The common origin and degenerative evolution of flagella in Actinobacteria

ABSTRACT Species of the phylum Actinobacteria have long time been thought mostly non-motile and non-flagellated, in spite of their extraordinary diversity in morphology, physiology, and ecology. It remains unclear how very few actinobacterial species acquired their flagellar genes and the role of flagellar motility in the evolution of different lineages within this large phylum. Here, we performed a comprehensive phylogenomic analysis of flagellar components in all actinobacterial species, including the deepest branches of this phylum identified recently. Our results provide robust evidence that all actinobacterial flagella shared a common origin and likely evolved from their last common flagellated ancestor by vertical inheritance. Later lineages underwent massive flagellar losses with the ecological switch from aquatic to terrestrial land or host-associated environments. In addition, the actinobacterial flagella also showed degenerative evolution in terms of their composition, leading to the simplest rod known so far. Furthermore, these evolutionary changes of flagella were accompanied by noteworthy variations in the chemosensory system and c-di-GMP mediated signaling network. Overall, we present here a detailed picture of flagellar evolution in Actinobacteria, which provides new insights into the evolution of major actinobacterial lineages and previously unobserved links between flagella and other biological features. The simplest flagellar rod as a product of degenerative evolution could possibly serve as a model for future nanomachine reconstruction in synthetic biology. IMPORTANCE Flagellar motility plays an important role in the environmental adaptation of bacteria and is found in more than 50% of known bacterial species. However, this important characteristic is sparsely distributed within members of the phylum Actinobacteria, which constitutes one of the largest bacterial groups. It is unclear why this important fitness organelle is absent in most actinobacterial species and the origin of flagellar genes in other species. Here, we present detailed analyses of the evolution of flagellar genes in Actinobacteria, in conjunction with the ecological distribution and cell biological features of major actinobacterial lineages, and the co-evolution of signal transduction systems. The results presented in addition to clarifying the puzzle of sporadic distribution of flagellar motility in Actinobacteria, also provide important insights into the evolution of major lineages within this phylum. Flagellar motility plays an important role in the environmental adaptation of bacteria and is found in more than 50% of known bacterial species. However, this important characteristic is sparsely distributed within members of the phylum Actinobacteria, which constitutes one of the largest bacterial groups. It is unclear why this important fitness organelle is absent in most actinobacterial species and the origin of flagellar genes in other species. Here, we present detailed analyses of the evolution of flagellar genes in Actinobacteria, in conjunction with the ecological distribution and cell biological features of major actinobacterial lineages, and the co-evolution of signal transduction systems. The results presented in addition to clarifying the puzzle of sporadic distribution of flagellar motility in Actinobacteria, also provide important insights into the evolution of major lineages within this phylum.