Microbial metal physiology: ions to ecosystems

Life depends on metal ions. The levels of metal ions vary widely across environments; many areas of the open ocean are chronically metal-limited, whereas other natural and human-affected environments have exceptionally high metal concentrations. Within the human host, the fitness of commensal and pathogenic microorganisms can be constrained by both metal limitation and intoxication. Limitation occurs when metals are deficient or in forms not suitable for import. Conversely, metal excess can lead to toxicity; microorganisms then rely on metal export to maintain suitable intracellular levels. Metalloregulatory systems play a central part in enabling microorganisms to acclimate to changes in metal availability. The analysis of metalloregulators and their regulons unveils physiologically relevant transport and trafficking functions, reveals processes affected by metal imbalance and provides insights into intracellular metal pools. In this Review, I explore the key processes of metal transport, trafficking, storage and regulation. I next highlight selected microorganisms that illustrate how to thrive in environments that are chronically or transiently metal-limited, or where high metal levels are toxic. A detailed understanding of microbial metal physiology can be harnessed to improve the health of diverse ecosystems, for bioremediation and biomining, and to restrict the growth of bacterial pathogens.