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Zinc is an essential micronutrient required for proper structure and function of many proteins. Bacteria regularly encounter zinc depletion and have evolved diverse mechanisms to continue growth when zinc is limited, including the expression of zinc-independent paralogs of zinc-binding proteins. Mycobacteria have a conserved operon encoding four zinc-independent alternative ribosomal proteins (AltRPs) that are expressed when zinc is depleted. It is unknown if mycobacterial AltRPs replace their primary paralogs in the ribosome and maintain protein synthesis under zinc-limited conditions, and if such replacements contribute to their physiology. This study shows that AltRPs from  Mycobacterium smegmatis  are essential for growth when zinc ion is scarce. Specifically, the deletion mutant of this operon (Δ altRP ) is unable to grow in media containing a high-affinity zinc chelator, while growth of the wild type strain is unaffected under the same conditions. However, when zinc is gradually depleted during growth in zinc-limited medium, the Δ altRP  mutant maintains the same growth rate as seen for the wild type strain. In contrast to  M .  smegmatis  grown with sufficient zinc supplementation that forms shorter cells when transitioning from logarithmic to stationary phase,  M .  smegmatis  deficient for zinc elongates after the expression of AltRPs in late logarithmic phase. These zinc-depleted bacteria also exhibit a remarkable morphology characterized by a condensed chromosome, increased number of polyphosphate granules, and distinct appearance of lipid bodies and the cell wall compared to the zinc-replete cells. However, the Δ altRP  cells fail to elongate and transition into the zinc-limited morphotype, resembling the wild type zinc-replete bacteria instead. Therefore, the  altRP  operon in  M .  smegmatis  has a vital role in continuation of growth when zinc is scarce and in triggering specific morphogenesis during the adaptation to zinc limitation, suggesting that AltRPs can functionally replace their zinc-dependent paralogs, but also contribute to mycobacterial physiology in a unique way.

Alternative ribosomal proteins are required for growth and morphogenesis of Mycobacterium smegmatis under zinc limiting conditions