Nejvíce citovaný článek - PubMed ID 35979496
Lightella neohaematopini: A new lineage of highly reduced endosymbionts coevolving with chipmunk lice of the genus Neohaematopinus
The parvorder Rhynchophthirina with a single genus Haematomyzus is a small group of ectoparasites of unclear phylogenetic position, related to sucking and chewing lice. Previous screening based on the 16S rRNA gene indicated that Haematomyzus harbors a symbiotic bacterium whose DNA exhibits a strong shift in nucleotide composition typical of obligate mutualistic symbionts in insects. Within Phthiraptera, the smallest known genomes are found in the symbionts associated with sucking lice, which feed exclusively on mammal blood, compared to the generally larger genomes of the symbionts inhabiting chewing lice, which feed on skin derivatives. In this study, we investigate the genome characteristics of the symbiont associated with Haematomyzus elephantis. We sequenced and assembled the H. elephantis metagenome, extracted a genome draft of its symbiotic bacterium, and showed that the symbiont has a significantly reduced genome, which is with 0.39 Mbp the smallest genome among the symbionts known from Phthiraptera. Multigenic phylogenetic analysis places the symbiont into one of three clusters composed of long-branched symbionts from other insects. More specifically, it clusters together with symbionts from several other sucking lice and also with Wigglesworthia glossinidia, an obligate symbiont of tsetse flies. Consistent with the dramatic reduction of its genome, the H. elephantis symbiont lost many metabolic capacities. However, it retained functional pathways for four B vitamins, a trait typical for symbionts in blood-feeding insects. Considering genomic, metabolic, and phylogenetic characteristics, the new symbiont closely resembles those known from several sucking lice rather than chewing lice.IMPORTANCERhynchophthirina is a unique small group of permanent ectoparasites that is closely related to both sucking and chewing lice. These two groups of lice differ in their morphology, ecology, and feeding strategies. As a consequence of their different dietary sources, i.e., mammals' blood vs vertebrate skin derivatives, they also exhibit distinct patterns of symbiosis with obligate bacterial symbionts. While Rhynchophthirina shares certain traits with sucking and chewing lice, the nature of its obligate symbiotic bacterium and its metabolic role is not known. In this study, we assemble the genome of symbiotic bacterium from Haematomyzus elephantis (Rhynchophthirina), demonstrating its close similarity and phylogenetic proximity to several symbionts of sucking lice. The genome is highly reduced (representing the smallest genome among louse-associated symbionts) and exhibits a significant loss of metabolic pathways. However, similar to other sucking louse symbionts, it retains essential pathways for the synthesis of several B vitamins.
- Klíčová slova
- endosymbionts, genomics, lice,
- MeSH
- Bacteria * genetika klasifikace izolace a purifikace MeSH
- fylogeneze MeSH
- genom bakteriální * MeSH
- Phthiraptera * mikrobiologie MeSH
- RNA ribozomální 16S genetika MeSH
- symbióza * MeSH
- zvířata MeSH
- Check Tag
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
- Názvy látek
- RNA ribozomální 16S MeSH
Symbiosis between insects and bacteria has been established countless times. While it is well known that the symbionts originated from a variety of different bacterial taxa, it is usually difficult to determine their environmental source and a route of their acquisition by the host. In this study, we address this question using a model of Neisseriaceae symbionts in rodent lice. These bacteria established their symbiosis independently with different louse taxa (Polyplax, Hoplopleura, Neohaematopinus), most likely from the same environmental source. We first applied amplicon analysis to screen for candidate source bacterium in the louse environment. Since lice are permanent ectoparasites, often specific to the particular host, we screened various microbiomes associated with three rodent species (Microtus arvalis, Clethrionomys glareolus, and Apodemus flavicollis). The analyzed samples included fur, skin, spleen, and other ectoparasites sampled from these rodents. The fur microbiome data revealed a Neisseriaceae bacterium, closely related to the known louse symbionts. The draft genomes of the environmental Neisseriaceae, assembled from all three rodent hosts, converged to a remarkably small size of approximately 1.4 Mbp, being even smaller than the genomes of the related symbionts. Our results suggest that the rodent fur microbiome can serve as a source for independent establishment of bacterial symbiosis in associated louse species. We further propose a hypothetical scenario of the genome evolution during the transition of a free-living bacterium to the member of the rodent fur-associated microbiome and subsequently to the facultative and obligate louse symbionts.
- Klíčová slova
- Anoplura, Fur microbiome, Metagenomics, Rodents, Sucking lice, Symbiosis,
- MeSH
- Bacteria genetika klasifikace izolace a purifikace MeSH
- fylogeneze MeSH
- mikrobiota * MeSH
- Phthiraptera mikrobiologie MeSH
- RNA ribozomální 16S genetika MeSH
- symbióza * MeSH
- zvířata MeSH
- Check Tag
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
- Názvy látek
- RNA ribozomální 16S MeSH
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.
- Klíčová slova
- bacterial symbiosis, coevolution, genome evolution, hematophagy,
- MeSH
- Anoplura * MeSH
- Bacteria MeSH
- Diptera * mikrobiologie MeSH
- Enterobacteriaceae MeSH
- fylogeneze MeSH
- Gammaproteobacteria * genetika MeSH
- hmyz MeSH
- symbióza MeSH
- vitamin B komplex * MeSH
- zvířata MeSH
- Check Tag
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
- Názvy látek
- vitamin B komplex * MeSH