Streptococcus pneumoniae is the world's foremost bacterial pathogen. It is a causative agent of pneumonia, meningitis, and otitis media, and is responsible for more than one million deaths annually. Acquisition of first-row transition metal ions from the human host is crucial to its ability to cause invasive disease. These metal ions are scavenged from the host by the integral membrane ATP-binding cassette (ABC) permeases and here we show how these transporters facilitate S. pneumoniae transition metal homeostasis. Our work has shown that manganese ions, which are essential for virulence and oxidative stress management, are specifically acquired by the ABC permease, PsaBCA, despite the inability of the metal-receptor protein, PsaA, to discriminate between first row transition metal ions. Here, we show how PsaA achieves functional specificity for metal ions via a novel ‘spring-hammer’ binding modality, in which protein conformational changes are coupled to coordination chemistry at the metal binding site of the protein. Manganese ions, which are coordinated by PsaA in a sub-optimal manner, can be released into the Psa permease, thus permitting import into the pathogen. By contrast, zinc ions, which are optimally coordinated by PsaA, cannot be released and inhibit the function of the permease complex. Thus, the ability of PsaA to specifically release only manganese ions, despite its promiscuity for a range of divalent cations, enables the PsaBCA permease to achieve functional selectivity for manganese transport. Maintaining specific acquisition of poorly abundant metal ions, such as manganese, is crucial in the context of the host-pathogen interaction where the chemical composition of the environment can change rapidly during the course of infection. Here, we show that the relative abundance of zinc ions in the host exerts a dramatic effect on infection by S. pneumoniae and directly influences manganese acquisition and disease burden. Collectively, these findings provide new insights into the roles of transition metal ions at the host-pathogen interface.