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In genetic conflicts between intergenomic and selfish elements, driver and killer elements achieve biased survival, replication, or transmission over sensitive and targeted elements through a wide range of molecular mechanisms, including mimicry. Driving mechanisms manifest at all organismal levels, from the biased propagation of individual genes, as demonstrated by transposable elements, to the biased transmission of genomes, as illustrated by viruses, to the biased transmission of cell lineages, as in cancer. Targeted genomes are vulnerable to molecular mimicry through the conserved motifs they use for their own signaling and regulation. Mimicking these motifs enables an intergenomic or selfish element to control core target processes, and can occur at the sequence, structure, or functional level. Molecular mimicry was first appreciated as an important phenomenon more than twenty years ago. Modern genomics technologies, databases, and machine learning approaches offer tremendous potential to study the distribution of molecular mimicry across genetic conflicts in nature. Here, we explore the theoretical expectations for molecular mimicry between conflicting genomes, the trends in molecular mimicry mechanisms across known genetic conflicts, and outline how new examples can be gleaned from population genomic datasets. We discuss how mimics involving short sequence-based motifs or gene duplications can evolve convergently from new mutations. Whereas, processes that involve divergent domains or fully-folded structures occur among genomes by horizontal gene transfer. These trends are largely based on a small number of organisms and should be reevaluated in a general, phylogenetically independent framework. Currently, publicly available databases can be mined for genotypes driving non-Mendelian inheritance patterns, epistatic interactions, and convergent protein structures. A subset of these conflicting elements may be molecular mimics. We propose approaches for detecting genetic conflict and molecular mimicry from these datasets.
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The intracellular symbiont Wolbachia pipientis evolved after the divergence of arthropods and nematodes, but it reached high prevalence in many of these taxa through its abilities to infect new hosts and their germlines. Some strains exhibit long-term patterns of co-evolution with their hosts, while other strains are capable of switching hosts. This makes strain selection an important factor in symbiont-based biological control. However, little is known about the ecological and evolutionary interactions that occur when a promiscuous strain colonizes an infected host. Here, we study what occurs when two strains come into contact in host cells following horizontal transmission and infection. We focus on the faithful wMel strain from Drosophila melanogaster and the promiscuous wRi strain from Drosophila simulans using an in vitro cell culture system with multiple host cell types and combinatorial infection states. Mixing D. melanogaster cell lines stably infected with wMel and wRi revealed that wMel outcompetes wRi quickly and reproducibly. Furthermore, wMel was able to competitively exclude wRi even from minuscule starting quantities, indicating that this is a nearly deterministic outcome, independent of the starting infection frequency. This competitive advantage was not exclusive to wMel's native D. melanogaster cell background, as wMel also outgrew wRi in D. simulans cells. Overall, wRi is less adept at in vitro growth and survival than wMel and its in vivo state, revealing differences between the two strains in cellular and humoral regulation. These attributes may underlie the observed low rate of mixed infections in nature and the relatively rare rate of host-switching in most strains. Our in vitro experimental framework for estimating cellular growth dynamics of Wolbachia strains in different host species and cell types provides the first strategy for parameterizing endosymbiont and host cell biology at high resolution. This toolset will be crucial to our application of these bacteria as biological control agents in novel hosts and ecosystems.
Assuntos
Drosophila melanogaster , Simbiose , Wolbachia , Wolbachia/fisiologia , Animais , Drosophila melanogaster/microbiologia , Evolução Biológica , Drosophila simulans/microbiologia , Linhagem CelularRESUMO
The alphaproteobacterium Wolbachia pipientis infects arthropod and nematode species worldwide, making it a key target for host biological control. Wolbachia-driven host reproductive manipulations, such as cytoplasmic incompatibility (CI), are credited for catapulting these intracellular bacteria to high frequencies in host populations. Positive, perhaps mutualistic, reproductive manipulations also increase infection frequencies, but are not well understood. Here, we identify molecular and cellular mechanisms by which Wolbachia influences the molecularly distinct processes of germline stem cell (GSC) self-renewal and differentiation. We demonstrate that wMel infection rescues the fertility of flies lacking the translational regulator mei-P26 and is sufficient to sustain infertile homozygous mei-P26-knockdown stocks indefinitely. Cytology revealed that wMel mitigates the impact of mei-P26 loss through restoring proper pMad, Bam, Sxl, and Orb expression. In Oregon R files with wild-type fertility, wMel infection elevates lifetime egg hatch rates. Exploring these phenotypes through dual-RNAseq quantification of eukaryotic and bacterial transcripts revealed that wMel infection rescues and offsets many gene expression changes induced by mei-P26 loss at the mRNA level. Overall, we show that wMel infection beneficially reinforces host fertility at mRNA, protein, and phenotypic levels, and these mechanisms may promote the emergence of mutualism and the breakdown of host reproductive manipulations.
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Proteínas de Drosophila , Wolbachia , Animais , Drosophila/metabolismo , Fertilidade , Diferenciação Celular , Células Germinativas/metabolismo , Células-Tronco/metabolismo , RNA Mensageiro/metabolismo , Drosophila melanogaster/genética , Proteínas de Ligação a RNA/genética , Proteínas de Drosophila/metabolismoRESUMO
High-throughput short-read sequencing has taken on a central role in research and diagnostics. Hundreds of different assays take advantage of Illumina short-read sequencers, the predominant short-read sequencing technology available today. Although other short-read sequencing technologies exist, the ubiquity of Illumina sequencers in sequencing core facilities and the high capital costs of these technologies have limited their adoption. Among a new generation of sequencing technologies, Oxford Nanopore Technologies (ONT) holds a unique position because the ONT MinION, an error-prone long-read sequencer, is associated with little to no capital cost. Here we show that we can make short-read Illumina libraries compatible with the ONT MinION by using the rolling circle to concatemeric consensus (R2C2) method to circularize and amplify the short library molecules. This results in longer DNA molecules containing tandem repeats of the original short library molecules. This longer DNA is ideally suited for the ONT MinION, and after sequencing, the tandem repeats in the resulting raw reads can be converted into high-accuracy consensus reads with similar error rates to that of the Illumina MiSeq. We highlight this capability by producing and benchmarking RNA-seq, ChIP-seq, and regular and target-enriched Tn5 libraries. We also explore the use of this approach for rapid evaluation of sequencing library metrics by implementing a real-time analysis workflow.
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Nanoporos , Análise de Sequência de DNA/métodos , Biblioteca Gênica , Sequenciamento de Nucleotídeos em Larga Escala/métodos , Sequenciamento de Cromatina por ImunoprecipitaçãoRESUMO
SignificanceIn marine ecosystems, transmission of microbial symbionts between host generations occurs predominantly through the environment. Yet, it remains largely unknown how host genetics, symbiont competition, environmental conditions, and geography shape the composition of symbionts acquired by individual hosts. To address this question, we applied population genomic approaches to four species of deep-sea hydrothermal vent snails that live in association with chemosynthetic bacteria. Our analyses show that environment is more important to strain-level symbiont composition than host genetics and that symbiont strains show genetic variation indicative of adaptation to the distinct geochemical conditions at each vent site. This corroborates a long-standing hypothesis that hydrothermal vent invertebrates affiliate with locally adapted symbiont strains to cope with the variable conditions characterizing their habitats.
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Fontes Hidrotermais , Bactérias/genética , Ecossistema , Fontes Hidrotermais/microbiologia , Metagenômica , Simbiose/genéticaRESUMO
Bacterial symbionts bring a wealth of functions to the associations they participate in, but by doing so, they endanger the genes and genomes underlying these abilities. When bacterial symbionts become obligately associated with their hosts, their genomes are thought to decay towards an organelle-like fate due to decreased homologous recombination and inefficient selection. However, numerous associations exist that counter these expectations, especially in marine environments, possibly due to ongoing horizontal gene flow. Despite extensive theoretical treatment, no empirical study thus far has connected these underlying population genetic processes with long-term evolutionary outcomes. By sampling marine chemosynthetic bacterial-bivalve endosymbioses that range from primarily vertical to strictly horizontal transmission, we tested this canonical theory. We found that transmission mode strongly predicts homologous recombination rates, and that exceedingly low recombination rates are associated with moderate genome degradation in the marine symbionts with nearly strict vertical transmission. Nonetheless, even the most degraded marine endosymbiont genomes are occasionally horizontally transmitted and are much larger than their terrestrial insect symbiont counterparts. Therefore, horizontal transmission and recombination enable efficient natural selection to maintain intermediate symbiont genome sizes and substantial functional genetic variation.
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Bactérias/patogenicidade , Bivalves/microbiologia , Transferência Genética Horizontal , Genoma Bacteriano , Recombinação Genética , Simbiose/genética , Animais , Bactérias/genética , Bivalves/genética , Evolução Molecular , Variação GenéticaRESUMO
There are many compelling examples of molecular convergence at individual genes. However, the prevalence and the relative importance of adaptive genome-wide convergence remain largely unknown. Many recent works have reported striking examples of excess genome-wide convergence, but some of these studies have been called into question because of the use of inappropriate null models. Here, we sequenced and compared the genomes of 12 species of anole lizards that have independently converged on suites of adaptive behavioral and morphological traits. Despite extensive searches for a genome-wide signature of molecular convergence, we found no evidence supporting molecular convergence at specific amino acids either at individual genes or at genome-wide comparisons; we also uncovered no evidence supporting an excess of adaptive convergence in the rates of amino acid substitutions within genes. Our findings indicate that comprehensive phenotypic convergence is not mirrored at genome-wide protein-coding levels in anoles, and therefore, that adaptive phenotypic convergence is likely not constrained by the evolution of many specific protein sequences or structures.
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Adaptação Biológica , Substituição de Aminoácidos , Evolução Molecular , Lagartos/genética , Fenótipo , Animais , Ecossistema , Feminino , Lagartos/anatomia & histologia , Masculino , Índias OcidentaisRESUMO
[This corrects the article DOI: 10.1371/journal.ppat.1007216.].
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Widespread success of the intracellular bacterium Wolbachia across insects and nematodes is due to efficient vertical transmission and reproductive manipulations. Many strains, including wMel from Drosophila melanogaster, exhibit a specific concentration to the germplasm at the posterior pole of the mature oocyte, thereby ensuring high fidelity of parent-offspring transmission. Transport of Wolbachia to the pole relies on microtubules and the plus-end directed motor kinesin heavy chain (KHC). However, the mechanisms mediating Wolbachia's association with KHC remain unknown. Here we show that reduced levels of the host canonical linker protein KLC results in dramatically increased levels of Wolbachia at the oocyte's posterior, suggesting that KLC and some key associated host cargos outcompete Wolbachia for association with a limited amount of KHC motor proteins. Consistent with this interpretation, over-expression of KHC causes similarly increased levels of posteriorly localized Wolbachia. However, excess KHC has no effect on levels of Vasa, a germplasm component that also requires KHC for posterior localization. Thus, Wolbachia transport is uniquely KHC-limited because these bacteria are likely outcompeted for binding to KHC by some host cargo/linker complexes. These results reveal a novel host-symbiont interaction that underscores the precise regulation required for an intracellular bacterium to co-opt, but not disrupt, vital host processes.
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Ligação Competitiva , Drosophila melanogaster/microbiologia , Interações Hospedeiro-Patógeno , Cinesinas/metabolismo , Oócitos/microbiologia , Wolbachia/fisiologia , Animais , Polaridade Celular , Drosophila melanogaster/metabolismo , Células Germinativas/microbiologia , Interações Hospedeiro-Patógeno/fisiologia , Microtúbulos/metabolismo , Oócitos/metabolismo , Oogênese/fisiologia , Transporte Proteico , Distribuição Tecidual , Wolbachia/metabolismoRESUMO
Even the simplest microbial-eukaryotic mutualisms are comprised of entire populations of symbionts at the level of the host individual. Early work suggested that these intrahost populations maintain low genetic diversity as a result of transmission bottlenecks or to avoid competition between symbiont genotypes. However, the amount of genetic diversity among symbionts within a single host remains largely unexplored. To address this, we investigated the chemosynthetic symbiosis between the bivalve Solemya velum and its intracellular bacterial symbionts, which exhibits evidence of both vertical and horizontal transmission. Intrahost symbiont populations were sequenced to high coverage (200-1,000×). Analyses of nucleotide diversity revealed that the symbiont genome sequences were largely homogeneous within individual host specimens, consistent with vertical transmission, except for particular regions that were polymorphic in â¼20% of host specimens. These variant sites were also found segregating in other host individuals from the same population, colocalized to several regions of the genome, and consistently co-occurred on the same short read pairs (derived from the same chromosome). These results strongly suggest that these variant haplotypes originated through recombination events, potentially during prior mixed infections or in the external environment, rather than as novel mutations within symbiont populations. This abundant genetic diversity could have a profound influence on symbiont evolution as it provides the opportunity for selection to limit the extent of reductive genome evolution commonly seen in obligate intracellular bacteria and to enable the evolution of adaptive genotypes.
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Bactérias/genética , Bivalves/genética , Simbiose/genética , Alelos , Animais , Sequência de Bases , Evolução Molecular , Variação Genética/genética , Genoma Bacteriano , Haplótipos/genética , Filogenia , Recombinação Genética/genéticaRESUMO
BACKGROUND: Symbioses between chemoautotrophic bacteria and marine invertebrates are rare examples of living systems that are virtually independent of photosynthetic primary production. These associations have evolved multiple times in marine habitats, such as deep-sea hydrothermal vents and reducing sediments, characterized by steep gradients of oxygen and reduced chemicals. Due to difficulties associated with maintaining these symbioses in the laboratory and culturing the symbiotic bacteria, studies of chemosynthetic symbioses rely heavily on culture independent methods. The symbiosis between the coastal bivalve, Solemya velum, and its intracellular symbiont is a model for chemosynthetic symbioses given its accessibility in intertidal environments and the ability to maintain it under laboratory conditions. To better understand this symbiosis, the genome of the S. velum endosymbiont was sequenced. RESULTS: Relative to the genomes of obligate symbiotic bacteria, which commonly undergo erosion and reduction, the S. velum symbiont genome was large (2.7 Mb), GC-rich (51%), and contained a large number (78) of mobile genetic elements. Comparative genomics identified sets of genes specific to the chemosynthetic lifestyle and necessary to sustain the symbiosis. In addition, a number of inferred metabolic pathways and cellular processes, including heterotrophy, branched electron transport, and motility, suggested that besides the ability to function as an endosymbiont, the bacterium may have the capacity to live outside the host. CONCLUSIONS: The physiological dexterity indicated by the genome substantially improves our understanding of the genetic and metabolic capabilities of the S. velum symbiont and the breadth of niches the partners may inhabit during their lifecycle.
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Bivalves/microbiologia , Ecossistema , Genoma Bacteriano , Espaço Intracelular/microbiologia , Simbiose , Animais , Composição de Bases/genética , Elementos de DNA Transponíveis/genética , Genes Bacterianos , Redes e Vias Metabólicas/genética , Dados de Sequência Molecular , Oxirredução , RNA de Transferência/genéticaRESUMO
A new lecanicephalidean genus, Seussapex gen. n., is erected for specimens collected from stingrays from the Indo-West Pacific resembling the little known species Tenia [sic] narinari MacCallum, 1917 from the spotted eagle ray, Aetobatus narinari (Euphrasen). Members of this new genus are unique in their possession of a multi-tiered apical structure comprising a bipartite apical modification of the scolex proper, and an externally bipartite apical organ with anterior and posterior glandular compartments internally. The appearance of the scolex varies dramatically depending on state of protrusion and/or evagination of these different parts which appear to be able to function independently. Seussapex karybares sp. n. parasitizing Himantura uarnak 2 (sensu Naylor et al., 2012) in northern Australia is described as the type species and Tenia [sic] narinari is transferred to the new genus. The two species differ in scolex length and width of the posterior dome-shaped portion of the apical organ. Histological sections of scoleces stained using the periodic acid-Schiff(PAS) reaction showed the surface of the anterior part of the apical organ and the anterior glandular compartment to stain PAS positive, suggesting a chemical mode of attachment to the host's intestinal mucosal surface. Extensive collecting efforts of stingrays in the Indo-West Pacific shows Seussapex gen. n. to be restricted to species of Himantura Miller et Henle and suggests additional diversity in this group of hosts. In addition, the host identity of Seussapex narinari (MacCallum, 1917) comb. n. is called into question.
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Cestoides/classificação , Cestoides/isolamento & purificação , Infecções por Cestoides/veterinária , Doenças dos Peixes/parasitologia , Rajidae , Animais , Cestoides/fisiologia , Cestoides/ultraestrutura , Infecções por Cestoides/epidemiologia , Infecções por Cestoides/parasitologia , Doenças dos Peixes/epidemiologia , Oceano Pacífico/epidemiologia , Especificidade da EspécieRESUMO
Host-microbe systems are evolutionary niches that produce coevolved biological interactions and are a key component of global health. However, these systems have historically been a difficult field of biological research due to their experimental intractability. Impactful advances in global health will be obtained by leveraging in silico screens to identify genes involved in mediating interspecific interactions. These predictions will progress our understanding of these systems and lay the groundwork for future in vitro and in vivo experiments and bioengineering projects. A driver of host-manipulation and intracellular survival utilized by host-associated microbes is molecular mimicry, a critical mechanism that can occur at any level from DNA to protein structures. We applied protein structure prediction and alignment tools to explore host-associated bacterial structural proteomes for examples of protein structure mimicry. By leveraging the Legionella pneumophila proteome and its many known structural mimics, we developed and validated a screen that can be applied to virtually any host-microbe system to uncover signals of protein mimicry. These mimics represent candidate proteins that mediate host interactions in microbial proteomes. We successfully applied this screen to other microbes with demonstrated effects on global health, Helicobacter pylori and Wolbachia , identifying protein mimic candidates in each proteome. We discuss the roles these candidates may play in important Wolbachia -induced phenotypes and show that Wobachia infection can partially rescue the loss of one of these factors. This work demonstrates how a genome-wide screen for candidates of host-manipulation and intracellular survival offers an opportunity to identify functionally important genes in host-microbe systems.
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Wolbachia is an obligate intracellular α-proteobacterium, which commonly infects arthropods and filarial nematodes. Different strains of Wolbachia are capable of a wide range of regulatory manipulations in their diverse hosts, including the modulation of host cellular differentiation to influence host reproduction. The genetic basis for the majority of these phenotypes is unknown. The wWil strain from the neotropical fruit fly, Drosophila willistoni, exhibits a remarkably high affinity for host germline-derived cells relative to the somatic cells. This trait could be leveraged for understanding how Wolbachia influences the host germline and for controlling host populations in the field. To further the use of this strain in biological and biomedical research, we sequenced the genome of the wWil strain isolated from host cell culture cells. Here, we present the first high quality Nanopore assembly of wWil, the Wolbachia endosymbiont of D. willistoni. Our assembly resulted in a circular genome of 1.27 Mb with a BUSCO completeness score of 99.7%. Consistent with other insect-associated Wolbachia strains, comparative genomic analysis revealed that wWil has a highly mosaic genome relative to the closely related wMel and wAu strains from Drosophila melanogaster and Drosophila simulans, respectively.
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Drosophila , Genoma Bacteriano , Simbiose , Wolbachia , Wolbachia/genética , Animais , Drosophila/microbiologia , Drosophila/genética , Simbiose/genética , Filogenia , Sequenciamento Completo do Genoma/métodos , Genômica/métodosRESUMO
Wolbachia is an obligate intracellular α-proteobacterium which commonly infects arthropods and filarial nematodes. Different strains of Wolbachia are capable of a wide range of regulatory manipulations in many hosts and modulate host cellular differentiation to influence host reproduction. The genetic basis for the majority of these phenotypes is unknown. The wWil strain from the neotropical fruit fly, Drosophila willistoni, exhibits a remarkably high affinity for host germline-derived cells relative to the soma. This trait could be leveraged for understanding how Wolbachia influences the host germline and for controlling host populations in the field. To further the use of this strain in biological and biomedical research, we sequenced the genome of the wWil strain isolated from host cell culture cells. Here, we present the first high quality nanopore assembly of wWil, the Wolbachia endosymbiont of D. willistoni. Our assembly resulted in a circular genome of 1.27 Mb with a BUSCO completeness score of 99.7%. Consistent with other insect-associated Wolbachia strains, comparative genomic analysis revealed that wWil has a highly mosaic genome relative to the closely related wMel strain from Drosophila melanogaster.
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The intracellular symbiont Wolbachia pipientis evolved after the divergence of arthropods and nematodes, but it reached high prevalence in many of these taxa through its abilities to infect new hosts and their germlines. Some strains exhibit long-term patterns of co-evolution with their hosts, while other strains are capable of switching hosts. This makes strain selection an important factor in symbiont-based biological control. However, little is known about the ecological and evolutionary interactions that occur when a promiscuous strain colonizes an infected host. Here, we study what occurs when two strains come into contact in host cells following horizontal transmission and infection. We focus on the faithful wMel strain from Drosophila melanogaster and the promiscuous wRi strain from Drosophila simulans using an in vitro cell culture system with multiple host cell types and combinatorial infection states. Mixing D. melanogaster cell lines stably infected with wMel and wRi revealed that wMel outcompetes wRi quickly and reproducibly. Furthermore, wMel was able to competitively exclude wRi even from minuscule starting quantities, indicating that this is a nearly deterministic outcome, independent of the starting infection frequency. This competitive advantage was not exclusive to wMel's native D. melanogaster cell background, as wMel also outgrew wRi in D. simulans cells. Overall, wRi is less adept at in vitro growth and survival than wMel and its in vivo state, revealing differences between cellular and humoral regulation. These attributes may underlie the observed low rate of mixed infections in nature and the relatively rare rate of host-switching in most strains. Our in vitro experimental framework for estimating cellular growth dynamics of Wolbachia strains in different host species, tissues, and cell types provides the first strategy for parameterizing endosymbiont and host cell biology at high resolution. This toolset will be crucial to our application of these bacteria as biological control agents in novel hosts and ecosystems.
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Bacterial symbionts that manipulate the reproduction of their hosts are important factors in invertebrate ecology and evolution, and are being leveraged for host biological control. Infection prevalence restricts which biological control strategies are possible and is thought to be strongly influenced by the density of symbiont infection within hosts, termed titer. Current methods to estimate infection prevalence and symbiont titers are low-throughput, biased towards sampling infected species, and rarely measure titer. Here we develop a data mining approach to estimate symbiont infection frequencies within host species and titers within host tissues. We applied this approach to screen ~32,000 publicly available sequence samples from the most common symbiont host taxa, discovering 2,083 arthropod and 119 nematode infected samples. From these data, we estimated that Wolbachia infects approximately 44% of all arthropod and 34% of all nematode species, while other reproductive manipulators only infect 1-8% of arthropod and nematode species. Although relative titers within hosts were highly variable within and between arthropod species, a combination of arthropod host species and Wolbachia strain explained approximately 36% of variation in Wolbachia titer across the dataset. To explore potential mechanisms for host control of symbiont titer, we leveraged population genomic data from the model system Drosophila melanogaster. In this host, we found a number of SNPs associated with titer in candidate genes potentially relevant to host interactions with Wolbachia. Our study demonstrates that data mining is a powerful tool to detect bacterial infections and quantify infection intensities, thus opening an array of previously inaccessible data for further analysis in host-symbiont evolution.
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Artrópodes , Wolbachia , Animais , Drosophila melanogaster/genética , Mineração de Dados , Ecologia , Reprodução , Wolbachia/genéticaRESUMO
The intra-host composition of horizontally transmitted microbial symbionts can vary across host populations due to interactive effects of host genetics, environmental, and geographic factors. While adaptation to local habitat conditions can drive geographic subdivision of symbiont strains, it is unknown how differences in ecological characteristics among host-symbiont associations influence the genomic structure of symbiont populations. To address this question, we sequenced metagenomes of different populations of the deep-sea mussel Bathymodiolus septemdierum, which are common at Western Pacific deep-sea hydrothermal vents and show characteristic patterns of niche partitioning with sympatric gastropod symbioses. Bathymodiolus septemdierum lives in close symbiotic relationship with sulfur-oxidizing chemosynthetic bacteria but supplements its symbiotrophic diet through filter-feeding, enabling it to occupy ecological niches with little exposure to geochemical reductants. Our analyses indicate that symbiont populations associated with B. septemdierum show structuring by geographic location, but that the dominant symbiont strain is uncorrelated with vent site. These patterns are in contrast to co-occurring Alviniconcha and Ifremeria gastropod symbioses that exhibit greater symbiont nutritional dependence and occupy habitats with higher spatial variability in environmental conditions. Our results suggest that relative habitat homogeneity combined with sufficient symbiont dispersal and genomic mixing might promote persistence of similar symbiont strains across geographic locations, while mixotrophy might decrease selective pressures on the host to affiliate with locally adapted symbiont strains. Overall, these data contribute to our understanding of the potential mechanisms influencing symbiont population structure across a spectrum of marine microbial symbioses that occupy contrasting ecological niches. IMPORTANCE Beneficial relationships between animals and microbial organisms (symbionts) are ubiquitous in nature. In the ocean, microbial symbionts are typically acquired from the environment and their composition across geographic locations is often shaped by adaptation to local habitat conditions. However, it is currently unknown how generalizable these patterns are across symbiotic systems that have contrasting ecological characteristics. To address this question, we compared symbiont population structure between deep-sea hydrothermal vent mussels and co-occurring but ecologically distinct snail species. Our analyses show that mussel symbiont populations are less partitioned by geography and do not demonstrate evidence for environmental adaptation. We posit that the mussel's mixotrophic feeding mode may lower its need to affiliate with locally adapted symbiont strains, while microhabitat stability and symbiont genomic mixing likely favors persistence of symbiont strains across geographic locations. Altogether, these findings further our understanding of the mechanisms shaping symbiont population structure in marine environmentally transmitted symbioses.
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Gastrópodes , Fontes Hidrotermais , Mytilidae , Animais , Fontes Hidrotermais/microbiologia , Mytilidae/genética , Bactérias/genética , Ecossistema , Geografia , Gastrópodes/microbiologiaRESUMO
Bacteria participate in a wide diversity of symbiotic associations with eukaryotic hosts that require precise interactions for bacterial recognition and persistence. Most commonly, host-associated bacteria interfere with host gene expression to modulate the immune response to the infection. However, many of these bacteria also interfere with host cellular differentiation pathways to create a hospitable niche, resulting in the formation of novel cell types, tissues, and organs. In both of these situations, bacterial symbionts must interact with eukaryotic regulatory pathways. Here, we detail what is known about how bacterial symbionts, from pathogens to mutualists, control host cellular differentiation across the central dogma, from epigenetic chromatin modifications, to transcription and mRNA processing, to translation and protein modifications. We identify four main trends from this survey. First, mechanisms for controlling host gene expression appear to evolve from symbionts co-opting cross-talk between host signaling pathways. Second, symbiont regulatory capacity is constrained by the processes that drive reductive genome evolution in host-associated bacteria. Third, the regulatory mechanisms symbionts exhibit correlate with the cost/benefit nature of the association. And, fourth, symbiont mechanisms for interacting with host genetic regulatory elements are not bound by native bacterial capabilities. Using this knowledge, we explore how the ubiquitous intracellular Wolbachia symbiont of arthropods and nematodes may modulate host cellular differentiation to manipulate host reproduction. Our survey of the literature on how infection alters gene expression in Wolbachia and its hosts revealed that, despite their intermediate-sized genomes, different strains appear capable of a wide diversity of regulatory manipulations. Given this and Wolbachia's diversity of phenotypes and eukaryotic-like proteins, we expect that many symbiont-induced host differentiation mechanisms will be discovered in this system.
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Artrópodes/microbiologia , Diferenciação Celular , Nematoides/microbiologia , Simbiose , Wolbachia , Animais , Genoma Bacteriano , Reprodução , Wolbachia/genéticaRESUMO
Symbiotic associations between bacteria and eukaryotes exhibit a range of transmission strategies. The rates and distributions of transmission modes have not been thoroughly investigated across associations, despite their consequences on symbiont and host evolution. To address this empirically, I compiled data from the literature on bacteria-multicellular eukaryote associations for which transmission mode data was available. Of the total 528 analyzed symbioses, 21.2% were strictly horizontally transmitted, 36.0% exhibited some form of mixed mode transmission and 42.8% were strictly vertically transmitted. Controlling for phylogenetically independent symbiosis events revealed modes were approximately equally distributed among the 113 independent associations, at 32.1%+/-0.57% horizontal, 37.8%+/-1.4% mixed mode and 31.1%+/-1.3% vertical transmission. Binning symbioses by environment revealed an abundance of vertical transmission on land and a lack of it in aquatic environments. The naturally occurring uneven distribution of taxa among environments prevented controlling for host/symbiont phylogeny. However, the results were robust over a large number of independently evolved associations, suggesting that many vertically transmitted bacteria are capable of mixed mode transmission and barriers exist that reduce the rate of horizontal transmission events. Thus, both the environment type and host/symbiont taxa influence symbiont transmission mode evolution.