The reduced genome of a heritable symbiont from an ectoparasitic feather feeding louse

Abstract

Background: Feather feeding lice are abundant and diverse ectoparasites that complete their entire life cycle on an avian host. The principal or sole source of nutrition for these lice is feathers. Feathers appear to lack four amino acids that the lice would require to complete development and reproduce. Several insect groups have acquired heritable and intracellular bacteria that can synthesize metabolites absent in an insect's diet, allowing insects to feed exclusively on nutrient-poor resources. Multiple species of feather feeding lice have been shown to harbor heritable and intracellular bacteria. We expected that these bacteria augment the louse's diet with amino acids and facilitated the evolution of these diverse and specialized parasites. Heritable symbionts of insects often have small genomes that contain a minimal set of genes needed to maintain essential cell functions and synthesize metabolites absent in the host insect's diet. Therefore, we expected the genome of a bacterial endosymbiont in feather lice would be small, but encode pathways for biosynthesis of amino acids.

Results: We sequenced the genome of a bacterial symbiont from a feather feeding louse (Columbicola wolffhuegeli) that parasitizes the Pied Imperial Pigeon (Ducula bicolor) and used its genome to predict metabolism of amino acids based on the presence or absence of genes. We found that this bacterial symbiont has a small genome, similar to the genomes of heritable symbionts described in other insect groups. However, we failed to identify many of the genes that we expected would support metabolism of amino acids in the symbiont genome. We also evaluated other gene pathways and features of the highly reduced genome of this symbiotic bacterium.

Conclusions: Based on the data collected in this study, it does not appear that this bacterial symbiont can synthesize amino acids needed to complement the diet of a feather feeding louse. Our results raise additional questions about the biology of feather chewing lice and the roles of symbiotic bacteria in evolution of diverse avian parasites.

Keywords: Endosymbiont; Genome reduction; Keratin; Metabolic complementation; Phthiraptera.

Fig. 1

Phylogenetic relationship of the Columbicola wolffhuegeli endosymbiont to other γ-proteobacteria. Tree is based on nhPhyML search that started from our initial maximum-likelihood tree obtained from a RAxML search. Values at nodes represent selected bootstrap values obtained from the initial RAxML starting tree. Red taxon labels represent the C. wolffhuegeli endosymbiont described in this study and the two taxa that were used in our comparative genomics study. Ca. Candidatus

Fig. 2

Amino acid and B-vitamin predicted biosynthensis pathways in the Columbicola wolffhuegeli endosymbiont (CWE) genome, blood sucking louse endosymbiont Candidatus Riesia pediculicola USDA (Riesia) genome and phloem feeding insect endosymbiont Buchnera aphidicola APS (Buchnera) genome. Solid boxes indicate pathways is predicted to be intact, gradient boxes indicate the pathway is incomplete, and empty boxes indicate the pathway is absent

Fig. 3

Comparison of total genes by functional category between Columbicola wolffhuegeli endosymbiont and two other endosymbionts based on metabolic predictions. (Top) Comparison of C. wolffhuegeli endosymbiont and an endosymbiont from a blood feeding louse (Candidatus Riesia pediculicola). (Bottom) Comparison of C. wolffhuegeli endosymbiont and an endosymbiont from a phloem feeding insect (Buchera aphidicola). Red and green bars indicate private functions and blue bars indicate functions found in both genomes being compared. Metab. Metabolism, CWE Columbicola wolffhuegeli endosymbiont

Fig. 4

Comparison of γ-proteobacteria genomes by size and base composition. Colors red and green indicate if the genome was derived from an insect endosymbiont or some other type of bacteria. Red indicates the genome of the Columbicola wolffhuegeli endosymbiont (CWE)