Biology subjects

Zhaxybayeva, O.

Publications and source records attributed to Zhaxybayeva, O..

16 recordsLinked to original sources

bioRxiv2024

Bacterial growth temperature as a horizontally acquired polygenic trait

Evolutionary events leading to organismal preference for a specific growth temperature, as well as genes whose products are needed for a proper function at that temperature, are poorly understood. Using 64 bacteria from phylum Thermotogota as a model system, we examined how optimal growth temperature changed throughout Thermotogota history. We inferred that Thermotogotas last common ancestor was a thermophile and that some Thermotogota evolved the mesophilic and hyperthermophilic lifestyles secondarily. By modeling gain and loss of genes throughout Thermotogota history and by reconstructing their phylogenies, we demonstrated that adaptations to lower and higher growth temperature require both the acquisition of necessary genes and loss of unnecessary genes. Via a pangenome-wide association study, we correlated presence/absence of 68 gene families with specific optimal growth temperature intervals. While some of these genes are poorly characterized, most are involved in metabolism of amino acids, nucleotides, carbohydrates, and lipids, as well as in signal transduction and regulation of transcription. Most of the 68 genes have a history of horizontal gene transfer to/from other bacteria and archaea, suggesting that parallel acquisitions of genes likely promote independent adaptations of different Thermotogota species to specific growth temperatures. SignificanceWhile the currently known range of life-permitting temperatures spans from -15{degrees}C to +122{degrees}C, most living organisms, including microbes, can grow only in a narrow temperature interval around their optimal growth temperature. The genetic and genomic determinants of such preference remain poorly understood. Using genomes from Thermotogota, a group of bacteria that collectively can grow between 20{degrees} and 90{degrees}C, we detected 68 genes, presence of which strongly correlates with growth at specific optimal growth temperature. Our findings dramatically expand a list of genes that are likely important for both lowering and increasing preferred growth temperature of a microorganism. We also demonstrated that these genes were usually horizontally acquired from other bacteria and archaea that likely share environment with Thermotogota, highlighting the importance of gene exchange in microbial adaptation.

evolutionary biology↗

bioRxiv2023

Homology detection using a protein secondary structure-based large language model

Detection of homology among proteins is fundamental to understanding protein function. Unfortunately, traditional homology searches using amino acid sequence similarity are limited when numerous amino acid substitutions have accumulated either due to billions of years of evolution or through processes of accelerated change. Recent applications of deep-learning approaches demonstrate that "protein language" models of amino acid sequences can improve the accuracy of the traditional homology searches. Ultimately, the ability to work seamlessly with tertiary structures of proteins will solve the homology detection challenge and provide accompanying insights directly related to function, but to date the use of 3D structures suffers both from data availability and computational bottlenecks. Herein, we present the Protein Secondary Structure Language (ProSSL) model, an efficient encoding of protein secondary structure information in a Transformer-based deep-learning architecture. We conjecture that the secondary protein structure, which is better conserved than primary sequences and much more easily predictable and available than tertiary protein structure, could aid in the task of homology detection. ProSSL has the computational advantages of primary sequence-based homology detection, while also providing important structural information for similarity scoring. Using two case studies of large, diverse viral protein families, we show that the ProSSL model successfully captures patterns of secondary structure arrangements and is effective in detecting homologs either as a pre-trained or fine-tuned model. In both tasks, we accurately detect members of these protein families, including those missed in traditional amino acid similarity searches. We also illustrate how functional insights from the individual ProSSL models could be obtained from the use of the Shapley Additive exPlanations (SHAP) values. Author SummaryWhen DNA is obtained from an organism or an environment, scientists are tasked with determining the functions of the proteins encoded in the genetic material. Such "functional annotation" relies on assigning functions based on the similarity of the proteins to counterparts in databases comprising annotated sequence data. Especially challenging is an ability to recognize similarity in proteins that accumulated a lot of amino acid changes. It is well-known that spatial structure of proteins that share ancestry and perform similar functions evolves much slower than the sequences of the proteins amino acids. Thus, comparison of 3D structures could address this challenge, but the data is still limited to certain classes of proteins, and the requisite computations are expensive. Herein we present a deep-learning model derived from protein secondary structure representation, a symbolic encoding of the way neighboring amino acid residues of a protein interact with each other. Unlike 3D structure, the secondary structure is quickly and accurately predictable from amino acid sequences of proteins. Using two viral proteins as case studies, we demonstrate that our model works well for detection of protein similarity, including identification of very distantly related proteins.

bioinformatics↗

bioRxiv2023

Co-evolution of gene transfer agents and their alphaproteobacterial hosts

Gene transfer agents (GTAs) are enigmatic elements that resemble small viruses and are known to be produced during nutritional stress by some bacteria and archaea. The production of GTAs is regulated by quorum sensing, under which a small fraction of the population acts as GTA producers, while the rest become GTA recipients. In contrast to canonical viruses, GTAs cannot propagate themselves because they package pieces of the producing cells genome. In alphaproteobacteria, GTAs are mostly vertically inherited and reside in their hosts genomes for hundreds of millions of years. While GTAs ability to transfer genetic material within a population and their long-term preservation suggests an increased fitness of GTA-producing microbes, the associated benefits and type of selection that maintains GTAs are poorly understood. By comparing rates of evolutionary change in GTA genes to the rates in gene families abundantly present across 293 alphaproteobacterial genomes, we detected 59 gene families that likely co-evolve with GTA genes. These gene families are predominantly involved in stress response, DNA repair, and biofilm formation. We hypothesize that biofilm formation enables the physical proximity of GTA-producing cells, limiting GTA-derived benefits only to a group of closely related cells. We further conjecture that population structure of biofilm-forming sub-populations ensures that the trait of GTA production is maintained despite the inevitable rise of "cheating" genotypes. Because release of GTA particles kills the producing cell, maintenance of GTAs is an exciting example of social evolution in a microbial population. ImportanceGene transfer agents (GTAs) are viruses domesticated by some archaea and bacteria as vehicles for carrying pieces of the host genome. Produced under certain environmental conditions, GTA particles can deliver DNA to neighboring, closely related cells. Function of GTAs remains uncertain. While making GTAs is suicidal for a cell, GTA-encoding genes are widespread in genomes of alphaproteobacteria. Such GTA persistence implies functional benefits but raises question about how selection maintains this lethal trait. By showing that GTA genes co-evolve with genes involved in stress response, DNA repair, and biofilm formation, we provide support for the hypothesis that GTAs facilitate DNA exchange during the stress conditions and present a model for how GTAs persist in biofilm-forming bacterial populations despite being lethal.

evolutionary biology↗

bioRxiv2023

Early divergence and gene exchange highways in the evolutionary history of Mesoaciditogales

The placement of a non-hyperthermophilic order Mesoaciditogales at the base of Thermotogota tree challenges the prevailing hypothesis that the last common ancestor of Thermotogota was a hyperthermophile. Yet, given the long branch leading to the only two Mesoaciditogales described to-date, the phylogenetic position of the order may be due to the long branch attraction artifact. By testing various models and applying data recoding in phylogenetic reconstructions, we observed that Mesoaciditogales basal placement is strongly supported by the conserved marker genes assumed to be vertically inherited. However, based on the taxonomic content of 1,181 gene families and a phylogenetic analysis of 721 gene family trees, we also found that a substantial number of Mesoaciditogales genes are more closely related to species from the order Petrotogales. These genes contribute to coenzyme transport and metabolism, fatty acid biosynthesis, genes known to respond to heat and cold stressors, and include many genes of unknown functions. The Petrotogales comprise moderately thermophilic and mesophilic species with similar temperature tolerances to that of Mesoaciditogales. Our findings hint at extensive horizontal gene transfer between, or parallel independent gene gains by, the two ecologically similar lineages, and suggest that the exchanged genes may be important for adaptation to comparable temperature niches. SignificanceThe high-temperature phenotype is often referenced when conjecturing about characteristics of the last common ancestor of all present-day organisms. Such inferences rely on accuracy of phylogenetic trees, especially with respect to lineages that branch closest to the last common ancestor. Here, we examined evolutionary history of Mesoaciditogales, an early-branching lineage within Thermotogota phylum, which is one of the early-diverging groups of bacteria. Thermotogota is composed of thermophiles, hyperthermophiles and mesophiles, who collectively can grow between 20 to 90 degrees Celsius, making it challenging to infer the growth temperature of their common ancestor. Our analysis revealed a complex evolutionary history of Mesoaciditogales genome content impacted by horizontal gene transfer, highlighting the challenges of ancestral phenotype inferences using present-day genomes.

evolutionary biology↗

bioRxiv2022

Distribution and abundance of tetraether lipid cyclization genes in terrestrial hot springs reflects pH

Many Archaea produce membrane-spanning glycerol dibiphytanyl glycerol tetraether (GDGTs) lipids that serve as unique biomarkers of past environments. These lipids can contain up to eight cyclopentane rings, where an increase in ring cyclization is generally associated with growth in more acidic, higher temperature, or more energy limited conditions. Recently the genes that encode GDGT ring synthases, grsAB, were identified and characterized in model thermoacidophiles Sulfolobus acidocaldarius and Saccharolobus solfataricus. However, the distribution and abundance of grs homologs across environments inhabited by these and related Archaea remains unknown. To address this, we examined the distribution of grs homologs in archaeal and bacterial cultivar genomes, single cell genomes, metagenomes, and metatranscriptomes from thermal springs across the planet, where temperature, pH, and geochemical data take at time of sampling. The relative abundance of grs in these microbial communities exhibits a strong negative correlation with pH, and weak positive correlation with temperature. Genomes and metagenome-assembled genomes (MAGs) from Archaea that encode two or more copies of grs are significantly more widespread in low pH springs. Homologs of grs were detected in MAGs from 12 archaeal classes, with the most well-represented being the Thermoproteia. Homologs of grs were also detected among several classes of uncultured Archaea, including the Korarchaeia, Bathyarchaeia, and Hadarchaeia. Several Nitrososphaeria MAGs had high copy numbers of grs (> 3), and the functional role of these copies cannot yet be explained. Notably, grs genes were also found in MAGs from the bacterial class Acidobacteria. Based on phylogenetic analyses, it is likely that Acidobacteria acquired these genes horizontally from Archaea. Broadly, our results highlight the key role of grs-catalyzed lipid cyclization in the diversification of Archaea in hot and acidic environments.

microbiology↗

bioRxiv2022

Selection for translational efficiency in genes associated with alphaproteobacterial gene transfer agents

Gene transfer agents (GTAs) are virus-like elements that are encoded by some bacterial and archaeal genomes. The production of GTAs can be induced by the carbon depletion and results in host lysis and release of virus-like particles that contain mostly random fragments of the host DNA. The remaining members of a GTA-producing population act as GTA recipients by producing proteins needed for the GTA-mediated DNA acquisition. Here, we detect a codon usage bias towards codons with more readily available tRNAs in the RcGTA-like GTA genes of alphaproteobacterial genomes. Such bias likely improves the translational efficacy during GTA gene expression. While the strength of codon usage bias fluctuates substantially among individual GTA genes and across taxonomic groups, it is especially pronounced in Sphingomonadales, whose members are known to inhabit nutrient-depleted environments. By screening genomes for gene families with similar trends in codon usage biases to those in GTA genes, we found a gene that likely encodes head completion protein in some GTAs were it appeared missing, and 13 genes previously not implicated in GTA lifecycle. The latter genes are involved in various molecular processes, including the homologous recombination and transport of scarce organic matter. Our findings provide insights into the role of selection for translational efficiency in evolution of GTA genes, and outline genes that are potentially involved in the previously hypothesized integration of GTA-delivered DNA into the host genome. ImportanceHorizontal gene transfer (HGT) is a fundamental process that drives evolution of microorganisms. HGT can result a rapid dissemination of beneficial genes within and among microbial communities, and can be achieved via multiple mechanisms. One peculiar HGT mechanism involves viruses "domesticated" by some bacteria and archaea (their hosts). These so-called gene transfer agents (GTAs) are encoded in hosts genomes, produced under starvation conditions, and cannot propagate themselves as viruses. We show that GTA genes are under selection to improve efficiency of their translation when the host activates GTA production. The selection is especially pronounced in bacteria that occupy nutrient-depleted environments. Intriguingly, several genes involved in DNA incorporation into a genome are under similar selection pressure, suggesting that they may facilitate integration of GTA-delivered DNA into the host genome. Our findings underscore the potential importance of GTAs as a mechanism of HGT under nutrient-limited conditions, which are widespread in microbial habitats.

evolutionary biology↗

bioRxiv2022

Formal Recognition and Classification of Gene Transfer Agents as Viriforms

Morphological and genetic features strongly suggest that gene transfer agents (GTAs) are caudoviricete-derived entities that have evolved in concert with cellular genomes to such a degree that they should not be considered viruses. Indeed, GTA particles resemble caudoviricete virions but, in contrast to caudoviricetes (or any viruses), GTAs can encapsidate at best only part of their own genomes, are induced solely in small subpopulations of prokaryotic host cells and are transmitted vertically as part of cellular genomes during replication and division. Therefore, the lifecycles of GTAs are analogous to virus-derived entities found in parasitoid wasps, which have recently been recognized as non-virus entities and therefore reclassified as viriforms. We evaluated three distinct, independently exapted GTA groups for which the genetic basis for GTA particle production has been established. Based on the evidence, we outline a classification scheme for these viriforms.

evolutionary biology↗

bioRxiv2020

Viruses of the Thermotogota; the vehicles on the highways of gene sharing.

Phylogenomic analyses of bacteria from the phylum Thermotogota have shown extensive lateral gene transfer (LGT) with distantly related organisms, particularly with Firmicutes. One likely mechanism of such DNA transfer is viruses. However, to date only three temperate viruses have been characterized in this phylum, all infecting bacteria from the Marinitoga genus. Here we report 17 proviruses integrated into genomes of eight Thermotogota genera and induce viral particle production from one of the proviruses. The proviruses fall into two groups based on sequence similarity, gene synteny and taxonomic classification. Proviruses of one group are found in six genera and are similar to the previously identified Marinitoga viruses, while proviruses from the second group are only distantly related to the proviruses of the first group, have different genome organization and are found in only two genera. Both groups are closely related to Firmicutes in genomic and phylogenetic analyses, and one of the groups show evidence of very recent LGT and are therefore likely capable of infecting cells from both phyla. We conjecture that viruses are responsible for a large portion of the observed gene flow between Firmicutes and Thermotogota.

evolutionary biology↗

bioRxiv2020

Phylogenetic evidence of headful packaging strategy in gene transfer agents

Gene transfer agents (GTAs) are virus-like particles encoded and produced by many bacteria and archaea. Unlike viruses, GTAs package fragments of the host genome instead of the genes that encode the components of the GTA itself. As a result of this non-specific DNA packaging, GTAs can transfer genes within bacterial and archaeal communities. GTAs clearly evolved from viruses and are thought to have been maintained in prokaryotic genomes due to the advantages associated with their DNA transfer capacity. The most-studied GTA is produced by the alphaproteobacterium Rhodobacter capsulatus (RcGTA), which packages random portions of the host genome at a lower DNA density than usually observed in tailed bacterial viruses. How the DNA packaging properties of RcGTA evolved from those of the ancestral virus remains unknown. To address this question, we reconstructed the evolutionary history of the large subunit of the terminase (TerL), a highly conserved enzyme used by viruses and GTAs to package DNA. We found that RcGTA-like TerLs grouped within viruses that employ the headful packaging strategy. Because distinct mechanisms of viral DNA packaging correspond to differences in the TerL amino acid sequence, our finding suggests that RcGTA evolved from a headful packaging virus. Headful packaging is the least sequence-specific mode of DNA packaging, which would facilitate the switch from packaging of the viral genome to packaging random pieces of the host genome during GTA evolution.

evolutionary biology↗

bioRxiv2020

Nutrient supplementation experiments on saltern microbial communities support utilization of DNA as a source of phosphorus

All environments including hypersaline ones harbor measurable concentrations of dissolved extracellular DNA (eDNA) that can be utilized by microbes as a nutrient. However, it remains poorly understood which eDNA components are used, and who in a community utilizes it. For this study, we incubated a saltern microbial community with combinations of carbon, nitrogen, phosphorus, and DNA, and tracked the community response in each microcosm treatment via 16S rRNA and rpoB gene sequencing. We show that microbial communities used DNA only as a phosphorus source, and provision of other sources of carbon and nitrogen was needed to exhibit a substantial growth. The taxonomic composition of eDNA in the water column changed with the availability of inorganic phosphorus or supplied DNA, hinting at preferential uptake of eDNA from specific organismal sources. Especially favored for growth was eDNA from the most abundant taxa, suggesting some haloarchaea prefer eDNA from closely related taxa. Additionally, microcosms composition shifted substantially depending on the provided nutrient combinations. These shifts allowed us to predict supplemented nutrients from microbial composition with high accuracy, suggesting that nutrient availability in an environment could be assessed from a taxonomic survey of its microbial community.

microbiology↗

bioRxiv2020

Selection for reducing energy cost of protein production drives the GC content and amino acid composition bias in gene transfer agents

Gene transfer agents (GTAs) are virus-like elements integrated into bacterial genomes, particularly, those of Alphaproteobacteria. The GTAs can be induced under nutritional stress, incorporate random fragments of bacterial DNA into mini-phage particles, lyse the host cells and infect neighboring bacteria, thus enhancing horizontal gene transfer. We show that the GTA genes evolve under pronounced positive selection for the reduction of the energy cost of protein production as shown by comparison of the amino acid compositions with both homologous viral genes and host genes. The energy saving in GTA genes is comparable to or even more pronounced than that in the genes encoding the most abundant, essential bacterial proteins. In cases when viruses acquire genes from GTAs, the bias in amino acid composition disappears in the course of evolution, showing that reduction of the energy cost of protein is an important factor of evolution of GTAs but not bacterial viruses. These findings strongly suggest that GTAs are bacterial adaptations rather than selfish, virus-like elements. Because GTA production kills the host cell and does not propagate the GTA genome, it appears likely that the GTAs are retained in the course of evolution via kin or group selection. Therefore, we hypothesize that GTA facilitate the survival of bacterial populations under energy-limiting conditions through the spread of metabolic and transport capabilities via horizontal gene transfer and increase of nutrient availability resulting from the altruistic suicide of GTA-producing cells. ImportanceKin and group selection remain controversial topics in evolutionary biology. We argue that these types of selection are likely to operate in bacterial populations by showing that bacterial Gene Transfer Agents (GTAs), but not related viruses, evolve under positive selection for the reduction of the energy cost of a GTA particle production. We hypothesize that GTAs are dedicated devices for the survival of bacteria under the conditions of nutrient limitation. The benefits conferred by GTAs under nutritional stress appear to include horizontal dissemination of genes that could provide bacteria with enhanced capabilities for nutrient utilization and the increase of nutrient availability through the lysis of GTA-producing bacteria.

evolutionary biology↗

bioRxiv2019

Machine-learning classification suggests that many alphaproteobacterial prophages may instead be gene transfer agents

Many of the sequenced bacterial and archaeal genomes encode regions of viral provenance. Yet, not all of these regions encode bona fide viruses. Gene transfer agents (GTAs) are thought to be former viruses that are now maintained in genomes of some bacteria and archaea and are hypothesized to enable exchange of DNA within bacterial populations. In Alphaproteobacteria, genes homologous to the head-tail gene cluster that encodes structural components of the Rhodobacter capsulatus GTA (RcGTA) are found in many taxa, even if they are only distantly related to Rhodobacter capsulatus. Yet, in most genomes available in GenBank RcGTA-like genes have annotations of typical viral proteins, and therefore are not easily distinguished from their viral homologs without additional analyses. Here, we report a support vector machine classifier that quickly and accurately distinguishes RcGTA-like genes from their viral homologs by capturing the differences in the amino acid composition of the encoded proteins. Our open-source classifier is implemented in Python and can be used to scan homologs of the RcGTA genes in newly sequenced genomes. The classifier can also be trained to identify other types of GTAs, or even to detect other elements of viral ancestry. Using the classifier trained on a manually curated set of homologous viruses and GTAs, we detected RcGTA-like head-tail gene clusters in 57.5% of the 1,423 examined alphaproteobacterial genomes. We also demonstrated that more than half of the in silico prophage predictions are instead likely to be GTAs, suggesting that in many alphaproteobacterial genomes the RcGTA-like elements remain unrecognized.\n\nData depositionSequence alignments and phylogenetic trees are available in a FigShare repository at DOI 10.6084/m9.figshare.8796419. The Python source code of the described classifier and additional scripts used in the analyses are available via a GitHub repository at https://github.com/ecg-lab/GTA-Hunter-v1

genomics↗

bioRxiv2019

From morphogenesis to pathogenesis: A cellulose loosening protein is one of the most widely distributed tools in nature

Plants must rearrange the network of complex carbohydrates in their cell walls during normal growth and development. To accomplish this, all plants depend on proteins called expansins that non-enzymatically loosen hydrogen bonds between cellulose microfibrils. Because of their key role in cell wall extension during growth, expansin genes are ubiquitous, diverse, and abundant throughout all land plants. Surprisingly, expansin genes have more recently been found in some bacteria and microbial eukaryotes, where their biological functions are largely unknown. Here, we reconstruct the phylogeny of microbial expansin genes. We find these genes in all eukaryotic microorganisms that have structural cellulose in their cell walls, suggesting expansins evolved in ancient marine microorganisms long before the evolution of land plants. We also find expansins in an unexpectedly high phylogenetic diversity of bacteria and fungi that do not have cellulosic cell walls. These bacteria and fungi with expansin genes inhabit varied ecological contexts mirroring the diversity of terrestrial and aquatic niches where plant and/or algal cellulosic cell walls are present. The microbial expansin phylogeny shows evidence of multiple horizontal gene transfer events within and between bacterial and eukaryotic microbial lineages, which may in part underlie their unusually broad phylogenetic distribution. Taken together, we find expansins to be unexpectedly widespread in both bacterial and eukaryotic genetic backgrounds, and that the contribution of these genes to bacterial and fungal ecological interactions with plants and algae has likely been underappreciated.\n\nImportanceCellulose is the most abundant biopolymer on earth. In plant cell walls, where most global cellulose biomass is found, cellulose microfibrils occur intertwined with hemicelluloses and pectins. The rigidity of this polysaccharide matrix provides plant cell walls with structural support, but this rigidity also restricts cellular growth and development. Irreversible, non-enzymatic loosening of structural carbohydrates by expansin proteins is key to successful cell wall growth in plants and green algae. Here, we find that expansin genes are distributed far more broadly throughout diverse bacterial and fungal lineages lacking cellulosic cell walls than previously known. Multiple horizontal gene transfer events are in part responsible for their unusually wide phylogenetic distribution. Together, these results suggest that in addition to being the key evolutionary innovation by which eukaryotes remodel structural cellulose in their cell walls, expansins likely have remarkably broad and under-recognized utility for microbial species that interact with plant and algal structural cellulose in diverse ecological contexts.

evolutionary biology↗

bioRxiv2019

The structure of a highly conserved picocyanobacterial protein reveals a Tudor domain with a novel tRNA binding function

Cyanobacteria of the Prochlorococcus and marine Synechococcus genera are the most abundant photosynthetic microbes in the ocean. Intriguingly, the genomes of these bacteria are very divergent even within each genus, both in gene content and at amino acid level of the encoded proteins. One striking exception to this is a 62 amino acid protein, termed Prochlorococcus/Synechococcus Hyper Conserved Protein (PSHCP). PSHCP is not only found in all sequenced Prochlorococcus and marine Synechococcus genomes but it is also nearly 100% identical in its amino acid sequence across all sampled genomes. Such universal distribution and sequence conservation suggests an essential cellular role of the encoded protein in these bacteria. However, the function of PSHCP is unknown. We used Nuclear Magnetic Resonance (NMR) spectroscopy to determine its structure. We found that 52 of the 62 amino acids in PSHCP form a Tudor domain, while the remainder of the protein is disordered. NMR titration experiments revealed that PSHCP has only a weak affinity for DNA, but an 18.5 fold higher affinity for tRNA, hinting at an involvement of PSHCP in translation. Computational docking and mutagenesis studies identified a positively charged patch surrounding residue K30 that serves as the primary docking site for tRNA on PSHCP. These results provide the first insight into the structure and function of PSHCP and suggest a new function for Tudor domains in recognizing tRNA.

biochemistry↗

bioRxiv2018

An introduced crop plant is driving diversification of the virulent bacterial pathogen Erwinia tracheiphila

Erwinia tracheiphila is the causal agent of bacterial wilt of cucurbits, an economically important phytopathogen affecting few cultivated Cucurbitaceae host plant species in temperate Eastern North America. However, essentially nothing is known about E. tracheiphila population structure or genetic diversity. To address this shortcoming, a representative collection of 88 E. tracheiphila isolates was gathered from throughout its geographic range, and their genomes were sequenced. Phylogenomic analysis revealed three genetic clusters with distinct hrpT3SS virulence gene repertoires, host plant association patterns, and geographic distributions. The low genetic variation within each cluster suggests a recent population bottleneck followed by population expansion. We showed that in the field and greenhouse, cucumber (Cucumis sativus), which was introduced to North America by early Spanish conquistadors, is the most susceptible host plant species, and the only species susceptible to isolates from all three lineages. The establishment of large agricultural populations of highly susceptible C. sativus in temperate Eastern North America may have facilitated the original emergence of E. tracheiphila into cucurbit agro-ecosystems, and this introduced plant species may now be acting as a highly susceptible reservoir host. Our findings have broad implications for agricultural sustainability by drawing attention to how worldwide crop plant movement, agricultural intensification and locally unique environments may affect the emergence, evolution, and epidemic persistence of virulent microbial pathogens.\n\nImportanceErwinia tracheiphila is a virulent phytopathogen that infects two genera of cucurbit crop plants, Cucurbita spp. (pumpkin and squash) and Cucumis spp. (muskmelon and cucumber). One of the unusual ecological traits of this pathogen is that it is limited to temperate Eastern North America. Here, we complete the first large-scale sequencing of an E. tracheiphila isolate collection. From phylogenomic, comparative genomic, and empirical analyses, we find that introduced Cucumis spp. crop plants are driving the diversification of E. tracheiphila into multiple, closely related lineages. Together, the results from this study show that locally unique biotic (plant population) and abiotic (climate) conditions can drive the evolutionary trajectories of locally endemic pathogens in unexpected ways.

evolutionary biology↗

bioRxiv2017

Insights into Origin and Evolution of α-proteobacterial Gene Transfer Agents

Several bacterial and archaeal lineages produce nanostructures that morphologically resemble small tailed viruses, but, unlike most viruses, contain apparently random pieces of the host genome. Since these elements can deliver the packaged DNA to other cells, they were dubbed Gene Transfer Agents (GTAs). Because many genes involved in GTA production have viral homologs, it has been hypothesized that the GTA ancestor was a virus. Whether GTAs represent an atypical virus, a defective virus, or a virus co-opted by the prokaryotes for some function, remains to be elucidated. To evaluate these possibilities, we examined the distribution and evolutionary histories of genes that encode a GTA in the -proteobacterium Rhodobacter capsulatus (RcGTA). We report that although homologs of many individual RcGTA genes are abundant across bacteria and their viruses, RcGTA-like genomes are mainly found in one subclade of -proteobacteria. When compared to the viral homologs, genes of the RcGTA-like genomes evolve significantly slower, and do not have higher %A+T nucleotides than their host chromosomes. Moreover, they appear to reside in stable regions of the bacterial chromosomes that are generally conserved across taxonomic orders. These findings argue against RcGTA being an atypical or a defective virus. Our phylogenetic analyses suggest that RcGTA ancestor likely originated in the lineage that gave rise to contemporary -proteobacterial orders Rhizobiales, Rhodobacterales, Caulobacterales, Parvularculales, and Sphingomonadales, and since that time the RcGTA-like element has co-evolved with its host chromosomes. Such evolutionary history is compatible with maintenance of these elements by bacteria due to some selective advantage. As for many other prokaryotic traits, horizontal gene transfer played a substantial role in the evolution of RcGTA-like elements, not only in shaping its genome components within the orders, but also in occasional dissemination of RcGTA-like regions across the orders and even to different bacterial phyla.

evolutionary biology↗