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When bioelectrochemical systems meet extremophiles, possibilities and challenges
Linnaeus University, Faculty of Health and Life Sciences, Department of Biology and Environmental Science. (Ctr Ecol & Evolut Microbial Model Syst EEMiS)ORCID iD: 0000-0003-1610-8211
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 [en]
acidophiles, psychrophiles, haloalkaliphiles, bioelectrochemical systems, microbial sulfur metabolism, 16S rRNA gene amplicon sequencing, metagenomics, metatranscriptomics
National Category
Bioremediation
Research subject
Ecology, Microbiology
Identifiers
URN: urn:nbn:se:lnu:diva-77543ISBN: 978-91-88761-82-8 (print)ISBN: 978-91-88761-83-5 (electronic)OAI: oai:DiVA.org:lnu-77543DiVA, id: diva2:1244794
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
List of papers
1. Electricity generation from an inorganic sulfur compound containing mining wastewater by acidophilic microorganisms
Open this publication in new window or tab >>Electricity generation from an inorganic sulfur compound containing mining wastewater by acidophilic microorganisms
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2016 (English)In: Research in Microbiology, ISSN 0923-2508, E-ISSN 1769-7123, Vol. 167, no 7, p. 568-575Article in journal (Refereed) Published
Abstract [en]

Sulfide mineral processing often produces large quantities of wastewaters containing acid-generating inorganic sulfur compounds. If released untreated, these wastewaters can cause catastrophic environmental damage. In this study, microbial fuel cells were inoculated with acidophilic microorganisms to investigate whether inorganic sulfur compound oxidation can generate an electrical current. Cyclic voltammetry suggested that acidophilic microorganisms mediated electron transfer to the anode, and that electricity generation was catalyzed by microorganisms. A cation exchange membrane microbial fuel cell, fed with artificial wastewater containing tetrathionate as electron donor, reached a maximum whole cell voltage of 72 +/- 9 mV. Stepwise replacement of the artificial anolyte with real mining process wastewater had no adverse effect on bioelectrochemical performance and generated a maximum voltage of 105 +/- 42 mV. 16S rRNA gene sequencing of the microbial consortia resulted in sequences that aligned within the genera Thermoplasma, Ferroplasma, Leptospirillum, Sulfobacillus and Acidithiobacillus. This study opens up possibilities to bioremediate mining wastewater using microbial fuel cell technology. (C) 2016 The Authors. Published by Elsevier Masson SAS on behalf of Institut Pasteur.

Keywords
Microbial fuel cell, Electricity generation, Acidophile, Mining, Wastewater
National Category
Environmental Sciences
Research subject
Natural Science, Environmental Science
Identifiers
urn:nbn:se:lnu:diva-57087 (URN)10.1016/j.resmic.2016.04.010 (DOI)000383293900005 ()27155452 (PubMedID)2-s2.0-84974796855 (Scopus ID)
Available from: 2016-10-06 Created: 2016-10-06 Last updated: 2018-11-16Bibliographically approved
2. A novel inorganic sulfur compound metabolizing Ferroplasma-like population is suggested to mediate extracellular electron transfer
Open this publication in new window or tab >>A novel inorganic sulfur compound metabolizing Ferroplasma-like population is suggested to mediate extracellular electron transfer
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2018 (English)In: Frontiers in Microbiology, ISSN 1664-302X, E-ISSN 1664-302X, article id 2945Article in journal (Refereed) Published
Abstract [en]

Mining and processing of metal sulfide ores produces waters containing metals and inorganic sulfur compounds such as tetrathionate and thiosulfate. If released untreated, these sulfur compounds can be oxidized to generate highly acidic wastewaters [termed 'acid mine drainage (AMD)'] that cause severe environmental pollution. One potential method to remediate mining wastewaters is the maturing biotechnology of 'microbial fuel cells' that offers the sustainable removal of acid generating inorganic sulfur compounds alongside producing an electrical current. Microbial fuel cells exploit the ability of bacterial cells to transfer electrons to a mineral as the terminal electron acceptor during anaerobic respiration by replacing the mineral with a solid anode. In consequence, by substituting natural minerals with electrodes, microbial fuel cells also provide an excellent platform to understand environmental microbemineral interactions that are fundamental to element cycling. Previously, tetrathionate degradation coupled to the generation of an electrical current has been demonstrated and here we report a metagenomic and metatranscriptomic analysis of the microbial community. Reconstruction of inorganic sulfur compound metabolism suggested the substrate tetrathionate was metabolized by the Ferroplasma-like and Acidithiobacillus-like populations via multiple pathways. Characterized Ferroplasma species do not utilize inorganic sulfur compounds, suggesting a novel Ferroplasma-likepopulation had been selected. Oxidation of intermediate sulfide, sulfur, thiosulfate, and adenylylsulfate released electrons and the extracellular electrontransfer to the anode was suggested to be dominated by candidate soluble electron shuttles produced by the Ferroplasma-like population. However, as the soluble electron shuttle compounds also have alternative functions within the cell, it cannot be ruled out that acidophiles use novel, uncharacterized mechanisms to mediate extracellular electron transfer. Several populations within the community were suggested to metabolize intermediate inorganicsulfur compounds by multiple pathways, which highlights the potential for mutualistic or symbiotic relationships. This study provided the genetic base for acidophilic microbial fuel cells utilized for the remediation of inorganic sulfur compounds from AMD.

Place, publisher, year, edition, pages
Frontiers Media S.A., 2018
National Category
Microbiology
Research subject
Ecology, Microbiology
Identifiers
urn:nbn:se:lnu:diva-78860 (URN)10.3389/fmicb.2018.02945 (DOI)000452119800001 ()
Available from: 2018-11-16 Created: 2018-11-16 Last updated: 2019-01-18Bibliographically approved
3. Microbial Community and Metabolic Activity in Thiocyanate Degrading Low Temperature Microbial Fuel Cells
Open this publication in new window or tab >>Microbial Community and Metabolic Activity in Thiocyanate Degrading Low Temperature Microbial Fuel Cells
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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
Keywords
MFC, thiocyanate degradation, extracellular electron transfer, low temperature, metatranscriptomics
National Category
Microbiology Ecology
Research subject
Ecology, Microbiology
Identifiers
urn:nbn:se:lnu:diva-78412 (URN)10.3389/fmicb.2018.02308 (DOI)000445903500001 ()
Available from: 2018-10-22 Created: 2018-10-22 Last updated: 2019-02-27Bibliographically approved
4. Haloalkaliphilic microorganisms assist sulfide removal in a microbial electrolysis cell
Open this publication in new window or tab >>Haloalkaliphilic microorganisms assist sulfide removal in a microbial electrolysis cell
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2018 (English)In: Journal of Hazardous Materials, ISSN 0304-3894, E-ISSN 1873-3336, Vol. 363, p. 197-204Article in journal (Refereed) Published
Abstract [en]

Several industrial processes produce toxic sulfide containing streams that are often scrubbed using caustic solutions. An alternative, cost effective sulfidetreatment method is bioelectrochemical sulfide removal. For the first time, a haloalkaliphilic sulfide-oxidizing microbial consortium was introduced to the anodic chamber of a microbial electrolysis cell operated at alkaline pH and with 1.0 M sodium ions. Under anode potential control, the highest sulfideremoval rate was 2.16 mM/day and chemical analysis supported that the electrical current generation was from the sulfide oxidation. Biotic operation produced a maximum current density of 3625 mA/m(2) compared to 210 mA/m2 while under abiotic operation. Furthermore, biotic electrical production was maintained for a longer period than for abiotic operation, potentially due to the passivation of the electrode by elemental sulfur during abiotic operation. The use of microorganisms reduced the energy input in this study compared to published electrochemical sulfide removal technologies. Sulfide-oxidizing populations dominated both the planktonic and electrode-attached communities with 16S rRNA gene sequences aligning within the genera Thioctikalivibrio, Thioalkaihnicrobium, and Desulfurivibrio. The dominance of the Desulfurivibrio-like population on the anode surface offered evidence for the first haloalkaliphilic bacterium able to couple electrons from sulfide oxidation to extracellular electron transfer to the anode.

Place, publisher, year, edition, pages
Elsevier, 2018
National Category
Microbiology
Research subject
Ecology, Microbiology
Identifiers
urn:nbn:se:lnu:diva-78859 (URN)10.1016/j.jhazmat.2018.09.049 (DOI)000449891900022 ()30308358 (PubMedID)
Note

Is included in the dissertation as a manuscript.

Available from: 2018-11-16 Created: 2018-11-16 Last updated: 2018-12-06Bibliographically approved

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Doctoral Thesis (Comprehensive Summary)(6482 kB)87 downloads
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