Search bioRxiv⌕ Search

Biology subjects

Martinu, J.

Publications and source records attributed to Martinu, J..

8 recordsLinked to original sources

Arsenophonus ghosts in bed bug genomes: multiple origins and 50 million years of persistence

Although numerous studies have documented horizontal gene transfer (HGT) from bacteria into insect genomes, they have been heavily biased toward the endosymbiont Wolbachia. In contrast, comparatively few studies have examined HGT from other symbionts and insect-associated bacteria. Moreover, research on these systems has primarily focused on transferred genes that retain function in the insect host, contributing to metabolism, symbiosis, detoxification, or host adaptation. Consequently, relatively few empirical systems have been available to investigate the persistence, degradation, diversification, and vertical inheritance of apparently non-functional HGT-derived sequences over macroevolutionary timescales. The widespread occurrence of putatively Arsenophonus-derived sequences across Cimicidae therefore provides a rare opportunity to extend these investigations beyond the Wolbachia model and to examine the long-term evolutionary fate of non-functional HGT-derived DNA across tens of millions of years of host diversification. We show that Arsenophonus-derived HGTs have multiple independent origins across Cimicidae but that one major HGT lineage has persisted through diversification of the subfamily Cimicinae for at least 50 million years. Phylogenetic and compositional analyses indicate that an ancestral Arsenophonus-derived genomic region has undergone progressive fragmentation, leaving numerous dispersed, apparently non-functional remnants while preserving a clear evolutionary signature. These results extend the study of bacterial HGT beyond the Wolbachia model and demonstrate that non-functional symbiont-derived DNA can persist over macroevolutionary timescales.

evolutionary biology↗

Generalist vs specialist strategy shapes microbiomes in blood feeding parasite Polyplax serrata.

Insects live in association with bacterial communities, collectively referred to as the microbiome. Microbiome composition varies widely across insect taxa and is shaped by multiple factors, including host phylogeny, environmental conditions, geographic distribution, and nutritional ecology. One hypothesis is that microbiome composition may also reflect whether the host adopts a generalist or specialist ecological strategy. We tested this hypothesis using the sucking louse Polyplax serrata, which offers several advantages as a model system. First, as permanent ectoparasites, lice inhabit a relatively stable and simplified environment, thereby minimizing potential confounding variables. Second, within P. serrata, two closely related lineages have been identified: one restricted to a single rodent host (Apodemus flavicollis), and the other exploiting two hosts (A. flavicollis and A. sylvaticus). We analyzed and compared microbiome structure in these two lineages using 16S rRNA gene amplicon sequencing. While alpha diversity did not differ between the lineages, beta diversity differed significantly, particularly in pairwise dissimilarities among individual samples. These results suggest that in P. serrata, host specialization strategy influences microbiome diversity, with the "generalist" lineage harboring more heterogeneous communities. This finding extends previous observations on ecological divergence between the two lineages, showing that closely related cryptic species with highly similar genomes, living sympatrically in the same environment, can rapidly evolve distinct life strategies that, in turn, shape both their genetic structure and their microbiomes.

evolutionary biology↗

Viral metagenome characterization reveals species-specific virome profiles in Triatominae populations from the southern United States

Kissing bugs (Triatominae) are hematophagous insects and the principal vectors of Trypanosoma cruzi, the causative agent of Chagas disease. While their bacterial microbiomes have received considerable attention, the diversity of viruses associated with these insects remains poorly understood. To address this gap, we investigated the metavirome of five Triatominae species from the southern United States (Triatoma rubida, T. sanguisuga, T. gerstaeckeri, T. indictiva, and Hospesneotomae protracta), sampled in Texas, New Mexico, and Arizona. We sequenced gut and reproductive tissues from 23 field-collected specimens and assembled 41 viral operational taxonomic units (vOTUs), 40 of which are novel and together constitute 13 viral families, including Chuviridae, Arenaviridae, Orthomyxoviridae, Partitiviridae, Solemoviridae, Circoviridae, Rhabdoviridae, Microviridae, Xinmoviridae, Astroviridae, Narnaviridae, Tombusviridae, and the order Elliovirales. The vOTUs composition and abundance analysis examined variables including host species, sex, tissue type, blood meal, and T. cruzi infection status, showing that metavirome diversity varied significantly among host species. Our findings demonstrate a species-specific metavirome and the presence of virus taxa linked to insects, plants, and vertebrates, highlighting the complex ecological interactions between viruses and triatomines. This study uncovers a diverse and largely novel set of metaviromes within North American Triatominae, providing a foundation for future research on virus-vector interactions.

ecology↗

Dynamic but constrained: Repeated acquisitions of nutritional symbionts in bed bugs (Heteroptera: Cimicidae) from a narrow taxonomic pool.

BackgroundBed bugs (Heteroptera: Cimicidae), like other strictly blood-feeding insects, harbor obligate bacterial symbionts that supply essential nutrients (especially B vitamins) lacking in their blood diet. The primary obligate symbionts are transovarially transmitted Wolbachia, notable for having horizontally acquired biotin operon. In addition to these symbionts with the confirmed nutritional role, bacteria from the genera Symbiopectobacterium and Tisiphia have also been found to be transovarially transmitted in bed bugs. Their significance to the host fitness remains unclear; they are considered facultative, and thus likely non-essential. However, this understanding of bed bugs symbiosis is based exclusively on studies of the human-associated common bed bug (Cimex lectularius) and few related Cimicinae species. Virtually nothing is known about the diversity, origins, or metabolic roles of symbionts across the more than hundred described bed bug species. ResultsUsing amplicon and metagenomic analyzes, we identified five different bacterial genera as potential bed bug symbionts: Wolbachia, Symbiopectobacterium, Sodalis, Serratia, and Tisiphia. The distribution of these bacteria among 13 bed bug species indicated at least 16 independent origins of symbiosis (some samples harboring multiple symbiont strains). A comparison of host and symbiont phylogenies suggested that some of these origins were followed by cospeciation. Not all bed bugs, however, harbored Wolbachia. In the subfamily Cacodminae, Symbiopectobacterium (previously known as facultative symbiont) was detected as the sole symbiont, suggesting its role as an essential, obligate symbiont. Analysis of 23 obtained genome drafts revealed considerable differences in their size and gene content, indicating that these bacteria have reached different stages in the evolution towards obligate symbiosis. As is common in symbiotic bacteria, the analyzed genomes have lost many biosynthetic capacities. A comparison of B-vitamin synthesis pathways showed that only two, riboflavin and lipoic acid, were preserved across all symbionts. ConclusionsAn overview of symbiosis across a broad phylogenetic span of bed bugs reveals that this insect family has undergone remarkably dynamic evolution, characterized by multiple independent symbiont acquisitions, episodes of cospeciations, and frequent co-occurrence of multiple symbionts within individual hosts. Interestingly, although these symbionts were acquired through multiple independent events, the majority belong to just three bacterial genera (Wolbachia, Symbiopectobacterium, and Sodalis), suggesting an unknown mechanisms underlying bed bug-symbiont specificity. Two aspects of this study warrant further investigation. First, the finding of Symbiopectobacterium as the sole obligate symbiont in Cacodminae suggests that expanding the taxonomic sampling may reveal an even more complex structure of symbiosis within bed bugs. Second, the inconsistencies and uncertainties in evaluating the functionality of the biotin synthesis indicate that further research will be necessary to better understand the evolution of this B vitamin pathway in symbiotic bacteria.

evolutionary biology↗

Highly resolved genomes as a tool for studying speciation history of two closely related louse lineages with different host specificities.

Sucking lice of the suborder Anoplura are permanent ectoparasites with specific lifestyle and highly derived features. Currently, genomic data are only available for a single species, the human louse Pediculus humanus. In this study we present genomes of two distinct lineages, with different host spectra, of a rodent louse Polyplax serrata. Genomes of these ecologically different lineages are closely similar in gene content, display a high level of synteny, but they also differ by a few duplications/translocations and single inversion. Compared to P. humanus, the two P. serrata genomes are noticeably larger (139 Mbp vs. 111 Mbp) and encode a higher number of genes. Similar to P. humanus, they are significantly reduced in sensory-related categories such as vision and olfaction. Utilizing a genome-wide set of genes, we perform phylogenetic reconstruction and evolutionary dating of the P. serrata lineages. Obtained estimates reveal their relatively deep origin (approx. 6.5 Mya), comparable to the time of split between the human and chimpanzee lice Pediculus humanus and P. schaeffi. This dating supports the view that the P. serrata lineages are likely to represent two cryptic species with different host spectra. Historical demographies of the two lineages show glaciation-related population size (Ne) reduction, but recent restoration of Ne was seen only in the less host specific lineage. Together with the louse genomes, we analyze genomes of their bacterial symbiont Legionella polyplacis, and evaluate their potential complementarity in synthesis of amino acids and B vitamins. We show that both systems, Polyplax/Legionella and Pediculus/Riesia, display almost identical patterns, with symbionts involved in synthesis of B vitamins but not amino acids.

genomics↗

Extremely reduced supergroup F Wolbachia: transition to obligate insect symbionts

Wolbachia are widely distributed symbionts among invertebrates that manifest by a broad spectrum of lifestyles from parasitism to mutualism. Wolbachia Supergroup F is considered a particularly interesting group which gave rise to symbionts of both arthropods and nematodes, and some of its members are obligate mutualists. Further investigations on evolutionary transitions in symbiosis have been hampered by a lack of genomic data for Supergroup F members. In this study, we present genomic data for five new supergroup F Wolbachia strains associated with four chewing lice species. These new strains in different evolutionary stages show genomic characteristics well-illustrating the evolutionary trajectory which symbiotic bacteria experience during their transition to mutualism. Three of the strains have not yet progressed with the transition, the other two show typical signs of ongoing gene deactivation and removal (genome size, coding density, low number of pseudogenes). Particularly, wMeur1, a symbiont fixed in all Menacanthus eurysternus populations across four continents, possesses a highly reduced genome of 733,850 bp with a horizontally acquired capacity for pantothenate synthesis. Comparing with other strains showed wMeur1 genome as the smallest currently known among all Wolbachia and the first example of Wolbachia which has completed genomic streamlining known from the gammaproteobacterial obligate symbionts.

evolutionary biology↗

Host "cleansing zone" at secondary contact: a new pattern in host-parasite population genetics.

We introduce a new pattern of population genetic structure in a host-parasite system that can arise after secondary contact (SC) of previously isolated populations. Due to different generation time and therefore different tempo of molecular evolution the host and parasite populations reach different degrees of genetic differentiation during their separation (e.g. in refugia). Consequently, during the SC the host populations are able to re-establish a single panmictic population across the whole recolonized area, while the parasite populations stop their dispersal at the SC zone and create a narrow hybrid zone (HZ). From the hosts perspective, the parasites HZ functions on a microevolutionary scale as a "host-cleansing filter": while passing from area A to area B, the hosts are rid of the area A parasites and acquire the area B parasites. We demonstrate this novel pattern on a model composed of Apodemus mice and Polyplax lice by comparing maternally inherited markers (complete mitochondrial genomes, and complete genomes of vertically transmitted symbiont Legionella polyplacis) with SNPs derived from the louse genomic data. We discuss circumstances which may lead to this pattern and possible reasons why it has been overlooked in the studies on host-parasite population genetics.

evolutionary biology↗

A new symbiotic lineage related to Neisseria and Snodgrassella arises from the dynamic and diverse microbiomes in sucking lice

Phylogenetic diversity of symbiotic bacteria in sucking lice suggests that lice have experienced a complex history of symbiont acquisition, loss, and replacement during their evolution. By combining metagenomics and amplicon screening across several populations of two louse genera (Polyplax and Hoplopleura) we describe a novel louse symbiont lineage related to Neisseria and Snodgrassella, and show its independent origin within dynamic lice microbiomes. While the genomes of these symbionts are highly similar in both lice genera, their respective distributions and status within lice microbiomes indicate that they have different functions and history. In Hoplopleura acanthopus, the Neisseria-related bacterium is a dominant obligate symbiont universally present across several hosts populations, and seems to be replacing a presumably older and more degenerated obligate symbiont. In contrast, the Polyplax microbiomes are dominated by the obligate symbiont Legionella polyplacis, with the Neisseria-related bacterium co-occurring only in some samples and with much lower abundance.

evolutionary biology↗