Marine picocyanobacteria are the most abundant photosynthetic bacterioplankton occupying a wide range of habitats across the world’s oceans. In order to survive in such diverse habitats, these organisms have developed various mechanisms to respond to specific environmental challenges they might encounter. One such challenge for cyanobacteria is the acquisition and homeostasis of micronutrients such as Zn and Cu, especially for those organisms occupying a variable ecosystem with an erratic nutrient supply. Metallothioneins are metal-binding proteins that potentially participate in such metal homeostasis mechanisms in these marine picocyanobacteria. Metallothioneins are small, cysteine-rich proteins capable of binding multiple metal ions, and have attracted intense scientific interest since their discovery in the 1950s. Over the last decade, they have been reported in every kingdom, from prokaryotic to eukaryotic, from bacteria to plants, from worms to mammals. Eukaryotic metallothioneins have been extensively studied. However, characterisation of bacterial metallothioneins is still rare. This research focused on the coastal cyanobacterium Synechococcus sp. CC9311, which is unusual in possessing four metallothionein genes (sync_0853, sync_1081, sync_2379 and sync_2426) while most marine picocyanobacteria contain only one, or none. Three metallothioneins were comprehensively characterised using a range of analytical and biophysical techniques. Mass spectrometry and nuclear magnetic resonance studies combined with homology modelling led to an unambiguous Zn3Cys8His cluster for BmtA0853, a highly likely Zn4Cys9His2 cluster for BmtA2426, and three possible configurations for BmtA1081. Analysis of gene expression profiles revealed that the four metallothioneins selectively participated in zinc scavenging, zinc homeostasis, cadmium detoxification, or protection from oxidising conditions. Growth of Synechococcus sp. CC9311 under various metal treatments also revealed that this coastal strain has developed a metal intensive physiology compared to the open ocean strain Synechococcus sp. WH8102.