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Function and Adaptation of Acidophiles in Natural and Applied Communities
Linnaeus University, Faculty of Health and Life Sciences, Department of Biology and Environmental Science. (Ctr Ecol & Evolut Microbial Model Syst EEMiS;Systems Biology of Extreme Microorganisms)ORCID iD: 0000-0003-0021-2452
2018 (English)Doctoral thesis, comprehensive summary (Other academic)
Abstract [en]

Acidophiles are organisms that have evolved to grow optimally at high concentrations of protons. Members of this group are found in all three domains of life, although most of them belong to the Archaea and Bacteria. As their energy demand is often met chemolithotrophically by the oxidation of basic ions and molecules such as Fe2+, H2, and sulfur compounds, they are often found in environments marked by the natural or anthropogenic exposure of sulfide minerals. Nonetheless, organoheterotrophic growth is also common, especially at higher temperatures. Beside their remarkable resistance to proton attack, acidophiles are resistant to a multitude of other environmental factors, including toxic heavy metals, high temperatures, and oxidative stress. This allows them to thrive in environments with high metal concentrations and makes them ideal for application in so-called biomining technologies.

The first study of this thesis investigated the iron-oxidizer Acidithiobacillus ferrivorans that is highly relevant for boreal biomining. Several unresolved nodes of its sulfur metabolism were elucidated with the help of RNA transcript sequencing analysis. A model was proposed for the oxidation of the inorganic sulfur compound tetrathionate. In a second paper, this species’ transcriptional response to growth at low temperature was explored and revealed that At. ferrivorans increases expression of only very few known cold-stress genes, underlining its strong adaptation to cold environments.

Another set of studies focused on the environmentally friendly metal winning technology of bioleaching. One of the most important iron-oxidizers in many biomining operations is Leptospirillum ferriphilum. Despite its significance, only a draft genome sequence was available for its type strain.Therefore, in the third paper of this thesis we published a high quality, closed genome sequence of this strain for future use as a reference, revealing a previously unidentified nitrogen fixation system and improving annotation of genes relevant in biomining environments. In addition, RNA transcript and protein patterns during L. ferriphilum’s growth on ferrous iron and in bioleaching culture were used to identify key traits that aid its survival in extremely acidic, metal-rich environments. The biomining of copper from chalcopyrite is plagued by a slow dissolution rate, which can reportedly be circumvented by low redox potentials. As conventional redox control is impossible in heap leaching, paper four explored the possibility of using differentially efficient iron oxidizers to influence this parameter. The facultative heterotrophic Sulfobacillus thermosulfidooxidans was identified as maintaining a redox potential of ~550 mV vs Ag/AgCl, favorable for chalcopyrite dissolution,while L. ferriphilum caused the potential to raise far above this critical value. RNA transcript analysis was used to identify genomic features that may contribute to this behavior.

Lastly, six fields in Northern Sweden were examined for the presence of acid sulfate soils in the fifth paper. The study revealed three acid sulfate soils. The presence of acidophiles that likely catalyze the production of acid in the soil was confirmed by community 16S gene amplicon analysis. One site that was flooded in a remediation attempt and is therefore anoxic still exhibited similar bacteria, however, these now likely grow via ferric iron reduction. This process consumes protons and could explain the observed rise in pH at this site.

This thesis examines acidophiles in pure culture, as well as natural and designed communities. Key metabolic traits involved in the adaptation to their habitats were elucidated, and their application in mining operations was discussed. Special attention was paid to acidophiles in chalcopyrite bioleaching and in cold environments, including environmental acid sulfate soils in Northern Sweden.

Place, publisher, year, edition, pages
Växjö: Linnaeus University Press, 2018.
Series
Linnaeus University Dissertations ; 328
Keywords [en]
Acidophiles, Biomining, Psychrophiles, Adaptation, Acid Sulfate Soil, Redox Control
National Category
Ecology
Research subject
Natural Science, Ecology
Identifiers
URN: urn:nbn:se:lnu:diva-77666ISBN: 978-91-88761-94-1 (print)ISBN: 978-91-88761-95-8 (electronic)OAI: oai:DiVA.org:lnu-77666DiVA, id: diva2:1246973
Public defence
2018-10-19, Norrgård, Kalmar, 09:30 (English)
Opponent
Supervisors
Available from: 2018-09-11 Created: 2018-09-10 Last updated: 2018-11-16Bibliographically approved
List of papers
1. RNA transcript sequencing reveals inorganic sulfur compound oxidation pathways in the acidophile Acidithiobacillus ferrivorans
Open this publication in new window or tab >>RNA transcript sequencing reveals inorganic sulfur compound oxidation pathways in the acidophile Acidithiobacillus ferrivorans
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2016 (English)In: FEMS Microbiology Letters, ISSN 0378-1097, E-ISSN 1574-6968, Vol. 363, no 7, article id fnw057Article in journal (Refereed) Published
Abstract [en]

Acidithiobacillus ferrivorans is an acidophile implicated in low-temperature biomining for the recovery of metals from sulfide minerals. Acidithiobacillus ferrivorans obtains its energy from the oxidation of inorganic sulfur compounds, and genes encoding several alternative pathways have been identified. Next-generation sequencing of At. ferrivorans RNA transcripts identified the genes coding for metabolic and electron transport proteins for energy conservation from tetrathionate as electron donor. RNA transcripts suggested that tetrathionate was hydrolyzed by the tetH1 gene product to form thiosulfate, elemental sulfur and sulfate. Despite two of the genes being truncated, RNA transcripts for the SoxXYZAB complex had higher levels than for thiosulfate quinone oxidoreductase (doxDA genes). However, a lack of heme-binding sites in soxX suggested that DoxDA was responsible for thiosulfate metabolism. Higher RNA transcript counts also suggested that elemental sulfur was metabolized by heterodisulfide reductase (hdr genes) rather than sulfur oxygenase reductase (sor). The sulfite produced as a product of heterodisulfide reductase was suggested to be oxidized by a pathway involving the sat gene product or abiotically react with elemental sulfur to form thiosulfate. Finally, several electron transport complexes were involved in energy conservation. This study has elucidated the previously unknown At. ferrivorans tetrathionate metabolic pathway that is important in biomining.

National Category
Microbiology
Research subject
Ecology, Microbiology
Identifiers
urn:nbn:se:lnu:diva-50210 (URN)10.1093/femsle/fnw057 (DOI)000377967800008 ()2-s2.0-84993237658 (Scopus ID)
Available from: 2016-03-04 Created: 2016-03-04 Last updated: 2018-10-24Bibliographically approved
2. Acidithiobacillus ferrivorans SS3 presents little RNA transcript response related to cold stress during growth at 8 A degrees C suggesting it is a eurypsychrophile
Open this publication in new window or tab >>Acidithiobacillus ferrivorans SS3 presents little RNA transcript response related to cold stress during growth at 8 A degrees C suggesting it is a eurypsychrophile
2016 (English)In: Extremophiles, ISSN 1431-0651, E-ISSN 1433-4909, Vol. 20, no 6, p. 903-913Article in journal (Refereed) Published
Abstract [en]

Acidithiobacillus ferrivorans is an acidophilic bacterium that represents a substantial proportion of the microbial community in a low temperature mining waste stream. Due to its ability to grow at temperatures below 15 A degrees C, it has previously been classified as 'psychrotolerant'. Low temperature-adapted microorganisms have strategies to grow at cold temperatures such as the production of cold acclimation proteins, DEAD/DEAH box helicases, and compatible solutes plus increasing their cellular membrane fluidity. However, little is known about At. ferrivorans adaptation strategies employed during culture at its temperature extremes. In this study, we report the transcriptomic response of At. ferrivorans SS3 to culture at 8 A degrees C compared to 20 A degrees C. Analysis revealed 373 differentially expressed genes of which, the majority were of unknown function. Only few changes in transcript counts of genes previously described to be cold adaptation genes were detected. Instead, cells cultured at cold (8 A degrees C) altered the expression of a wide range of genes ascribed to functions in transcription, translation, and energy production. It is, therefore, suggested that a temperature of 8 A degrees C imposed little cold stress on At. ferrivorans, underlining its adaptation to growth in the cold as well as suggesting it should be classified as a 'eurypsychrophile'.

Keywords
Extremophile, Psychrophile, Cold acclimation, Compatible solutes, Metabolism, Electron transport
National Category
Microbiology
Research subject
Ecology, Microbiology
Identifiers
urn:nbn:se:lnu:diva-59011 (URN)10.1007/s00792-016-0882-2 (DOI)000387270500009 ()27783177 (PubMedID)2-s2.0-84992386050 (Scopus ID)
Available from: 2016-12-15 Created: 2016-12-14 Last updated: 2018-09-10Bibliographically approved
3. Multi-omics reveal the lifestyle of the acidophilic, mineral-oxidizing model species Leptospirillum ferriphilumT
Open this publication in new window or tab >>Multi-omics reveal the lifestyle of the acidophilic, mineral-oxidizing model species Leptospirillum ferriphilumT
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2018 (English)In: Applied and Environmental Microbiology, ISSN 0099-2240, E-ISSN 1098-5336, Vol. 4, no 3, article id UNSP e02091-17Article in journal (Refereed) Published
Abstract [en]

Leptospirillum ferriphilum plays a major role in acidic, metal rich environments where it represents one of the most prevalent iron oxidizers. These milieus include acid rock and mine drainage as well as biomining operations. Despite its perceived importance, no complete genome sequence of this model species' type strain is available, limiting the possibilities to investigate the strategies and adaptations Leptospirillum ferriphilumT applies to survive and compete in its niche. This study presents a complete, circular genome of Leptospirillum ferriphilumT DSM 14647 obtained by PacBio SMRT long read sequencing for use as a high quality reference. Analysis of the functionally annotated genome, mRNA transcripts, and protein concentrations revealed a previously undiscovered nitrogenase cluster for atmospheric nitrogen fixation and elucidated metabolic systems taking part in energy conservation, carbon fixation, pH homeostasis, heavy metal tolerance, oxidative stress response, chemotaxis and motility, quorum sensing, and biofilm formation. Additionally, mRNA transcript counts and protein concentrations were compared between cells grown in continuous culture using ferrous iron as substrate and bioleaching cultures containing chalcopyrite (CuFeS2). Leptospirillum ferriphilumT adaptations to growth on chalcopyrite included a possibly enhanced production of reducing power, reduced carbon dioxide fixation, as well as elevated RNA transcripts and proteins involved in heavy metal resistance, with special emphasis on copper efflux systems. Finally, expression and translation of genes responsible for chemotaxis and motility were enhanced.

Place, publisher, year, edition, pages
American society for microbiology, 2018
National Category
Microbiology
Research subject
Ecology, Microbiology; Ecology, Microbiology
Identifiers
urn:nbn:se:lnu:diva-69199 (URN)10.1128/AEM.02091-17 (DOI)000423770000018 ()
Available from: 2017-12-13 Created: 2017-12-13 Last updated: 2018-10-24Bibliographically approved
4. Weak Iron Oxidation by Sulfobacillus thermosulfidooxidans Maintains a Favorable Redox Potential for Chalcopyrite Bioleaching
Open this publication in new window or tab >>Weak Iron Oxidation by Sulfobacillus thermosulfidooxidans Maintains a Favorable Redox Potential for Chalcopyrite Bioleaching
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2018 (English)In: Frontiers in Microbiology, ISSN 1664-302X, E-ISSN 1664-302X, Vol. 9, article id 3059Article in journal (Refereed) Published
Abstract [en]

Bioleaching is an emerging technology, describing the microbially assisted dissolution of sulfidicores that provides a more environmentally friendly alternative to many traditional metal extractionmethods, such as roasting or smelting. Industrial interest increases steadily and today, circa 15-20%of the world’s copper production can be traced back to this method. However, bioleaching of theworld’s most abundant copper mineral chalcopyrite suffers from low dissolution rates, oftenattributed to passivating layers, which need to be overcome to use this technology to its full potential.To prevent these passivating layers from forming, leaching needs to occur at a lowoxidation/reduction potential (ORP), but chemical redox control in bioleaching heaps is difficult andcostly. As an alternative, selected weak iron-oxidizers could be employed that are incapable ofscavenging exceedingly low concentrations of iron and therefore, raise the ORP just above the onsetof bioleaching, but not high enough to allow for the occurrence of passivation. In this study, wereport that microbial iron oxidation by Sulfobacillus thermosulfidooxidans meets these specifications.Chalcopyrite concentrate bioleaching experiments with S. thermosulfidooxidans as the sole ironoxidizer exhibited significantly lower redox potentials and higher release of copper compared tocommunities containing the strong iron oxidizer Leptospirillum ferriphilum. Transcriptomic responseto single and co-culture of these two iron oxidizers was studied and revealed a greatly decreasednumber of mRNA transcripts ascribed to iron oxidation in S. thermosulfidooxidans when cultured inthe presence of L. ferriphilum. This allowed for the identification of genes potentially responsible forS. thermosulfidooxidans’ weaker iron oxidation to be studied in the future, as well as underlined theneed for mechanisms to control the microbial population in bioleaching heaps

Place, publisher, year, edition, pages
Frontiers Media S.A., 2018
Keywords
redox control, microbial, bioleaching, chalcopyrite, iron oxidation, sulfobacillus, leptospirillum
National Category
Microbiology
Research subject
Ecology, Microbiology
Identifiers
urn:nbn:se:lnu:diva-77662 (URN)10.3389/fmicb.2018.03059 (DOI)000453089800001 ()30631311 (PubMedID)
Available from: 2018-09-10 Created: 2018-09-10 Last updated: 2019-01-23Bibliographically approved
5. Comparison of Boreal Acid Sulfate Soil Microbial Communities in Oxidative and Reductive Environments
Open this publication in new window or tab >>Comparison of Boreal Acid Sulfate Soil Microbial Communities in Oxidative and Reductive Environments
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2019 (English)In: Research in Microbiology, ISSN 0923-2508, E-ISSN 1769-7123Article in journal, Letter (Refereed) In press
Abstract [en]

Due to land uplift after the last ice age, previously stable Baltic Sea sulfidic sediments are becoming dry land. When these sediments are drained, the sulfide minerals are exposed to air and can release large amounts of metals and acid into the environment. This can cause severe ecological damage such as fish kills in rivers feeding the northern Baltic Sea. In this study, five sites were investigated for the occurrence of acid sulfate soils and their geochemistry and microbiology was identified. The pH and soil chemistry identified three of the areas as having classical acid sulfate soil characteristics and culture independent identification of 16S rRNA genes identified populations related to acidophilic bacteria capable of catalyzing sulfidic mineral dissolution, including species likely adapted to low temperature. These results were compared to an acid sulfate soil area that had been flooded for ten years and showed that the previously oxidized sulfidic materials had an increased pH compared to the unremediated oxidizied layers. In addition, the microbiology of the flooded soil had changed such that alkalinity producing ferric and sulfate reducing reactions had likely occurred. This suggested that flooding of acid sulfate soils mitigates their environmental impact.

Keywords
sulfide mineral; metal; sulfur; 16S rRNA gene; mitigation; wetland
National Category
Microbiology Earth and Related Environmental Sciences
Research subject
Natural Science, Environmental Science
Identifiers
urn:nbn:se:lnu:diva-77664 (URN)10.1016/j.resmic.2019.06.002 (DOI)
Available from: 2018-09-10 Created: 2018-09-10 Last updated: 2019-07-04

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