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Multi-omics reveal the lifestyle of the acidophilic, mineral-oxidizing model species Leptospirillum ferriphilumT
Linnaeus University, Faculty of Health and Life Sciences, Department of Biology and Environmental Science. (Ctr Ecol & Evolut Microbial Model Syst EEMiS)ORCID iD: 0000-0003-0021-2452
University of Luxembourg, Luxembourg.
Universität Duisburg-Essen, Germany.
Ruhr Universität Bochum, Germany.
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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. Vol. 4, no 3, article id UNSP e02091-17
National Category
Microbiology
Research subject
Ecology, Microbiology; Ecology, Microbiology
Identifiers
URN: urn:nbn:se:lnu:diva-69199DOI: 10.1128/AEM.02091-17ISI: 000423770000018OAI: oai:DiVA.org:lnu-69199DiVA, id: diva2:1165354
Available from: 2017-12-13 Created: 2017-12-13 Last updated: 2018-10-24Bibliographically approved
In thesis
1. Function and Adaptation of Acidophiles in Natural and Applied Communities
Open this publication in new window or tab >>Function and Adaptation of Acidophiles in Natural and Applied Communities
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
Acidophiles, Biomining, Psychrophiles, Adaptation, Acid Sulfate Soil, Redox Control
National Category
Ecology
Research subject
Natural Science, Ecology
Identifiers
urn:nbn:se:lnu:diva-77666 (URN)978-91-88761-94-1 (ISBN)978-91-88761-95-8 (ISBN)
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

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Christel, StephanBuetti-Dinh, AntoineDopson, Mark

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