Endosymbiotic bacteria of the boar louse Haematopinus apri (Insecta: Phthiraptera: Anoplura)

Abstract

Insects exclusively feeding on vertebrate blood are usually dependent on symbiotic bacteria for provisioning of B vitamins. Among them, sucking lice are prominent in that their symbiotic bacteria as well as their symbiotic organs exhibit striking diversity. Here we investigated the bacterial diversity associated with the boar louse Haematopinus apri in comparison with the hog louse Haematopinus suis. Amplicon sequencing analysis identified the primary endosymbiont predominantly detected from all populations of H. apri with some minor secondary bacterial associates. Sequencing and phylogenetic analysis of bacterial 16S rRNA gene confirmed that the endosymbionts of the boar louse H. apri, the hog louse H. suis and the cattle louse Haematopinus eurysternus form a distinct clade in the Gammaproteobacteria. The endosymbiont clade of Haematopinus spp. was phylogenetically distinct from the primary endosymbionts of other louse lineages. Fluorescence in situ hybridization visualized the endosymbiont localization within midgut epithelium, ovarial ampulla and posterior oocyte of H. apri, which were substantially the same as the endosymbiont localization previously described in H. suis and H. eurysternus. Mitochondrial haplotype analysis revealed that, although the domestic pig was derived from the wild boar over the past 8,000 years of human history, the populations of H. apri constituted a distinct sister clade to the populations of H. suis. Based on these results, we discussed possible evolutionary trajectories of the boar louse, the hog louse and their endosymbionts in the context of swine domestication. We proposed ‘Candidatus Haematopinicola symbiotica’ for the distinct clade of the endosymbionts of Haematopinus spp.

Variable organization of symbiont-containing tissue across planthoppers hosting different heritable endosymbionts

“…In contrast, in Camponotus ants, Hippoboscoidea flies, and some sucking lice, bacteriocytes are directly associated with the intestinal wall. They might be inserted between gut epithelium and muscle layer (in Hippoboscoidea flies and sucking lice) or between gut epithelial cells (in Camponotus ants) ( Buchner, 1965 ; Schröder et al, 1996 ; Nishide et al, 2022 ). In turn, in tsetse flies, paired bacteriomes are localized in the midgut lumen ( Rio et al, 2012 ), resembling the localization of the rectal organ in females of Vidania -hosting planthopper species, but to our knowledge, not reported so far from any other insect group.…”

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

“…To set the analysis in a broader phylogenetic span, and to provide a reliable outgroup, we further included 16S rRNA genes of several additional bacteria (Supplementary Table 2). Together with the six Neisseriaceae OTUs (5, 66, 102, 157, 793, and 815), the Neisseriaceae-related bacteria described from lice and flea (Jones et al 2008, Nishide et al 2022), and ten outgroups, the final matrix contained 2,905 sequences (see Supplementary Table 2 for detailed description of the matrix composition). These sequences were aligned using MAFFT with E-INS-i settings (Katoh et al 2002) implemented in Geneious Prime v.2020.2.5 (Kearse et al 2012).…”

“…Together with the six Neisseriaceae OTUs (5, 66, 102, 157, 793, and 815), the Neisseriaceae-related bacteria described from lice and flea (Jones et al 2008, Nishide et al 2022, and ten outgroups, the final matrix contained 2,905 sequences (see Supplementary Table 2 for detailed description of the matrix composition).…”

“…Third, recent studies revealed that within this diversity, one bacterial lineage related to Neisseriaceae established symbiosis independently with several groups of lice and reached different stages of evolution. While in some lice they show features typical for facultative symbionts (e.g., Polyplax serrata, Neohaematopinus pacificus , and possibly Haematopinus apri ; Nishide et al 2022, Rihova et al 2022, Rihova et al 2021), in others they function as obligate mutualists ( Hoplopleura acanthopus ; Rihova et al 2021). This frequent occurrence of the Neisseriaceae-related symbionts suggests that they may be acquired from the host, either as part of the fur/skin microbiome or from the host blood.…”