Comparative transcriptomics highlights convergent evolution of energy metabolic pathways in group-living spiders.
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ABSTRACT: Although widely thought to be aggressive, solitary, and potentially cannibalistic, some spider species have evolved group-living behaviors. The distinct transition provides the framework to uncover group-living evolution. Here, we conducted a comparative transcriptomic study and examined patterns of molecular evolution in two independently evolved group-living spiders and twelve solitary species. We report that positively selected genes among group-living spider lineages are significantly enriched in nutrient metabolism and autophagy pathways. We also show that nutrient-related genes of group-living spiders convergently experience amino acid substitutions and accelerated relative evolutionary rates. These results indicate adaptive convergence of nutrient metabolism that may ensure energy supply in group-living spiders. The decelerated evolutionary rate of autophagy-related genes in group-living lineages is consistent with an increased constraint on energy homeostasis as would be required in a group-living environment. Together, the results show that energy metabolic pathways play an important role in the transition to group-living in spiders.
Project description:Filtration usually eliminates water-living bacteria. Here, we report on the complete genome sequence of Minibacterium massiliensis, a beta-proteobacteria that was recovered from 0.22-mum filtered water used for patients in the hospital. The unexpectedly large 4,110,251-nucleotide genome sequence of M. massiliensis was determined using the traditional shotgun sequencing approach. Bioinformatic analyses shows that the M. massiliensis genome sequence illustrates characteristic features of water-living bacteria, including overrepresentation of genes encoding transporters and transcription regulators. Phylogenomic analysis based on the gene content of available bacterial genome sequences displays a congruent evolution of water-living bacteria from various taxonomic origins, principally for genes involved in energy production and conversion, cell division, chromosome partitioning, and lipid metabolism. This phylogenomic clustering partially results from lateral gene transfer, which appears to be more frequent in water than in other environments. The M. massiliensis genome analyses strongly suggest that water-living bacteria are a common source for genes involved in heavy-metal resistance, antibiotics resistance, and virulence factors.
Project description:Group-living behavior is taxonomically widespread but rare in spiders. The conventional view is that the main pathways to group-living in spiders are either sub-social, where extended maternal care leads to prolonged sibling association; or communal living, where individuals aggregate to exploit a common resource. Female egg-sac guarding behavior occurs throughout kleptoparasitic spiders in the subfamily Argyrodinae (Theridiidae), while individuals in group-living species cohabit in the resource rich webs of their host spiders. These attributes fit both sub-social and communal routes to group-living, which offers new insights to study the early stages of social evolution. We investigated whether members of kleptoparasitic groups in natural populations comprise related individuals by comparing the population structure of two group-living species, Argyrodes miniaceus and A. cf. fissifrons, and two solitary species, A. fasciatus and Neospintharus trigonum. We found that: (1) genetic-spatial autocorrelation in group-living species was highest among spiders sharing the same host web and declined steeply with increasing distance, but no significant autocorrelation at any scale for solitary species; (2) there was high relatedness among group members in two cases of group-living species, which indicated relatedness was not an adhesive agent in most of the groups, but no high relatedness in solitary species; and (3) the host web boundary was not the sole predictor of genetic structures in group-living species. These results suggest that population genetic structure in the group-living species is caused by limited dispersal of group members that is favored by ecological conditions, including the nature and size of resources. In contrast, the absence of genetic structuring in populations of solitary species indicates a high level of dispersal with individual interactions unlikely to have fitness benefits.
Project description:Next-generation sequencing technology is rapidly transforming the landscape of evolutionary biology, and has become a cost-effective and efficient means of collecting exome information for non-model organisms. Due to their taxonomic diversity, production of interesting venom and silk proteins, and the relative scarcity of existing genomic resources, spiders in particular are excellent targets for next-generation sequencing (NGS) methods. In this study, the transcriptomes of six entelegyne spider species from three genera (Cicurina travisae, C. vibora, Habronattus signatus, H. ustulatus, Nesticus bishopi, and N. cooperi) were sequenced and de novo assembled. Each assembly was assessed for quality and completeness and functionally annotated using gene ontology information. Approximately 100 transcripts with evidence of homology to venom proteins were discovered. After identifying more than 3,000 putatively orthologous genes across all six taxa, we used comparative analyses to identify 24 instances of positively selected genes. In addition, between ~ 550 and 1,100 unique orphan genes were found in each genus. These unique, uncharacterized genes exhibited elevated rates of amino acid substitution, potentially consistent with lineage-specific adaptive evolution. The data generated for this study represent a valuable resource for future phylogenetic and molecular evolutionary research, and our results provide new insight into the forces driving genome evolution in taxa that span the root of entelegyne spider phylogeny.
Project description:Spiders are renowned for their efficient capture of flying insects using intricate aerial webs. How the spider nervous systems evolved to cope with this specialized hunting strategy and various environmental clues in an aerial space remains unknown. Here, we report a brain cell atlas of >30,000 single-cell transcriptomes from a web-building spider (Hylyphantes graminicola). Our analysis revealed the preservation of ancestral neuron types in spiders, including the potential coexistence of noradrenergic and octopaminergic neurons, and many peptidergic neuronal types that are lost in insects. By comparing the genome of two newly sequenced plesiomorphic burrowing spiders with three aerial web-building spiders, we found that the positively selected genes in the ancestral branch of web-building spiders were preferentially expressed (42%) in the brain, especially in the three mushroom body-like neuronal types. By gene enrichment analysis and RNAi experiments, these genes were suggested to be involved in the learning and memory pathway and may influence the spiders’ web-building and hunting behavior. Our results provide key sources for understanding the evolution of behavior in spiders and reveal how molecular evolution drives neuron innovation and the diversification of associated complex behaviors.
Project description:Spiders are renowned for their efficient capture of flying insects using intricate aerial webs. How the spider nervous systems evolved to cope with this specialized hunting strategy and various environmental clues in an aerial space remains unknown. Here we report a brain-cell atlas of >30,000 single-cell transcriptomes from a web-building spider (Hylyphantes graminicola). Our analysis revealed the preservation of ancestral neuron types in spiders, including the potential coexistence of noradrenergic and octopaminergic neurons, and many peptidergic neuronal types that are lost in insects. By comparing the genome of two newly sequenced plesiomorphic burrowing spiders with three aerial web-building spiders, we found that the positively selected genes in the ancestral branch of web-building spiders were preferentially expressed (42%) in the brain, especially in the three mushroom body-like neuronal types. By gene enrichment analysis and RNAi experiments, these genes were suggested to be involved in the learning and memory pathway and may influence the spiders' web-building and hunting behaviour. Our results provide key sources for understanding the evolution of behaviour in spiders and reveal how molecular evolution drives neuron innovation and the diversification of associated complex behaviours.
Project description:BACKGROUND:Mycobacterium smegmatis is a saprophytic bacterium frequently used as a genetic surrogate to study pathogenic Mycobacterium tuberculosis. The PrrAB two-component genetic regulatory system is essential in M. tuberculosis and represents an attractive therapeutic target. In this study, transcriptomic analysis (RNA-seq) of an M. smegmatis ΔprrAB mutant was used to define the PrrAB regulon and provide insights into the essential nature of PrrAB in M. tuberculosis. RESULTS:RNA-seq differential expression analysis of M. smegmatis wild-type (WT), ΔprrAB mutant, and complementation strains revealed that during in vitro exponential growth, PrrAB regulates 167 genes (q < 0.05), 57% of which are induced in the WT background. Gene ontology and cluster of orthologous groups analyses showed that PrrAB regulates genes participating in ion homeostasis, redox balance, metabolism, and energy production. PrrAB induced transcription of dosR (devR), a response regulator gene that promotes latent infection in M. tuberculosis and 21 of the 25 M. smegmatis DosRS regulon homologues. Compared to the WT and complementation strains, the ΔprrAB mutant exhibited an exaggerated delayed growth phenotype upon exposure to potassium cyanide and respiratory inhibition. Gene expression profiling correlated with these growth deficiency results, revealing that PrrAB induces transcription of the high-affinity cytochrome bd oxidase genes under both aerobic and hypoxic conditions. ATP synthesis was ~ 64% lower in the ΔprrAB mutant relative to the WT strain, further demonstrating that PrrAB regulates energy production. CONCLUSIONS:The M. smegmatis PrrAB two-component system regulates respiratory and oxidative phosphorylation pathways, potentially to provide tolerance against the dynamic environmental conditions experienced in its natural ecological niche. PrrAB positively regulates ATP levels during exponential growth, presumably through transcriptional activation of both terminal respiratory branches (cytochrome c bc1-aa3 and cytochrome bd oxidases), despite transcriptional repression of ATP synthase genes. Additionally, PrrAB positively regulates expression of the dormancy-associated dosR response regulator genes in an oxygen-independent manner, which may serve to fine-tune sensory perception of environmental stimuli associated with metabolic repression.
Project description:High-elevation organisms experience shared environmental challenges that include low oxygen availability, cold temperatures, and intense ultraviolet radiation. Consequently, repeated evolution of the same genetic mechanisms may occur across high-elevation taxa. To test this prediction, we investigated the extent to which the same biochemical pathways, genes, or sites were subject to parallel molecular evolution for 12 Andean hummingbird species (family: Trochilidae) representing several independent transitions to high elevation across the phylogeny. Across high-elevation species, we discovered parallel evolution for several pathways and genes with evidence of positive selection. In particular, positively selected genes were frequently part of cellular respiration, metabolism, or cell death pathways. To further examine the role of elevation in our analyses, we compared results for low- and high-elevation species and tested different thresholds for defining elevation categories. In analyses with different elevation thresholds, positively selected genes reflected similar functions and pathways, even though there were almost no specific genes in common. For example, EPAS1 (HIF2α), which has been implicated in high-elevation adaptation in other vertebrates, shows a signature of positive selection when high-elevation is defined broadly (>1,500 m), but not when defined narrowly (>2,500 m). Although a few biochemical pathways and genes change predictably as part of hummingbird adaptation to high-elevation conditions, independent lineages have rarely adapted via the same substitutions.
Project description:BackgroundWe performed an exhaustive search for local structural similarities in an ensemble of non-redundant protein functional sites. With the purpose of finding new examples of convergent evolution, we selected only those matching sites composed of structural regions whose residue order is inverted in the relative protein sequences.ResultsA novel case of local analogy was detected between members of the ABC transporter and of the HprK/P families in their ATP binding site. This case cannot be derived by events of circular permutation since the residues of one of the region pairs are located in reverse order in the sequence of the two protein families. One of the analogous binding sites, the one identified in HprK/P, is known to also bind pyrophosphate, which is used as preferred energy source in its kinase and phosphorylase activity.ConclusionThe discovery of this striking molecular similarity, also associated to a functional similarity, may help in suggesting new experiments aimed at a deeper understanding of members of the ABC transporter family known to be involved in many serious human diseases.
Project description:Radiation therapy for head and neck cancer causes damage to the surrounding salivary glands, resulting in salivary gland hypofunction and xerostomia. Current treatments do not provide lasting restoration of salivary gland function following radiation; therefore, a new mechanistic understanding of the radiation-induced damage response is necessary for identifying therapeutic targets. The purpose of the present study was to investigate the metabolic phenotype of radiation-induced damage in parotid salivary glands by integrating transcriptomic and metabolomic data. Integrated data were then analyzed to identify significant gene-metabolite interactions. Mice received a single 5 Gy dose of targeted head and neck radiation. Parotid tissue samples were collected 5 days following treatment for RNA sequencing and metabolomics analysis. Altered metabolites and transcripts significantly converged on a specific region in the metabolic reaction network. Both integrative pathway enrichment using rank-based statistics and network analysis highlighted significantly coordinated changes in glutathione metabolism, energy metabolism (TCA cycle and thermogenesis), peroxisomal lipid metabolism, and bile acid production with radiation. Integrated changes observed in energy metabolism suggest that radiation induces a mitochondrial dysfunction phenotype. These findings validated previous pathways involved in the radiation-damage response, such as altered energy metabolism, and identified robust signatures in salivary glands, such as reduced glutathione metabolism, that may be driving salivary gland dysfunction.
Project description:BackgroundGenome size and gene content in bacteria are associated with their lifestyles. Obligate intracellular bacteria (i.e., mutualists and parasites) have small genomes that derived from larger free-living bacterial ancestors; however, the different steps of bacterial specialization from free-living to intracellular lifestyle have not been studied comprehensively. The growing number of available sequenced genomes makes it possible to perform a statistical comparative analysis of 317 genomes from bacteria with different lifestyles.ResultsCompared to free-living bacteria, host-dependent bacteria exhibit fewer rRNA genes, more split rRNA operons and fewer transcriptional regulators, linked to slower growth rates. We found a function-dependent and non-random loss of the same 100 orthologous genes in all obligate intracellular bacteria. Thus, we showed that obligate intracellular bacteria from different phyla are converging according to their lifestyle. Their specialization is an irreversible phenomenon characterized by translation modification and massive gene loss, including the loss of transcriptional regulators. Although both mutualists and parasites converge by genome reduction, these obligate intracellular bacteria have lost distinct sets of genes in the context of their specific host associations: mutualists have significantly more genes that enable nutrient provisioning whereas parasites have genes that encode Types II, IV, and VI secretion pathways.ConclusionOur findings suggest that gene loss, rather than acquisition of virulence factors, has been a driving force in the adaptation of parasites to eukaryotic cells. This comparative genomic analysis helps to explore the strategies by which obligate intracellular genomes specialize to particular host-associations and contributes to advance our knowledge about the mechanisms of bacterial evolution.