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Anaerobic Sulfur Metabolism Coupled to Dissimilatory Iron Reduction in the Extremophile Acidithiobacillus ferrooxidans
Center for Bioinformatics and Genome Biology, Fundacion Ciencia y Vida, Santiago and Depto. Ciencias Biologicas, Facultad de Ciencias Biologicas, Universidad Andres Bello, Santiago, Chile.
Umeå University, Faculty of Science and Technology, Department of Molecular Biology (Faculty of Science and Technology).
CNRS and Aix-Marseille Université, IMM, Plateforme Transcriptome, 13009 Marseille, France.
College of Natural Sciences, Bangor University, Bangor LL57 2UW, U.K..
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2013 (English)In: Applied and Environmental Microbiology, ISSN 0099-2240, E-ISSN 1098-5336, Vol. 79, no 7, 2172-2181 p.Article in journal (Refereed) Published
Abstract [en]

Gene transcription (microarrays) and protein levels (proteomics) were compared in cultures of the acidophilic chemolithotroph Acidithiobacillus ferrooxidans grown on elemental sulfur as the electron donor under aerobic and anaerobic conditions, using either molecular oxygen or ferric iron as the electron acceptor, respectively. No evidence supporting the role of either tetrathionate hydrolase or arsenic reductase in mediating the transfer of electrons to ferric iron (as suggested by previous studies) was obtained. In addition, no novel ferric iron reductase was identified. However, data suggested that sulfur was disproportionated under anaerobic conditions, forming hydrogen sulfide via sulfur reductase and sulfate via heterodisulfide reductase and ATP sulfurylase. Supporting physiological evidence for H2S production came from the observation that soluble Cu2+ included in anaerobically incubated cultures was precipitated (seemingly as CuS). Since H2S reduces ferric iron to ferrous in acidic medium, its production under anaerobic conditions indicates that anaerobic iron reduction is mediated, at least in part, by an indirect mechanism. Evidence was obtained for an alternative model implicating the transfer of electrons from S-0 to Fe3+ via a respiratory chain that includes a bc(1) complex and a cytochrome c. Central carbon pathways were upregulated under aerobic conditions, correlating with higher growth rates, while many Calvin-Benson-Bassham cycle components were upregulated during anaerobic growth, probably as a result of more limited access to carbon dioxide. These results are important for understanding the role of A. ferrooxidans in environmental biogeochemical metal cycling and in industrial bioleaching operations.

Place, publisher, year, edition, pages
American Society for Microbiology , 2013. Vol. 79, no 7, 2172-2181 p.
National Category
URN: urn:nbn:se:umu:diva-60633DOI: 10.1128/AEM.03057-12ISI: 000316183500008OAI: diva2:561758

Originally published in thesis in manuscript form

Available from: 2012-10-22 Created: 2012-10-22 Last updated: 2013-04-25Bibliographically approved
In thesis
1. Growth and survival of Acidithiobacilli in Acidic, metal rich environments
Open this publication in new window or tab >>Growth and survival of Acidithiobacilli in Acidic, metal rich environments
2012 (English)Doctoral thesis, comprehensive summary (Other academic)
Alternative title[sv]
Tillväxt och överlevnad av Acidithiobacilli i sura, metallrika miljöer
Abstract [en]

Acidithiobacilli are acidophilic microorganisms that play important roles in many natural processes such as acidification of the environment, influencing metal mobility, and impacting on global sulfur and iron cycles. Due to their distinct metabolic properties they can be applied in the industrial extraction of valuable metals. Acidithiobacilli thrive in an environment which is extremely acidic and usually low in organic carbon but highly polluted with metals. In the quest to gain insight into how these microorganisms can thrive in their extreme environment, relevant facets of metabolism, metal resistance, and pH homeostasis were exploredwith the focus on two model organisms,

Acidithiobacillus caldus and Acidithiobacillus ferrooxidans. Understanding these fundamental aspects of an acidophilic lifestyle will help to eventually control detrimental effects on the environment due to acidification and metal pollution as well as improving metal extraction utilizing acidophilic microorganisms.

Bioinformatics can give information about the genetic capacity of an organism. Likewise, ‘omics’ techniques, such as transcriptomics and proteomics to study gene transcription profiles and differentially expressed proteins canyield insights into general responses as well as giving clues regarding specific mechanisms for adaptation to life in extreme environments. This approach was used to investigate the sulfur metabolism of

At. caldus which is an important sulfur oxidizer for industrial metal extraction. It was found that sulfur oxidation pathways were diverse within acidithiobacilli and a model of At. caldus sulfur oxidation was proposed. Furthermore, At. ferrooxidans anaerobic sulfur oxidation coupled to ferric iron reduction was studied which can be of importance for industrial processes. It was shown that anaerobic sulfur oxidation was, at least in part, indirectly coupled to ferric iron reduction via sulfide generation. Moreover, metal toxicity and resistance mechanisms in acidophiles are of major interest. Thus, zinc toxicity in three model organisms, At. caldus, Acidimicrobium ferrooxidans, and ‘Ferroplasma acidarmanus’, was explored. An important finding was that the speciation of metals and other chemical influences were of great importance for zinc toxicity in acidophiles. Additionally, the three organisms showed distinct responses to elevated zinc levels. Finally, the response of At. caldus to various suboptimal growth pH was evaluated to gain insights into pH homeostasis mechanisms. The results indicated that At. caldus used acid resistance mechanisms similar to those described for neutrophilic microorganisms. Analysis of fatty acid profiles demonstrated an active modulation of the cyctoplasmic membrane in response to proton concentration, likely resulting in a more rigid membrane at lower pH.

Place, publisher, year, edition, pages
Umeå: Umeå Universitet, 2012. 70 p.
National Category
urn:nbn:se:umu:diva-60439 (URN)978-91-7459-474-4 (ISBN)
Public defence
2012-11-23, NUS - Norrlands universitetssjukhus, 933 Unod B9, Norrlands universitetssjukhus, Umeå, 09:00
Available from: 2012-11-02 Created: 2012-10-11 Last updated: 2012-10-23Bibliographically approved

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Mangold, StefanieDopson, Mark
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