Involvement of the cyanobacterial type IV pilus assembly complex in protein secretion

Protein secretion is a fundamental cellular function in all kingdoms of life. Components of bacterial type II protein secretion (T2S) systems share high homology with those of the type IV pilus (T4P) assembly systems, however, studies of numerous heterotrophic bacteria support distinct compositions and functions of the T2S and T4P complexes. Analyses of the exoproteomes of the cyanobacterium Synechococcus elongatus PCC7942 and its T4P-mutants revealed that many extracellular proteins are less abundant in the mutants’ exoproteomes compared to that of the wild-type. Moreover, bioinformatics analysis indicated that cyanobacteria possess only a single set of genes encoding T2S/T4P components. All together, these findings support involvement of the T4P apparatus in protein secretion. To test this hypothesis, we fused a nano-luciferase enzyme to the N-terminal secretion sequence of a protein that is less abundant in the exoproteomes of T4P-mutants compared to wild-type. The analysis revealed massive nano-luciferase secretion in wild-type but substantially reduced levels in T4P-mutants, thereby assigning a secretion function to the T4P complex. Such “two-in-one” function may provide cells with the benefits of genome streamlining while allowing expression of a versatile complex engaged in both pilus assembly and protein secretion.