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Front. Microbiol. | doi: 10.3389/fmicb.2019.00592

Proteomics reveal enhanced oxidative stress responses and metabolic adaptation in Acidithiobacillus ferrooxidans biofilm cells on pyrite

 Soeren Bellenberg1, 2*,  Dieu Huynh3, Ansgar Poetsch4,  Wolfgang Sand1, 3, 5 and  Mario Vera6*
  • 1Fakultät für Chemie, Universität Duisburg-Essen, Germany
  • 2Centre for Ecology and Evolution in Microbial Model Systems, Linnaeus University, Sweden
  • 3Freiberg University of Mining and Technology, Germany
  • 4University of Plymouth, United Kingdom
  • 5Donghua University, China
  • 6Pontificia Universidad Católica de Chile, Chile

Reactive oxygen species (ROS) cause oxidative stress and growth inhibition by inactivation of essential enzymes, DNA and lipid damage in microbial cells. Acid mine drainage (AMD) ecosystems are characterized by low pH values, enhanced levels of metal ions and low species abundance. Furthermore, metal sulfides, such as pyrite and chalcopyrite, generate extracellular ROS upon exposure to acidic water. Consequently, oxidative stress management is especially important in acidophilic leaching microorganisms present in industrial biomining operations, especially when forming biofilms on metal sulfides. Several adaptive mechanisms have been described, but the molecular repertoire of responses upon exposure to pyrite and the presence of ROS are not thoroughly understood in acidophiles. In this study the impact of the addition of H2O2 on iron oxidation activity in Acidithiobacillus ferrooxidans DSM 14882T was investigated. Iron(II)- or sulfur-grown cells showed a higher sensitivity towards H2O2 than pyrite-grown ones. In order to elucidate which molecular responses may be involved, we used shot-gun proteomics and compared proteomes of cells grown with iron(II)-ions against biofilm cells, grown for five days in presence of pyrite as sole energy source. In total 1157 proteins were identified. 213 and 207 ones were found to have increased levels in iron(II)-grown or pyrite-biofilm cells, respectively. Proteins associated with inorganic sulfur compound (ISC) oxidation were among the latter. In total, 80 proteins involved in ROS degradation, thiol redox regulation, macromolecule repair mechanisms, biosynthesis of antioxidants, as well as metal and oxygen homeostasis were found. 42 of these proteins had no significant changes in abundance, while 30 proteins had increased levels in pyrite-biofilm cells. New insights in ROS mitigation strategies, such as importance of globins for oxygen homeostasis and prevention of unspecific reactions of free oxygen that generate ROS are presented for A. ferrooxidans biofilm cells. Furthermore, proteomic analyses provide insights in adaptations of carbon fixation and oxidative phosphorylation pathways under these two growth conditions.

Keywords: Acidithiobacilli, Acidithiobacillus ferrooxidans, Proteomics, biofilm formaiton, Oxidative Stress, Pyrite (FeS2), reactive oxygen species, bioleaching, biomining, acid mine drainage

Received: 02 Nov 2018; Accepted: 08 Mar 2019.

Edited by:

Gloria P. Levicán, Universidad de Santiago de Chile, Chile

Reviewed by:

Weimin Zeng, Central South University, China
Laura Castro, Department of Materials Science and Metallurgical Engineering, Complutense University of Madrid, Spain  

Copyright: © 2019 Bellenberg, Huynh, Poetsch, Sand and Vera. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

* Correspondence:
Dr. Soeren Bellenberg, Fakultät für Chemie, Universität Duisburg-Essen, Duisburg, North Rhine-Westphalia, Germany,
Dr. Mario Vera, Pontificia Universidad Católica de Chile, Santiago, 3580000, Santiago Metropolitan Region (RM), Chile,