Protein subcellular relocalization and function of duplicated flagellar calcium binding protein genes in honey bee trypanosomatid parasite.

The honey bee trypanosomatid parasite, Lotmaria passim, contains two genes that encode the flagellar calcium binding protein (FCaBP) through tandem duplication in its genome. FCaBPs localize in the flagellum and entire body membrane of L. passim through specific N-terminal sorting sequences. This finding suggests that this is an example of protein subcellular relocalization resulting from gene duplication, altering the intracellular localization of FCaBP. However, this phenomenon may not have occurred in Leishmania, as one or both of the duplicated genes have become pseudogenes. Multiple copies of the FCaBP gene are present in several Trypanosoma species and Leptomonas pyrrhocoris, indicating rapid evolution of this gene in trypanosomatid parasites. The N-terminal flagellar sorting sequence of L. passim FCaBP1 is in close proximity to the BBSome complex, while that of Trypanosoma brucei FCaBP does not direct GFP to the flagellum in L. passim. Deletion of the two FCaBP genes in L. passim affected growth and impaired flagellar morphogenesis and motility, but it did not impact host infection. Therefore, FCaBP represents a duplicated gene with a rapid evolutionary history that is essential for flagellar structure and function in a trypanosomatid parasite. Author summary: Protein subcellular relocalization (PSR) was proposed as a mechanism for the functional divergence and retention of duplicate genes. We explored this hypothesis using flagellar calcium binding protein (FCaBP) genes duplicated in many trypanosomatid parasites. FCaBPs localize in the flagellum and entire body membrane of honey bee trypanosomatid parasite, Lotmaria passim through specific N-terminal sorting sequences. However, this is not common with all trypanosomatid parasites since one or both of the duplicated genes have become pseudogenes in Leishmania. N-terminal flagellar sorting sequence of FCaBP1 interacts with BBSome complex, and thus they must have co-evolved in each trypanosomatid species. FCaBPs are essential for the normal growth, flagellar morphogenesis, and motility but not host infection of L. passim. Our findings demonstrate that duplicated FCaBP genes have undergone PSR by changing amino acids in the N-terminal end with some but not all trypanosomatid parasites. In the parasites with multiple FCaBP genes, they play critical roles for the growth control as well as flagellar structure and function. [ABSTRACT FROM AUTHOR]