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Microbial Community and Metabolic Activity in Thiocyanate Degrading Low Temperature Microbial Fuel Cells
Linnaeus University, Faculty of Health and Life Sciences, Department of Biology and Environmental Science. (Ctr Ecol & Evolut Microbial Model Syst EEMiS)
Linnaeus University, Faculty of Health and Life Sciences, Department of Biology and Environmental Science. Wetsus, European Ctr Excellence Sustainable Water Technol, Netherlands. (Ctr Ecol & Evolut Microbial Model Syst EEMiS)
Linnaeus University, Faculty of Health and Life Sciences, Department of Biology and Environmental Science. (Ctr Ecol & Evolut Microbial Model Syst EEMiS)ORCID iD: 0000-0001-9005-5168
Linnaeus University, Faculty of Health and Life Sciences, Department of Biology and Environmental Science. (Ctr Ecol & Evolut Microbial Model Syst EEMiS)
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2018 (English)In: Frontiers in Microbiology, ISSN 1664-302X, E-ISSN 1664-302X, Vol. 9, article id 2308Article in journal (Refereed) Published
Abstract [en]

Thiocyanate is a toxic compound produced by the mining and metallurgy industries that needs to be remediated prior to its release into the environment. If the industry is situated at high altitudes or near the poles, economic factors require a low temperature treatment process. Microbial fuel cells are a developing technology that have the benefits of both removing such toxic compounds while recovering electrical energy. In this study, simultaneous thiocyanate degradation and electrical current generation was demonstrated and it was suggested that extracellular electron transfer to the anode occurred. Investigation of the microbial community by 16S rRNA metatranscriptome reads supported that the anode attached and planktonic anolyte consortia were dominated by a Thiobacillus-like population. Metatranscriptomic sequencing also suggested thiocyanate degradation primarily occurred via the 'cyanate' degradation pathway. The generated sulfide was metabolized via sulfite and ultimately to sulfate mediated by reverse dissimilatory sulfite reductase, APS reductase, and sulfate adenylyltransferase and the released electrons were potentially transferred to the anode via soluble electron shuttles. Finally, the ammonium from thiocyanate degradation was assimilated to glutamate as nitrogen source and carbon dioxide was fixed as carbon source. This study is one of the first to demonstrate a low temperature inorganic sulfur utilizing microbial fuel cell and the first to provide evidence for pathways of thiocyanate degradation coupled to electron transfer.

Place, publisher, year, edition, pages
Frontiers Media S.A., 2018. Vol. 9, article id 2308
Keywords [en]
MFC, thiocyanate degradation, extracellular electron transfer, low temperature, metatranscriptomics
National Category
Microbiology Ecology
Research subject
Ecology, Microbiology
Identifiers
URN: urn:nbn:se:lnu:diva-78412DOI: 10.3389/fmicb.2018.02308ISI: 000445903500001OAI: oai:DiVA.org:lnu-78412DiVA, id: diva2:1257728
Available from: 2018-10-22 Created: 2018-10-22 Last updated: 2019-02-27Bibliographically approved
In thesis
1. When bioelectrochemical systems meet extremophiles, possibilities and challenges
Open this publication in new window or tab >>When bioelectrochemical systems meet extremophiles, possibilities and challenges
2018 (English)Doctoral thesis, comprehensive summary (Other academic)
Abstract [en]

Extremophiles are microorganisms live and thrive in extreme environments that are harsh and hostile to most forms of life on earth (e.g. low pH, low temperature, high pH and high salinity). They have developed strategies to obtain nutrients and conserve energy to sustain life under these adverse conditions. Such metabolic capabilities are valuable to be exploit for industrial applications such as the remediation of environmental pollutions, which typically bring about extreme physicochemical conditions. The advancing technology bioelectrochemical systems can utilize the microbial metabolism to oxidize a substrate while simultaneously recover electrical energy or produce a useful product in an electrochemical set-up. It enables the remediation of pollutions, and its integration with extremophiles has opened up a wide range of possibilities to tackle various industrial waste streams with extreme conditions in an environmentally friendly manner. Inorganic sulfur compounds such as tetrathionate, thiocyanate and sulfide that originate from mining, metal refinery and petroleum industries are toxic and hazardous to the recipient water body and human health if discharged untreated. The remediation of these three compounds with bioelectrochemical systems that incorporates extremophiles was investigated in three separate studies of this thesis. 16S rRNA gene amplicon sequencing, metagenomics and metatranscriptomics are utilized to profile the microbial communities, and to understand their metabolic potential and states.

 

Tetrathionate degradation with acidophilic microorganisms in microbial fuel cells at pH 2 was demonstrated in the first study of this thesis. Electricity was produced from the oxidation of tetrathionate, facilitated by the anodic microbiome. 16S rRNA gene amplicon sequencing showed that this community was dominated by members of the genera Thermoplasma, Ferroplasma, Leptospirillum, Sulfobacillus and Acidithiobacillus. Metagenomic analysis reconstructed genomes that were most similar to the genera Ferroplasma, Acidithiobacillus, Sulfobacillus and Cuniculiplasma. Together with metatranscriptomic analysis, it was indicated that this microbial community was metabolizing tetrathionate and other intermediate sulfur compounds via multiple pathways, the electrons released from oxidation were suggested to be transferred to the electrode via soluble electron shuttles. In addition, the Ferroplasma-like population in this study was suggested to be active in metabolising inorganic sulfur compounds and synthesizing soluble electron shuttles. Since characterized Ferroplasma species do not utilize inorganic sulfur compounds, the anodic compartment might have selected a novel Ferroplasma population.

 

Next, thiocyanate degradation with psychrophilic microorganisms in microbial fuel cells at 8 °C was demonstrated for the first time. Electricity generation alongside with thiocyanate degradation facilitated by the anodic microbiome was observed. 16S rRNA gene amplicon sequencing and metatranscriptomics suggested that Thiobacillus was the predominant and most active population. mRNA analysis revealed that thiocyanate was metabolized primarily via the ‘cyanate’ degradation pathway; the resultant sulfide was oxidized; ammonium was assimilated; carbon dioxide was fixed as carbon source. It was also suggested by mRNA analysis that the consortium used multiple mechanisms to acclimate low temperature such as the synthesis of cold shock proteins, cold inducible proteins and molecular chaperones.

 

Finally, sulfide removal with haloalkaliphilic microorganisms in microbial electrolysis cells operated at pH 8.8 to 9.5 and with 1.0 M sodium ion was investigated. The anodic microbiome was hypothesized to facilitate current generation by the oxidation of sulfide and of intermediate sulfur compounds to sulfate, which was supported by chemical analysis and microbial profiling. Dominant populations from the anode had 16S rRNA gene sequences that aligned within the genera Thioalkalivibrio, Thioalkalimicrobium, and Desulfurivibrio, which are known for sulfide oxidation. Intriguingly, Desulfurivibrio dominated the electrode-attached community, possibly enriched by the electrode as a selecting pressure. This finding suggested a novel role of this organism to carry out sulfide oxidation coupled to electron transfer to the electrode.

 

These three studies demonstrated the possibilities of utilizing extremophilic bioelectrochemical systems to remediate various inorganic sulfur pollution streams. The advancing molecular microbiological tools facilitated the investigation towards the composition and metabolic state of the microbial community. Challenges remain in a more thorough understanding regarding the metabolism of extremophiles (e.g. sulfur metabolism and extracellular electron transfer) and better energy recovery in bioelectrochemical systems.

Place, publisher, year, edition, pages
Kalmar, Växjö: Linnaeus University Press, 2018. p. 70
Series
Linnaeus University Dissertations ; 325
Keywords
acidophiles, psychrophiles, haloalkaliphiles, bioelectrochemical systems, microbial sulfur metabolism, 16S rRNA gene amplicon sequencing, metagenomics, metatranscriptomics
National Category
Bioremediation
Research subject
Ecology, Microbiology
Identifiers
urn:nbn:se:lnu:diva-77543 (URN)978-91-88761-82-8 (ISBN)978-91-88761-83-5 (ISBN)
Public defence
2018-09-07, Fullriggaren, Landgången 4, Kalmar, 09:00 (English)
Opponent
Supervisors
Available from: 2018-09-03 Created: 2018-09-03 Last updated: 2018-11-16Bibliographically approved

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Ni, GaofengBroman, EliasSimone, DomenicoLundin, DanielLopez-Fernandez, MargaritaDopson, Mark

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