Biological chlorine cycling in the Arctic Coastal Plain

Abstract

This study explores biological chlorine cycling in coastal Arctic wet tundra soils. While many previous chlorine-cycling studies have focused on contaminated environments, it is now recognized that chlorine can cycle naturally between inorganic and organic forms in soils. However, these pathways have not previously been described for an Arctic ecosystem. We measured soil organic and inorganic Cl pools, characterized soils and plant tissues with chlorine K-edge X-ray absorption near-edge spectroscopy (Cl-XANES), measured dechlorination rates in laboratory incubations, and analyzed metagenomes and 16S rRNA genes along a chronosequence of revegetated drained lake basins. Concentrations of soil organic chlorinated compounds (Clorg) were correlated with organic matter content, with a steeper slope in older soils. The concentration and chemical diversity of Clorg increased with soil development, with Clorg in younger soils more closely resembling that of vegetation, and older soils having more complex and variable Cl-XANES signatures. Plant Clorg concentrations were higher than previously published values, and can account for the rapid accumulation of Clorg in soils. The high rates of Clorg input from plants also implies that soil Clorg pools turn over many times during soil development. Metagenomic analyses revealed putative genes for synthesis (haloperoxidases, halogenases) and breakdown (reductive dehalogenases, halo-acid dehalogenases) of Clorg, originating from diverse microbial genomes. Many genome sequences with close similarity to known organohalide respirers (e.g. Dehalococcoides) were identified, and laboratory incubations demonstrated microbial organohalide respiration in vitro. This study provides multiple lines of evidence for a complex and dynamic chlorine cycle in an Arctic tundra ecosystem.

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Acknowledgements

Dominic Goria, Matt Haggerty and the SDSU Ecological Metagenomics Class of 2012 were instrumental in metagenome creation and analysis. Donatella Zona and Paulo Olivas provided plant samples. We thank Trudy Bolin and Tianpin Wu at Argonne National Labs for their training and patience. This research used resources of the Advanced Photon Source, a U.S. Department of Energy (DOE) Office of Science User Facility operated for the DOE Office of Science by Argonne National Laboratory under Contract No. DE-AC02-06CH11357. XANES spectra were collected at the X-ray Operations and Research Beamline 9-BM-C at the Advanced Photon Source, Argonne National Laboratory in Lemont, Illinois, U.S.A. Competitive access to the APS was greatly aided by proof-of-concept XANES spectra collected at the Canadian Light Source by Yongfeng Hu. This work was supported in part by National Science Foundation Grants 0808604, 1204263 and 1712774.

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Zlamal, J.E., Raab, T.K., Little, M. et al. Biological chlorine cycling in the Arctic Coastal Plain. Biogeochemistry 134, 243–260 (2017). https://doi.org/10.1007/s10533-017-0359-0

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Keywords

  • Chlorine
  • Halogen
  • Organohalide respiration
  • XANES
  • Arctic
  • Dehalococcoides