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Fur microbiome as a putative source of symbiotic bacteria in sucking lice - PubMed

  • ️Mon Jan 01 2024

Fur microbiome as a putative source of symbiotic bacteria in sucking lice

Jana Martin Říhová et al. Sci Rep. 2024.

Abstract

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.

Keywords: Anoplura; Fur microbiome; Metagenomics; Rodents; Sucking lice; Symbiosis.

© 2024. The Author(s).

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Conflict of interest statement

The authors declare no competing interests.

Figures

Fig. 1
Fig. 1

Overview of the Neisseriaceae OTUs determined by amplicon analysis. A - % similarities (above diagonal) and single nucleotide differences (under diagonal) for the 16 S rRNA gene fragments acquired from the amplicon screening. HaMa = symbiont of H. acanthopus, PsAf = symbiont of P. serrata. B - Relative abundance of the Neisseriaceae OTUs comprising more than 10% (light green) or 50% (dark green) of all reads in the sample. Fur swabs of the samples highlighted in grey were used for the whole-genome sequencing. The samples from mouse spleens are not included in this overview since they did not contain relevant numbers of the reads of the analyzed Neisseraiceae OTUs (see Supplementary Table 1).

Fig. 2
Fig. 2

Phylogenetic tree inferred by PhyloBayes from concatenated 50-protein matrix (11,697 aa) using CAT-GTR model. Nodes with posterior probabilities not equal to 1 are designated by the green (0.5) and blue (> 0.8) dots. Clustering of the louse symbionts and the environmental OTU 5 samples (i.e., the genomes with 16 S rRNA genes identical to those of the amplicon OTU 5) is highlighted by blue background (dark for symbionts, light for the environmental OTU 5).

Fig. 3
Fig. 3

Hypothetical scenario of evolutionary relationship between the microbiome of rodent fur (specifically OTU 5), and the facultative/obligate symbionts in the rodent louse. The orange dots stand for the OTU 5 (in the mouse fur) and the closely related symbionts in the lice. For details on the gene losses and acquisitions see text.

Fig. 4
Fig. 4

Phylogenetic tree inferred by PhyML analysis from the matrix of 16SrRNA fragments corresponding to the amplicon screening (1,517 bp; ML under HKY85 + G + I model). Symbiotic bacteria of lice (“Symbiotic cluster”; designated by dark blue) form a monophyletic lineage together with the Neisseriaceae environmental bacteria (“OTU 5 cluster”; designated by light blue). OTU 66 corresponds to the symbiont of H. acanthopus . Values at the nodes show bootstrap supports.

Fig. 5
Fig. 5

Proportions of the genes of Neisseriales origin (green), the genes acquired by horizontal transfer (yellow), and the genes yielding no blast hits (grey). The numbers stand for the annotated genes/ genes without annotation.

Fig. 6
Fig. 6

Comparison of genome contents of the Neisseriaceae related symbionts and the environmental bacteria. A – Number of genes shared among the genomes. The numbers stand for orthologs/genes with assigned K numbers. B – Proportion of the shared genes: outer circles show orthologs, inner circles the genes with assigned K numbers.

Fig. 7
Fig. 7

Comparison of selected metabolic capacities of environmental OTU 5 (light blue background), louse symbionts (dark blue background), and three related Neisseriaceae. Colours of the cells stand for: grey - missing/nonfunctional pathways, light green - functional pathway, dark green – pathway functional due to HGT. Names in the cells indicate missing genes, which are however likely not essential for the pathway function (see the text). Asterisks indicate pathway with the same single gene missing in all genomes. Following genes are putative HGT in the dark green cells: nicotinate - nadB, nadA, nadC; biotin - bioF, bioA, bioD, bioB; heme - ALA5; T6SS - vasK, vasF, vasE, vasB, vasA, impF, impC, impB, impA, hcp, vgrG, vasG. For complete metabolic overview see Supplementary Table 4.

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References

    1. McCutcheon, J. P., Boyd, B. M. & Dale, C. The life of an insect endosymbiont from the cradle to the grave. Curr. Biol.29, R485–R495. 10.1016/j.cub.2019.03.032 (2019). - PubMed
    1. Husník, F., Chrudimský, T. & Hypša, V. Multiple origins of endosymbiosis within the Enterobacteriaceae (γ-Proteobacteria): convergence of complex phylogenetic approaches. BMC Biol.9, 87. 10.1186/1741-7007-9-87 (2011). - PMC - PubMed
    1. Gerhart, J. G., Moses, A. S. & Raghavan, R. A Francisella-like endosymbiont in the Gulf Coast tick evolved from a mammalian pathogen. Sci. Rep.6 (1), 33670. 10.1038/srep33670 (2016). - PMC - PubMed
    1. Chari, A. et al. Phenotypic characterization of Sodalis praecaptivus sp. nov., a close non-insect-associated member of the Sodalis-allied lineage of insect endosymbionts. Int. J. Syst. Evol. Microbiol.65, 1400–1405. 10.1099/ijs.0.000113 (2015). - PMC - PubMed
    1. Husník, F. Host–symbiont–pathogen interactions in blood-feeding parasites: Nutrition, immune cross-talk and gene exchange. Parasitology. 145, 1294–1303. 10.1017/S0031182018001104 (2018). - PubMed

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