From biomolecules to biogeochemistry: Exploring the interaction of an indigenous bacterium with gold

Santonu K Sanyal; Tara Pukala; Parul Mittal; Frank Reith; Joël Brugger; Barbara Etschmann; Jeremiah Shuster

doi:10.1016/j.chemosphere.2023.139657

From biomolecules to biogeochemistry: Exploring the interaction of an indigenous bacterium with gold

Chemosphere. 2023 Oct:339:139657. doi: 10.1016/j.chemosphere.2023.139657. Epub 2023 Aug 3.

Authors

Santonu K Sanyal¹, Tara Pukala², Parul Mittal³, Frank Reith, Joël Brugger⁴, Barbara Etschmann⁴, Jeremiah Shuster⁵

Affiliations

¹ School of Earth, Atmosphere and Environment, Monash University, Clayton, Victoria, 3800, Australia. Electronic address: santonu.sanyal@monash.edu.
² Adelaide Proteomics Centre, The University of Adelaide, Adelaide, South Australia, 5001, Australia; School of Physics, Chemistry and Earth Sciences, The University of Adelaide, Adelaide, South Australia, 5001, Australia.
³ Adelaide Proteomics Centre, The University of Adelaide, Adelaide, South Australia, 5001, Australia.
⁴ School of Earth, Atmosphere and Environment, Monash University, Clayton, Victoria, 3800, Australia.
⁵ Department of Earth Sciences, Western University, London, Ontario, N6A 3K7, Canada.

PMID: 37543229
DOI: 10.1016/j.chemosphere.2023.139657

Abstract

Specialised microbial communities colonise the surface of gold particles in soils/sediments, and catalyse gold dissolution and re-precipitation, thereby contributing to the environmental mobility and toxicity of this 'inert' precious metal. We assessed the proteomic and physiological response of Serratia proteamaculans, the first metabolically active bacterium enriched and isolated directly from natural gold particles, when exposed to toxic levels of soluble Au³⁺ (10 μM). The results were compared to a metal-free blank, and to cultures exposed to similarly toxic levels of soluble Cu²⁺ (0.1 mM); Cu was chosen for comparison because it is closely associated with Au in nature due to similar geochemical properties. A total of 273 proteins were detected from the cells that experienced the oxidative effects of soluble Au, of which 139 (51%) were upregulated with either sole expression (31%) or had synthesis levels greater than the Au-free control (20%). The majority (54%) of upregulated proteins were functionally different from up-regulated proteins in the bacteria-copper treatment. These proteins were related to broad functions involving metabolism and biogenesis, followed by cellular process and signalling, indicating significant specificity for Au. This proteomic study revealed that the bacterium upregulates the synthesis of various proteins related to oxidative stress response (e.g., Monothiol-Glutaredoxin, Thiol Peroxidase, etc.) and cellular damage repair, which leads to the formation of metallic gold nanoparticles less toxic than ionic gold. Therefore, indigenous bacteria may mediate the toxicity of Au through two different yet simultaneous processes: i) repairing cellular components by replenishing damaged proteins and ii) neutralising reactive oxygen species (ROS) by up-regulating the synthesis of antioxidants. By connecting the fields of molecular bacteriology and environmental biogeochemistry, this study is the first step towards the development of biotechnologies based on indigenous bacteria applied to gold bio-recovery and bioremediation of contaminated environments.

Keywords: Biogeochemistry; Copper; Gold; Gold-associated proteins; Microbe-mineral interaction; Serratia proteamaculans.

MeSH terms

Bacteria
Copper / toxicity
Gold* / chemistry
Gold* / toxicity
Metal Nanoparticles* / chemistry
Metal Nanoparticles* / toxicity
Proteomics

Substances

Gold
Copper