The Diversity and Function of Bacteria Enriched from Gold Particles: Understanding Bacterial Contribution to Biogeochemical Cycling of Gold

Abstract

In natural environments, gold is dissolved (oxidized), dispersed, and reconcentrated (reduced and aggregated). Collectively, these processes constitute the biogeochemical cycle of gold, which can be catalysed by bacteria, and have been interpreted from the characterisation of gold particles that have undergone (bio)transformation. Therefore, the primary focus of this study is to explore the diversity and function of bacteria residing on gold particles to understand their influence on particle structure and chemistry and hence gold biogeochemical cycling. In doing so, both culture-independent (direct amplification of bacterial 16S rDNA gene from particles) and dependent (enrichment of viable bacteria from particles) techniques were applied to get a comprehensive overview of the composition of microbial communities on gold particles. Diverse bacterial species belonging to different phyla were detected on gold particles, which was consistent with previous studies. The culture-independent approach provided a record of both past and present bacterial existence on gold particles, whereas, the culture-dependent approach enriched viable bacteria living on gold particles at the time of sampling. The detection and enrichment of bacteria from gold particles indicated that on Earth’s surficial environment gold particles could provide a solid substrate for bacterial colonisation. The biochemical activity of these bacteria, along with other environmental conditions, create microenvironments on gold particle surfaces (i.e. polymorphic layers) which promote particle biotransformation. The microstructures (porous textures and pure gold nanoparticles) on gold particle surfaces were interpreted as “products” of past biogeochemical processes (gold dissolution and precipitation). By analysing gold particle structure, chemistry and secondary gold concentration in the soil, gold biogeochemical cycling was estimated to be 1.60 × 10-9 M year-1 and was attributed, in part, to the viable bacteria living on the surface of those particles. The dissolution of particles during biogeochemical transformation can produce toxic soluble Au complexes thereby creating an “extreme” microenvironment. In this study, Au-tolerant bacteria were enriched (using a soluble Au concentration equivalent to the kinetic estimate) and were taxonomically diverse. This provides in-vitro evidence that gold biogeochemical cycling could act as a selective pressure on bacteria living on particles undergoing biotransformation. As a result, Au-tolerant bacteria are selected over time. The physiology, genomic, and functional characterisation of Au-tolerant bacteria demonstrated that these bacteria possess the ability to reduce cytotoxic soluble Au to gold nanoparticles (i.e. gold biomineralisation), harbour various types of genes (heavy-metal resistance, general-stress tolerance, and metabolic genes), and employ multiple mechanisms to mediate the toxicity of soluble Au. Therefore, Autolerant bacteria can survive gold biogeochemical cycling as well as catalyse particle biotransformation. Additionally, this present study also demonstrated that heavy-metal contamination (derived from anthropogenic activities) alters the natural gold biogeochemical cycling and modifies the dynamics of microbe-gold interactions. Mercury contamination in soils can directly influence gold particle structure by “erasing” evidence of past biogeochemical processes that increase the gold purity on the outer surface of particles. Conversely, mercury and other heavy metals could selectively enrich heavy-metal resistant bacteria on gold particles. Bacteria with these functional capabilities could amplify gold biogeochemical cycling. Overall, the thesis highlights the diversity and function of bacteria occurring on the surface of gold particles and how these bacteria could contribute to particle transformation. Moreover, this study provides greater insight on bacteria-gold interactions and expands our understanding of gold biogeochemistry in natural to engineered systems.