Abstract

Acidithiobacillus thiooxidans is one of the most studied biomining species, highlighting its ability to oxidize reduced inorganic sulfur compounds, coupled with its elevated capacity to live under an elevated concentration of heavy metals. In this work, using an in silico semi-automatic genome scale approach, two biological networks for A. thiooxidans Licanantay were generated: (i) An affinity transcriptional regulatory network composed of 42 regulatory family genes and 1,501 operons (57% genome coverage) linked through 2,646 putative DNA binding sites (arcs), (ii) A metabolic network reconstruction made of 523 genes and 1,203 reactions (22 pathways related to biomining processes). Through the identification of confident connections between both networks (V-shapes), it was possible to identify a sub-network of transcriptional factor (34 regulators) regulating genes (61 operons) encoding for proteins involved in biomining-related pathways. Network analysis suggested that transcriptional regulation of biomining genes is organized into different modules. The topological parameters showed a high hierarchical organization by levels inside this network (14 layers), highlighting transcription factors CysB, LysR, and IHF as complex modules with high degree and number of controlled pathways. In addition, it was possible to identify transcription factor modules named primary regulators (not controlled by other regulators in the sub-network). Inside this group, CysB was the main module involved in gene regulation of several bioleaching processes. In particular, metabolic processes related to energy metabolism (such as sulfur metabolism) showed a complex integrated regulation, where different primary regulators controlled several genes. In contrast, pathways involved in iron homeostasis and oxidative stress damage are mainly regulated by unique primary regulators, conferring Licanantay an efficient, and specific metal resistance response. This work shows new evidence in terms of transcriptional regulation at a systems level and broadens the study of bioleaching in A. thiooxidans species.

Highlights

  • Acidithiobacillus thiooxidans belongs to the Acidithiobacillia class of proteobacteria (Williams and Kelly, 2013)

  • The third class corresponded to local regulators, highlighting the proteins Fur and CueR, controllers of metal homeostasis and oxidative stress damage, two main cellular processes considering the mining environment where Licanantay was isolated (Latorre et al, 2016), during oxidative dissolution, autotrophic organisms are able to use ferrous iron and reduced sulfur compounds as electron donors

  • For A. thiooxidans species, sulfur metabolism plays a crucial role in the acquisition of electrons for their autotrophic growth (Wang et al, 2018)

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Summary

Introduction

Acidithiobacillus thiooxidans belongs to the Acidithiobacillia class of proteobacteria (Williams and Kelly, 2013). It is an autotrophic Gram-negative bacterium that obtains energy from the oxidation of reduced inorganic sulfur compounds (RISC). A. thiooxidans Licanantay was presented as one of the most relevant participants of a consortium of five natural copper-bioleaching acidophilic bacteria (Latorre et al, 2016). This bacterium was isolated directly from a copper mine in the north of Chile. Licanantay has an elevated capacity to survive under elevated concentrations of copper, arsenic, and chloride in relation to other biomining species and produces high quantities of glutathione (Martínez et al, 2013), a crucial metabolite directly or indirectly related to iron and RISC oxidation in bioleaching species

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