Affiliation:
1. Department of Parasitology, Faculty of Science, University of South Bohemia , České Budějovice, Czechia
2. Institute of Infection, Veterinary and Ecological Sciences, University of Liverpool , Liverpool, United Kingdom
3. Institute of Parasitology, Biology Centre, ASCR, v.v.i. , České Budějovice, Czechia
Abstract
ABSTRACT
Arsenophonus
is a widespread insect symbiont with life strategies that vary from parasitism to obligate mutualism. In insects living exclusively on vertebrate blood, mutualistic
Arsenophonus
strains are presumed to provide B vitamins missing in the insect host diet. Hippoboscidae, obligate blood feeders related to tsetse flies, have been previously suggested to have acquired
Arsenophonus
symbionts in several independent events. Based on comparative genomic analyses of 11 Hippoboscidae-associated strains, 9 of them newly assembled, we reveal a wide range of their genomic characteristics and phylogenetic affiliations. Phylogenetic patterns and genomic traits split the strains into two different types. Seven strains display characteristics of obligate mutualists with significantly reduced genomes and long phylogenetic branches. The remaining four strains cluster on short branches, and their genomes resemble those of free-living bacteria or facultative symbionts. Both phylogenetic positions and genomic traits indicate that evolutionary history of the Hippoboscidae-
Arsenophonus
associations is a mixture of short-term coevolutions with at least four independent origins. The comparative approach to a reconstruction of B vitamin pathways across the available
Arsenophonus
genomes has produced two kinds of patterns. On one hand, it indicates the different importance of individual B vitamins in the host-symbiont interaction. While some (riboflavin, pantothenate, and folate) seem to be synthesized by all Hippoboscidae-associated obligate symbionts, pathways for others (thiamine, nicotinamide, and cobalamin) are mostly missing. On the other hand, the broad comparison has produced patterns that can serve as bases for further assessments of the pathways’ completeness and functionality.
IMPORTANCE
Insects that live exclusively on vertebrate blood utilize symbiotic bacteria as a source of essential compounds, e.g., B vitamins. In louse flies, the most frequent symbiont originated in genus
Arsenophonus
, known from a wide range of insects. Here, we analyze genomic traits, phylogenetic origins, and metabolic capacities of 11
Arsenophonus
strains associated with louse flies. We show that in louse flies,
Arsenophonus
established symbiosis in at least four independent events, reaching different stages of symbiogenesis. This allowed for comparative genomic analysis, including convergence of metabolic capacities. The significance of the results is twofold. First, based on a comparison of independently originated
Arsenophonus
symbioses, it determines the importance of individual B vitamins for the insect host. This expands our theoretical insight into insect-bacteria symbiosis. The second outcome is of methodological significance. We show that the comparative approach reveals artifacts that would be difficult to identify based on a single-genome analysis.
Funder
Grantová Agentura České Republiky
Publisher
American Society for Microbiology
Subject
Computer Science Applications,Genetics,Molecular Biology,Modeling and Simulation,Ecology, Evolution, Behavior and Systematics,Biochemistry,Physiology,Microbiology