenic tolerant earthworm population. In: Soil Biology and Biochemistry. 2013 ; Vol. 57. pp. 524-532.
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Kille, P, Andre, J, Anderson, C, Ang, HN, Bruford, MW, Bundy, JG, Donnelly, R, Hodson, ME, Juma, G, Lahive, E, Morgan, AJ, Stürzenbaum, SR & Spurgeon, DJ 2013, 'DNA sequence variation and methylation in an arsenic tolerant earthworm population', Soil Biology and Biochemistry, vol. 57, pp. 524-532. https://doi.org/10.1016/j.soilbio.2012.10.014

DNA sequence variation and methylation in an arsenic tolerant earthworm population. / Kille, Peter; Andre, Jane; Anderson, Craig; Ang, Hui Na; Bruford, Michael W.; Bundy, Jacob G.; Donnelly, Robert; Hodson, Mark E.; Juma, Gabriela; Lahive, Elma; Morgan, A. John; Stürzenbaum, Stephen R.; Spurgeon, David J.

In: Soil Biology and Biochemistry, Vol. 57, 02.2013, p. 524-532.

Research output: Contribution to journalArticle

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T1 - DNA sequence variation and methylation in an arsenic tolerant earthworm population

AU - Kille, Peter

AU - Andre, Jane

AU - Anderson, Craig

AU - Ang, Hui Na

AU - Bruford, Michael W.

AU - Bundy, Jacob G.

AU - Donnelly, Robert

AU - Hodson, Mark E.

AU - Juma, Gabriela

AU - Lahive, Elma

AU - Morgan, A. John

AU - Stürzenbaum, Stephen R.

AU - Spurgeon, David J.

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N2 - Evidence is emerging that earthworms can evolve tolerance to trace element enriched soils. However, few studies have sought to establish whether such tolerance is determined through adaptation or plasticity. Here we report results from a combined analysis of mitochondrial (cytochrome oxidase II, COII), nuclear (amplified fragment length polymorphism, AFLP) variation and DNA methylation in populations of the earthworm Lumbricus rubellus from sites across an abandoned arsenic and copper mine. Earthworms from the mine site population demonstrated clear arsenic tolerance in comparison to a naïve strain. COII and AFLP results suggest that L. rubellus from the unexposed and the adapted populations comprises two cryptic lineages (Lineages A and B) each of which was present across all of the sites. AFLP analysis by lineage highlighted variations associated with soil metal/metalloid concentrations (most clearly for Lineage A) suggesting a genetic component to the observed tolerance. The methylation sensitive AFLP (Me-AFLP) identified a high genome methylation content (average 13.5%) in both lineages. For Lineage A, Me-AFLP analysis did not identify a strong association with soil arsenic levels. For Lineage B, however, a clear association of methylation patterns with soil arsenic concentrations was found. This suggests that Lineage B earthworms utilise epigenetic mechanisms to adapt to the presence of contamination. These fundamentally different genetic adjustments in the two clades indicate that the two lineages employ distinct adaptive strategies (genetic or epigenetic) in response to arsenic exposure. Mechanisms driving this variation may be founded within the colonisation histories of the lineages.

AB - Evidence is emerging that earthworms can evolve tolerance to trace element enriched soils. However, few studies have sought to establish whether such tolerance is determined through adaptation or plasticity. Here we report results from a combined analysis of mitochondrial (cytochrome oxidase II, COII), nuclear (amplified fragment length polymorphism, AFLP) variation and DNA methylation in populations of the earthworm Lumbricus rubellus from sites across an abandoned arsenic and copper mine. Earthworms from the mine site population demonstrated clear arsenic tolerance in comparison to a naïve strain. COII and AFLP results suggest that L. rubellus from the unexposed and the adapted populations comprises two cryptic lineages (Lineages A and B) each of which was present across all of the sites. AFLP analysis by lineage highlighted variations associated with soil metal/metalloid concentrations (most clearly for Lineage A) suggesting a genetic component to the observed tolerance. The methylation sensitive AFLP (Me-AFLP) identified a high genome methylation content (average 13.5%) in both lineages. For Lineage A, Me-AFLP analysis did not identify a strong association with soil arsenic levels. For Lineage B, however, a clear association of methylation patterns with soil arsenic concentrations was found. This suggests that Lineage B earthworms utilise epigenetic mechanisms to adapt to the presence of contamination. These fundamentally different genetic adjustments in the two clades indicate that the two lineages employ distinct adaptive strategies (genetic or epigenetic) in response to arsenic exposure. Mechanisms driving this variation may be founded within the colonisation histories of the lineages.

KW - Arsenic tolerance

KW - Cryptic lineages

KW - Adaptive variation

KW - DNA methylation

KW - Epigenetics

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DO - 10.1016/j.soilbio.2012.10.014

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JO - Soil Biology and Biochemistry

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