Endosymbiont Capture, a Repeated Process of Endosymbiont Transfer with Replacement in Trypanosomatids Angomonas spp.
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ABSTRACT:
SUBMITTER: Skalicky T
PROVIDER: S-EPMC8229890 | biostudies-literature |
REPOSITORIES: biostudies-literature
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Project description:Angomonas deanei is an endosymbiont-bearing trypanosomatid with several highly fragmented genome assemblies and unknown chromosome number. We present an assembly of the A. deanei nuclear genome based on Oxford Nanopore sequence that resolves into 29 complete or close-to-complete chromosomes. The assembly has several previously unknown special features; it has a supernumerary chromosome, a chromosome with a 340-kb inversion, and there is a translocation between two chromosomes. We also present an updated annotation of the chromosomal genome with 10,365 protein-coding genes, 59 transfer RNAs, 26 ribosomal RNAs, and 62 noncoding RNAs.
| S-EPMC8022732 | biostudies-literature
Project description:Bacteriophage flux can cause the majority of genetic diversity in free-living bacteria. This tenet of bacterial genome evolution generally does not extend to obligate intracellular bacteria owing to their reduced contact with other microbes and a predominance of gene deletion over gene transfer. However, recent studies suggest intracellular coinfections in the same host can facilitate exchange of mobile elements between obligate intracellular bacteria-a means by which these bacteria can partially mitigate the reductive forces of the intracellular lifestyle. To test whether bacteriophages transfer as single genes or larger regions between coinfections, we sequenced the genome of the obligate intracellular Wolbachia strain wVitB from the parasitic wasp Nasonia vitripennis and compared it against the prophage sequences of the divergent wVitA coinfection. We applied, for the first time, a targeted sequence capture array to specifically trap the symbiont's DNA from a heterogeneous mixture of eukaryotic, bacterial, and viral DNA. The tiled array successfully captured the genome with 98.3% efficiency. Examination of the genome sequence revealed the largest transfer of bacteriophage and flanking genes (52.2 kb) to date between two obligate intracellular coinfections. The mobile element transfer occurred in the recent evolutionary past based on the 99.9% average nucleotide identity of the phage sequences between the two strains. In addition to discovering an evolutionary recent and large-scale horizontal phage transfer between coinfecting obligate intracellular bacteria, we demonstrate that "targeted genome capture" can enrich target DNA to alleviate the problem of isolating symbiotic microbes that are difficult to culture or purify from the conglomerate of organisms inside eukaryotes.
| S-EPMC3068000 | biostudies-literature
Project description:The endosymbiosis in trypanosomatids is characterized by co-evolution between one bacterium and its host protozoan in a mutualistic relationship, thus constituting an excellent model to study organelle origin in the eukaryotic cell. In this association, an intense metabolic exchange is observed between both partners: the host provides energetic molecules and a stable environment to a reduced wall symbiont, while the bacterium is able to interfere in host metabolism by enhancing phospholipid production and completing essential biosynthesis pathways, such as amino acids and hemin production. The bacterium envelope presents a reduced cell wall which is mainly composed of cardiolipin and phosphatidylcholine, being the latter only common in intracellular prokaryotes. Phosphatidylinositol (PI) is also present in the symbiont and host cell membranes. This phospholipid is usually related to cellular signaling and to anchor surface molecules, which represents important events for cellular interactions.In order to investigate the production of PI and its derivatives in symbiont bearing trypanosomatids, aposymbiotic and wild type strains of Angomonas deanei, as well as isolated symbionts, were incubated with [(3)H]myo-inositol and the incorporation of this tracer was analyzed into inositol-containing molecules, mainly phosphoinositides and lipoproteins. Gene searches and their phylogenies were also performed in order to investigate the PI synthesis in symbiontbearing trypanosomatids.Our results showed that the bacterium did not incorporate the tracer and that both strains produced similar quantities of PI and its derivatives, indicating that the symbiont does not influence the production of these metabolites. Gene searches related to PI synthesis revealed that the trypanosomatid genome contains an inositol transporter, PI synthase and the myo-inositol synthase. Thus, the host is able to produce PI either from exogenous myo-inositol (inositol transporter) or from myo-inositol synthesized de novo. Phylogenetic analysis using other organisms as references indicated that, in trypanosomatids, the genes involved in PI synthesis have a monophyletic origin. In accordance with experimental data, sequences for myo-inositol transport or for myo-inositol and PI biosynthesis were not found in the symbiont.Altogether, our results indicate that the bacterium depends on the host to obtain PI.
| S-EPMC4424895 | biostudies-literature
Project description:Bacterial endosymbionts are found across the eukaryotic kingdom and profoundly impacted eukaryote evolution. In many endosymbiotic associations with vertically inherited symbionts, highly complementary metabolic functions encoded by host and endosymbiont genomes indicate integration of metabolic processes between the partner organisms. While endosymbionts were initially expected to exchange only metabolites with their hosts, recent evidence has demonstrated that also host-encoded proteins can be targeted to the bacterial symbionts in various endosymbiotic systems. These proteins seem to participate in regulating symbiont growth and physiology. However, mechanisms required for protein targeting and the specific endosymbiont targets of these trafficked proteins are currently unexplored owing to a lack of molecular tools that enable functional studies of endosymbiotic systems.Here we show that the trypanosomatid Angomonas deanei, which harbors a ?-proteobacterial endosymbiont, is readily amenable to genetic manipulation. Its rapid growth, availability of full genome and transcriptome sequences, ease of transfection, and high frequency of homologous recombination have allowed us to stably integrate transgenes into the A. deanei nuclear genome, efficiently generate null mutants, and elucidate protein localization by heterologous expression of a fluorescent protein fused to various putative targeting signals. Combining these novel tools with proteomic analysis was key for demonstrating the routing of a host-encoded protein to the endosymbiont, suggesting the existence of a specific endosymbiont-sorting machinery in A. deanei.After previous reports from plants, insects, and a cercozoan amoeba we found here that also in A. deanei, i.e. a member of a fourth eukaryotic supergroup, host-encoded proteins can be routed to the bacterial endosymbiont. This finding adds further evidence to our view that the targeting of host proteins is a general strategy of eukaryotes to gain control over and interact with a bacterial endosymbiont. The molecular resources reported here establish A. deanei as a time and cost efficient reference system that allows for a rigorous dissection of host-symbiont interactions that have been, and are still being shaped over evolutionary time. We expect this system to greatly enhance our understanding of the biology of endosymbiosis.
| S-EPMC5106770 | biostudies-literature
Project description:Eukaryotic genomes can acquire bacterial DNA via lateral gene transfer (LGT).1 A prominent source of LGT is Wolbachia,2 a widespread endosymbiont of arthropods and nematodes that is transmitted maternally through female germline cells.3,4 The DNA transfer from the Wolbachia endosymbiont wAna to Drosophila ananassae is extensive5-7 and has been localized to chromosome 4, contributing to chromosome expansion in this lineage.6 As has happened frequently with claims of bacteria-to-eukaryote LGT, the contribution of wAna transfers to the expanded size of D. ananassae chromosome 4 has been specifically contested8 owing to an assembly where Wolbachia sequences were classified as contaminants and removed.9 Here, long-read sequencing with DNA from a Wolbachia-cured line enabled assembly of 4.9 Mbp of nuclear Wolbachia transfers (nuwts) in D. ananassae and a 24-kbp nuclear mitochondrial transfer. The nuwts are <8,000 years old in at least two locations in chromosome 4 with at least one whole-genome integration followed by rapid extensive duplication of most of the genome with regions that have up to 10 copies. The genes in nuwts are accumulating small indels and mobile element insertions. Among the highly duplicated genes are cifA and cifB, two genes associated with Wolbachia-mediated Drosophila cytoplasmic incompatibility. The wAna strain that was the source of nuwts was subsequently replaced by a different wAna endosymbiont. Direct RNA Nanopore sequencing of Wolbachia-cured lines identified nuwt transcripts, including spliced transcripts, but functionality, if any, remains elusive.
| S-EPMC9311232 | biostudies-literature
Project description:Bats are infected with several trypanosomatid species; however, assessing the diversity of this interaction remains challenging since there are species apparently unable to grow in conventional culture media. Accordingly, the ecology and biology of the Molecular Operational Taxonomic Units (MOTUs) Trypanosoma spp. Neobats are unknown. Therefore, we performed the molecular characterization targeting the 18S small subunit rDNA from the blood clot of 280 bats of three Brazilian regions (Paraíba, Rio de Janeiro and Acre states), bypassing the selective pressure of hemoculture. From 68 (24%) positive blood clot samples, we obtained 49 satisfactory sequences. Of these successfully sequenced results, T. spp. Neobats (1, 3 and 4) represented 67%, with the most abundant T. sp. Neobat 4 (53%). Our results show: (1) high abundance and wide geographic range of T. sp. Neobat 4, restricted to Carollia bats; (2) high infection rate of T. sp. Neobat 4 in Carollia perspicillata populations (mean 26%); (3) infection with the monoxenous Crithidia mellificae; and (4) a new MOTU (T. sp. Neobat 5) in Artibeus cinereus, positioning in the Trypanosoma wauwau clade. These data corroborate the importance of bats as hosts of many Trypanosoma species and C. mellificae. They also show that the diversity of the T. wauwau clade is underestimated and warn about the high magnitude of trypanosomes we overpass with the hemoculture. Our findings combined with previous data show that T. spp. Neobats include host-specific and host-generalist species, probably playing different ecological roles: T. sp. Neobat 1 shows broad host range; T. spp. Neobat 3 and 4 are restricted to Artibeus and Carollia, respectively. Finally, T. Neobat 4 seems to be a well-succeeded parasite, especially within C. perspicillata metapopulations across a wide geographical distribution. This work is a step forward to understand the biology and life history of T. spp. Neobats.
| S-EPMC8449017 | biostudies-literature
Project description:BackgroundInsects living in nutritionally poor environments often establish long-term relationships with intracellular bacteria that supplement their diets and improve their adaptive and invasive powers. Even though these symbiotic associations have been extensively studied on physiological, ecological, and evolutionary levels, few studies have focused on the molecular dialogue between host and endosymbionts to identify genes and pathways involved in endosymbiosis control and dynamics throughout host development.ResultsWe simultaneously analyzed host and endosymbiont gene expression during the life cycle of the cereal weevil Sitophilus oryzae, from larval stages to adults, with a particular emphasis on emerging adults where the endosymbiont Sodalis pierantonius experiences a contrasted growth-climax-elimination dynamics. We unraveled a constant arms race in which different biological functions are intertwined and coregulated across both partners. These include immunity, metabolism, metal control, apoptosis, and bacterial stress response.ConclusionsThe study of these tightly regulated functions, which are at the center of symbiotic regulations, provides evidence on how hosts and bacteria finely tune their gene expression and respond to different physiological challenges constrained by insect development in a nutritionally limited ecological niche. Video Abstract.
| S-EPMC10717185 | biostudies-literature
Project description:Barcoding project of insect and plant trypanosomatids availables at Fiocruz Protozoa Culture Collection http://colprot.fiocruz.br/ Phenotype or genotype
| PRJNA549390 | ENA
Project description:Symbiotic interactions between organisms create new ecological niches. For example, many insects survive on plant-sap with the aid of maternally transmitted bacterial symbionts that provision essential nutrients lacking in this diet. Symbiotic partners often enter a long-term relationship in which the co-evolutionary fate of lineages is interdependent. Obligate symbionts that are strictly maternally transmitted experience genetic drift and genome degradation, compromising symbiont function and reducing host fitness unless hosts can compensate for these deficits. One evolutionary solution is the acquisition of a novel symbiont with a functionally intact genome. Whereas almost all aphids host the anciently acquired bacterial endosymbiont Buchnera aphidicola (Gammaproteobacteria), Geopemphigus species have lost Buchnera and instead contain a maternally transmitted symbiont closely related to several known insect symbionts from the bacterial phylum Bacteroidetes. A complete genome sequence shows the symbiont has lost many ancestral genes, resulting in a genome size intermediate between that of free-living and symbiotic Bacteroidetes. The Geopemphigus symbiont retains biosynthetic pathways for amino acids and vitamins, as in Buchnera and other insect symbionts. This case of evolutionary replacement of Buchnera provides an opportunity to further understand the evolution and functional genomics of symbiosis.
| S-EPMC5864228 | biostudies-literature
Project description:BackgroundAdapting to changes in the environment is the foundation of species survival, and is usually thought to be a gradual process. However, transposable elements (TEs), epigenetic modifications, and/or genetic material acquired from other organisms by means of horizontal gene transfer (HGTs), can also lead to novel adaptive traits. Social insects form dense societies, which attract and maintain extra- and intracellular accessory inhabitants, which may facilitate gene transfer between species. The wood ant Formica exsecta (Formicidae; Hymenoptera), is a common ant species throughout the Palearctic region. The species is a well-established model for studies of ecological characteristics and evolutionary conflict.ResultsIn this study, we sequenced and assembled draft genomes for F. exsecta and its endosymbiont Wolbachia. The F. exsecta draft genome is 277.7 Mb long; we identify 13,767 protein coding genes, for which we provide gene ontology and protein domain annotations. This is also the first report of a Wolbachia genome from ants, and provides insights into the phylogenetic position of this endosymbiont. We also identified multiple horizontal gene transfer events (HGTs) from Wolbachia to F. exsecta. Some of these HGTs have also occurred in parallel in multiple other insect genomes, highlighting the extent of HGTs in eukaryotes.ConclusionWe present the first draft genome of ant F. exsecta, and its endosymbiont Wolbachia (wFex), and show considerable rates of gene transfer from the symbiont to the host. We expect that especially the F. exsecta genome will be valuable resource in further exploration of the molecular basis of the evolution of social organization.
| S-EPMC6469114 | biostudies-literature