Abstract Large surface proteins in bacteria serve important functions in aggregation, biofilm formation and cell interaction processes. In Apilactobacillus kunkeei, a defensive symbiont of the honeybee Apis mellifera, as much as 6% of the 1.5 Mb genome consists of five consecutive genes for extracellular surface proteins of 3,000-8,000 amino acids, named Giant1-5. Here, we predict the structures of these proteins and provide a study of their origin and evolution. The structure predictions suggest that the Giant1-4 proteins contain a β-solenoid domain at their N-terminal ends with similarity to the β-solenoid domain in serine-rich repeat proteins, which mediates binding to glycoproteins, polysaccharides and epithelial cells. Phylogenetic analyses based on the β-solenoid domains of the Giant1-3 proteins indicate sequence exchange between two genera of otherwise distantly related obligate fructophilic lactic acid bacteria, while the diversification of the positional homologs of the giant1-3 genes in the A. kunkeei population is mostly due to short, intra-genic recombination events. Genes for the Giant4-5 proteins were only identified in A. kunkeei and two closely related bacterial species, suggesting that they were added to the giant gene cluster more recently. The phylogenetic analyses indicate co-evolution of the giant4-5 genes in A. kunkeei, and the near sequence identity of one of the two giant4-5 subtypes correlates with predicted recombination events that span across both genes. Our findings provide new insights into the evolution of very large surface proteins in the bacterial ecosystem adapted to the carbohydrate-rich growth niches provided by bees, their food sources and food products.
Pedersen et al. (Wed,) studied this question.