University of Oulu

Ziegelhöfer A and Kujala K (2021) Assessing the Diversity and Metabolic Potential of Psychrotolerant Arsenic-Metabolizing Microorganisms From a Subarctic Peatland Used for Treatment of Mining-Affected Waters by Culture-Dependent and -Independent Techniques. Front. Microbiol. 12:648412. doi: 10.3389/fmicb.2021.648412

Assessing the diversity and metabolic potential of psychrotolerant arsenic-metabolizing microorganisms from a subarctic peatland used for treatment of mining-affected waters by culture-dependent and -independent techniques

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Author: Ziegelhöfer, Aileen1,2; Kujala, Katharina2
Organizations: 1Faculty for Chemistry & Biotechnology, Aachen University of Applied Sciences, Jülich, Germany
2Water, Energy and Environmental Engineering Research Unit, University of Oulu, Oulu, Finland
Format: article
Version: published version
Access: open
Online Access: PDF Full Text (PDF, 6.7 MB)
Persistent link: http://urn.fi/urn:nbn:fi-fe2021101150605
Language: English
Published: Frontiers Media, 2021
Publish Date: 2021-10-11
Description:

Abstract

Arsenic contamination in water by natural causes or industrial activities is a major environmental concern, and treatment of contaminated waters is needed to protect water resources and minimize the risk for human health. In mining environments, treatment peatlands are used in the polishing phase of water treatment to remove arsenic (among other contaminants), and peat microorganisms play a crucial role in arsenic removal. The present study assessed culture-independent diversity obtained through metagenomic and metatranscriptomic sequencing and culture-dependent diversity obtained by isolating psychrotolerant arsenic-tolerant, arsenite-oxidizing, and arsenate-respiring microorganisms from a peatland treating mine effluent waters of a gold mine in Finnish Lapland using a dilution-to-extinction technique. Low diversity enrichments obtained after several transfers were dominated by the genera Pseudomonas, Polaromonas, Aeromonas, Brevundimonas, Ancylobacter, and Rhodoferax. Even though maximal growth and physiological activity (i.e., arsenite oxidation or arsenate reduction) were observed at temperatures between 20 and 28°C, most enrichments also showed substantial growth/activity at 2–5°C, indicating the successful enrichments of psychrotolerant microorganisms. After additional purification, eight arsenic-tolerant, five arsenite-oxidizing, and three arsenate-respiring strains were obtained in pure culture and identified as Pseudomonas, Rhodococcus, Microbacterium, and Cadophora. Some of the enriched and isolated genera are not known to metabolize arsenic, and valuable insights on arsenic turnover pathways may be gained by their further characterization. Comparison with phylogenetic and functional data from the metagenome indicated that the enriched and isolated strains did not belong to the most abundant genera, indicating that culture-dependent and -independent methods capture different fractions of the microbial community involved in arsenic turnover. Rare biosphere microorganisms that are present in low abundance often play an important role in ecosystem functioning, and the enriched/isolated strains might thus contribute substantially to arsenic turnover in the treatment peatland. Psychrotolerant pure cultures of arsenic-metabolizing microorganisms from peatlands are needed to close the knowledge gaps pertaining to microbial arsenic turnover in peatlands located in cold climate regions, and the isolates and enrichments obtained in this study are a good starting point to establish model systems. Improved understanding of their metabolism could moreover lead to their use in biotechnological applications intended for bioremediation of arsenic-contaminated waters.

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Series: Frontiers in microbiology
ISSN: 1664-302X
ISSN-E: 1664-302X
ISSN-L: 1664-302X
Volume: 12
Article number: 648412
DOI: 10.3389/fmicb.2021.648412
OADOI: https://oadoi.org/10.3389/fmicb.2021.648412
Type of Publication: A1 Journal article – refereed
Field of Science: 218 Environmental engineering
Subjects:
Funding: Funding for this work was provided by the Academy of Finland (projects 287397 “Microbial transformations of arsenic and antimony in Northern natural peatlands treating mine waste waters” and 322753 “Capturing the unknown microbial players and genes involved in the cycling of arsenic and antimony in Northern peatland soils”), the Renlund Foundation (project “Fate of accumulated arsenic and antimony in peatlands used for treatment of mining-affected wastewaters”), and the University of Oulu.
Academy of Finland Grant Number: 287397
322753
Detailed Information: 287397 (Academy of Finland Funding decision)
322753 (Academy of Finland Funding decision)
Dataset Reference: The original contributions presented in the study are publicly available. 16S rRNA gene and ITS sequence data can be found in NCBI under accession numbers MW496900–MW497062 (enrichments), MW800181–MW800195 (bacterial isolates), and MW800602 (fungal isolate). The metagenome and metatranscriptome sequence data are available at MGRast under project numbers mgm4838788.3, mgm4928889.3, and mgm4928890.3.
Copyright information: © 2021 Ziegelhöfer and Kujala. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
  https://creativecommons.org/licenses/by/4.0/