Biology subjects

Russell, J. A.

Publications and source records attributed to Russell, J. A..

11 recordsLinked to original sources

bioRxiv2025

Modular evolution and strain-specific partnerships: how Hamiltonella defensa shapes defense and symbiont communities in aphids

Insects frequently carry maternally-transmitted endosymbionts that mediate ecological interactions, including resource acquisition and host defense. All pea aphids (Acyrthosiphon pisum), for example, carry the obligate nutritional symbiont Buchnera, while most have one or more of the seven heritable facultative symbionts, which play diverse roles. A common symbiont, Hamiltonella defensa, confers protection against the parasitic wasp Aphidius ervi via a toxin-bearing bacteriophage called APSE, with strain-level variation in protection best predicted by APSE variant. Yet, little is known about Hamiltonella/APSE strain variation in the field, resulting in an incomplete understanding of the full arsenal of symbiont defenses and how these change over space and time. Here, we characterized Hamiltonella/APSE diversity in over 3,000 field-collected aphids from two North American populations across multiple years. We identified bacterial strains representing five Hamiltonella clades, seven APSE variants, and numerous toxin alleles, resulting in at least 38 distinct combinations. We found that APSEs moved laterally among Hamiltonella strains more readily than toxins among phage backbones, together generating modular defensive diversity. Hamiltonella strains exhibited strain-specific coinfection preferences with other symbionts, particularly Fukatsuia, Rickettsia, and Rickettsiella, indicating strain-level structuring of heritable bacterial communities. Geographic and temporal analyses revealed dramatic regional differences and rapid population turnover, with combinations conferring intermediate laboratory protection dominating despite the decline of highly protective strains, suggesting ecological success goes beyond parasitoid resistance alone. This extensive cryptic diversity provides standing genetic variation enabling rapid evolutionary responses to biological control efforts and anthropogenic stressors, including climate change, with implications for pest management and host adaptation.

evolutionary biology↗

bioRxiv2025

ORF1ab Codon Frequency Model Predicts Host-Pathogen Relationship in Orthocoronavirinae

Predicting phenotypic properties of a virus directly from its sequence data is an attractive goal for viral epidemiology. Here, we focus narrowly on the Orthocoronavirinae clade and demonstrate models that are powerfully predictive for a human-pathogen phenotype with >86% average precision and >99% average recall on the withheld test set groups, using only Orf1ab codon frequencies. We show alternative examples for other viral coding sequences and feature representations that do not perform well and discuss what distinguishes the models that are performant. These models point to a small subset of features, specifically 5 codons, that are critical to the success of the models. We discuss and contextualize how this observation may fit within a larger model for the role of translation in virus-host agreement.

bioinformatics↗

bioRxiv2023

ANOTHER TOOL IN THE TOOLBOX: Wolbachia-mediated protection against a specialized fungal pathogen of aphids

Aphids harbor nine heritable facultative symbionts, most mediating one or more ecological interactions. However, one aphid symbiont, Wolbachia, has eluded functional characterization despite being well-studied in other arthropods. In Pentalonia aphids, global pests of banana, Wolbachia was hypothesized to function as a co-obligate symbiont alongside the traditional obligate Buchnera, but subsequent genomic analyses failed to support this role. Sampling across multiple aphid populations, we found that > 80% of Pentalonia aphids carried a M-supergroup strain of Wolbachia named wPni. While the lack of fixation confirms that Wolbachia is not a co-obligate symbiont, the high infection frequencies in these entirely asexual aphids strongly suggested Wolbachia confers net fitness benefits. Finding no correlation between Wolbachia and aphid food plants use, we challenged Wolbachia-infected aphids with common natural enemies. While Wolbachia did not protect aphids against parasitoids, this symbiont conferred significant protection against the specialized fungal pathogen, Pandora neoaphidis, and improved aphid fitness in the absence of enemy challenge. Thus, we identified a new phenotype for the multifaceted Wolbachia and highlight a system that provides unique opportunities to merge key models of heritable symbiosis to better understand infection dynamics in nature and mechanisms underpinning symbiont-mediated phenotypes. IMPORTANCE: Wolbachia symbionts spread and persist in a wide range of arthropods and nematodes by using a range of functional strategies, including reproductive manipulation, providing protection against viral and bacterial pathogens or by provisioning nutrients. Despite being one of the best-studied symbionts, little is known about the strains that infect aphids. In this study, we characterized the functional role of a Supergroup M Wolbachia strain infecting strictly asexual aphids of the genus Pentalonia. We report for the first time that this symbiont also defends against fungal entomopathogens and expand on the range of phenotypes conferred by this multifaceted symbiont.

microbiology↗

bioRxiv2022

Microbial symbionts are shared between ants and their associated beetles

The transmission of microbial symbionts across individuals and generations can be critical for animal development and survival. Likewise, the transmission of microbes across closely interacting species could also affect host biology. Army ants (Formicidae: Dorylinae) and their hundreds of closely associated insect species (myrmecophiles) can provide a unique insight into interspecific symbiont sharing. Here, we compared the microbiota of workers and larvae of the army ant Eciton burchellii with those of 13 myrmecophile beetle species using 16S rRNA amplicon sequencing. We found that the previously characterized symbionts of army ant workers (Unclassified Firmicutes and Unclassified Entomoplasmatales) were largely absent from ant larvae and from myrmecophiles, whose microbial communities were usually dominated by Rickettsia, Wolbachia, Rickettsiella, and/or Weissella. Strikingly, different species of myrmecophiles and ant larvae often shared identical 16S rRNA genotypes of common bacteria. In particular, army ant larvae, some workers, and several myrmecophile species often hosted identical Weissella (Lactobacillales), based on 16S rRNA and also protein-coding gene sequences. Also, we found high relatedness between some newly characterized Weissella and animal-associated strains from aquatic and marine habitats. Looking more broadly, we found Weissella OTUs in 11.6% of samples from nearly all habitats and environments characterized by the Earth Microbiome Project. Together, our data show that unrelated but closely interacting species can share much of their microbiota. The high relatedness of strains found across such disparate hosts as ants, beetles, trout, and whales suggests that some versatile microbes move between hosts and habitats despite few opportunities for direct interaction.

ecology↗

bioRxiv2021

A Genotype-to-Phenotype Modeling Framework to Predict Human Pathogenicity of Novel Coronaviruses

Leveraging prior viral genome sequencing data to make predictions on whether an unknown, emergent virus harbors a phenotype-of-concern has been a long-sought goal of genomic epidemiology. A predictive phenotype model built from nucleotide-level information alone has previously been considered un-tenable with respect to RNA viruses due to the ultra-high intra-sequence variance of their genomes, even within closely related clades. Building from our prior work developing a degenerate k-mer method to accommodate this high intra-sequence variation of RNA virus genomes for modeling frameworks, and leveraging a taxonomic group-shuffle-split paradigm on complete coronavirus assemblies from prior to October 2018, we trained multiple regularized logistic regression classifiers at the nucleotide k-mer level capable of accurately predicting withheld SARS-CoV-2 genome sequences as human pathogens and accurately predicting withheld Swine Acute Diarrhea Syndrome coronavirus (SADS-CoV) genome sequences as non-human pathogens. LASSO feature selection identified several degenerate nucleotide predictor motifs with high model coefficients for the human pathogen class that were present across widely disparate classes of coronaviruses. However, these motifs differed in which genes they were present in, what specific codons were used to encode them, and what the translated amino acid motif was. This emphasizes the importance of a phenetic view of emerging pathogenic RNA viruses, as opposed to the canonical phylogenetic interpretations most-commonly used to track and manage viral zoonoses. Applying our model to more recent Orthocoronavirinae genomes deposited since October 2018 yields a novel contextual view of pathogen-potential across bat-related, canine-related, porcine-related, and rodent-related coronaviruses and critical adaptations which may have contributed to the emergence of the pandemic SARS-CoV-2 virus. Finally, we discuss the utility of these predictive models (and their associated predictor motifs) to novel biosurveillance protocols that substantially increase the pound-for-pound information content of field-collected sequencing data and make a strong argument for the necessity of routine collection and sequencing of zoonotic viruses.

bioinformatics↗

bioRxiv2021

The secrets to domestic bliss - Partner fidelity and environmental filtering preserve stage-specific turtle ant gut symbioses for over 40 million years

BackgroundGut microbiomes can vary across development, a pattern often found for insects with complete metamorphosis. With varying nutritional need and distinct opportunities for microbial acquisition, questions arise as to how such holometabolous insects retain helpful microbes at larval and adult stages. Ants are an intriguing system for such study. In a number of lineages adults digest only liquid food sources, while larvae digest solid foods. Like some other social insects, workers and soldiers of some ant species engage in oral-anal trophallaxes, enabling microbial transfer among siblings. But do queens, the typical colony founding caste, obtain symbionts through such transfer? Does this enable transgenerational symbiont passage? And does the resulting partner fidelity promote the evolution of beneficial symbionts? Furthermore, how might such adult-centric biology shape larval microbiomes? To address these questions, we characterized symbiotic gut bacteria across 13 species of Cephalotes turtle ants, with up to 40-million years of divergence. Adding to the prior focus on workers we, here, study underexplored castes and stages including queens, soldiers, and larvae, by performing 16S rRNA qPCR, amplicon sequencing, and phylogenetic classification. ResultsWe show that adult microbiomes are conserved across species and largely across castes. Nearly 95% of the bacteria in adults have, thus far, been found only in Cephalotes ants. Furthermore, the microbiomes from most adults exhibit phylosymbiosis, a trend in which microbiome community similarity recapitulates patterns of host relatedness. Additionally, an abundant, adult-enriched symbiont cospeciates with some Cephalotes. Evidence here suggests that these partner fidelity patterns extend from transgenerational symbiont transfer through alate gyne dispersal and subsequent colony-founding by queens. Like adults, larvae of Cephalotes species exhibit strong microbiome conservation. Phylosymbiosis patterns are weaker, however, with further evidence elevating environmental filtering as a primary mechanism behind such conservation. Specifically, while adult-enriched symbionts are found in most larvae, symbionts of older larvae are highly related to free-living bacteria from the Enterobacteriaceae, Lactobacillales, and Actinobacteria. ConclusionsOur findings suggest that both partner fidelity and conserved environmental filtering drive stable, stage-specific, social insect symbioses. We discuss the implications for our broader understanding of insect microbiomes, and the means of sustaining a beneficial microbiome.

evolutionary biology↗

bioRxiv2021

In their sister's footsteps: Taxonomic divergence obscures substantial functional overlap among the metabolically diverse symbiotic gut communities of adult and larval turtle ants

Gut bacterial symbionts can support animal nutrition by facilitating digestion and providing valuable metabolites. While the composition of gut symbiont communities shifts with host development in holometabolous insects, changes in symbiotic roles between immature and adult stages are not well documented, especially in ants. Here, we explored the metabolic capabilities of microbiomes sampled from herbivorous turtle ant (Cephalotes sp.) larvae and adult workers through genomic and metagenomic screenings and targeted in vitro metabolic assays. We reveal that larval guts harbor bacterial symbionts from the Enterobacteriales, Lactobacillales and Rhizobiales orders, with impressive metabolic capabilities, including catabolism of plant and fungal recalcitrant fibers common in turtle ant diets, and energy-generating fermentation. Additionally, several members of the specialized turtle ant adult gut microbiome, sampled downstream of an anatomical barrier that dams large food particles, show a conserved potential to depolymerize many dietary fibers and other carbohydrates. Symbionts from both life stages have the genomic capacity to recycle nitrogen, synthesize amino acids and B-vitamins, and perform several key aspects of sulfur metabolism. We also document, for the first time in ants, an adult-associated Campylobacterales symbiont with an apparent capacity to anaerobically oxidize sulfide, reduce nitrate, and fix carbon dioxide. With help of their gut symbionts, including several bacteria likely acquired from the environment, turtle ant larvae appear as an important component of turtle ant colony digestion and nutrition. In addition, the conserved nature of the digestive, energy-generating, and nutritive capacities among adult-enriched symbionts suggests that nutritional ecology of turtle ant colonies has long been shaped by specialized, behaviorally-transferred gut bacteria with over 46 million years of residency.

evolutionary biology↗

bioRxiv2020

PanGIA: A Metagenomics Analytical Framework for RoutineBiosurveillance and Clinical Pathogen Detection

Metagenomics is emerging as an important tool in biosurveillance, public health, and clinical applications. However, ease-of-use for execution and data analysis remains a barrier-of-entry to the adoption of metagenomics in applied health and forensics settings. In addition, these venues often have more stringent requirements for reporting, accuracy, and precision than the traditional ecological research role of the technology. Here, we present PanGIA (Pan-Genomics for Infectious Agents), a novel bioinformatics analysis platform for hosting, processing, analyzing, and reporting shotgun metagenomics data of complex samples suspected of containing one or more pathogens. PanGIA was developed to address gaps that often preclude clinicians, medical technicians, forensics personnel, or other non-expert end-users from the routine application of metagenomics for pathogen identification. Though primarily designed to detect pathogenic microorganisms within clinical and environmental metagenomics data, PanGIA also serves as an analytical framework for microbial community profiling and comparative metagenomics. To provide statistical confidence in PanGIAs taxonomic assignments, the system provides two independent estimations of probability for species and strain level detection. First, PanGIA integrates coverage data with uniqueness information mapped across each reference genome for a stand-alone determination of confidence for each query sequence at each taxonomy level. Second, if a negative-control sample is provided, PanGIA compares this sample with a corresponding experimental unknown sample and determines a measure of confidence associated with detection above background. An integrated graphical user interface allows interactive interrogation and enables users to summarize multiple sample results by confidence score, normalized read abundance, reference genome linear coverage, depth-of-coverage, RPKM, and other metrics to detect specific organisms-of-interest. Comparison testing of the PanGIA algorithm against a number of recent k-mer, read-mapping, and marker-gene based taxonomy classifiers across various real-world datasets with spiked targets shows superior mean positive predictive value, sensitivity, and specificity. PanGIA can process a five million paired-end read dataset in under 1 hour on commodity computational hardware. The source code and documentation are publicly available at https://github.com/LANL-Bioinformatics/PanGIA or https://github.com/mriglobal/PanGIA. The database for PanGIA can be downloaded from ftp://bioinformatics.mriglobal.org/. The full GUI-based PanGIA analysis environment is available in a Docker container and can be installed from https://hub.docker.com/r/poeli/pangia/.

bioinformatics↗

bioRxiv2020

Vorpal: A Novel RNA Virus Feature-Extraction Algorithm Demonstrated Through Interpretable Genotype-to-Phenotype Linear Models

In the analysis of genomic sequence data, so-called "alignment free" approaches are often selected for their relative speed compared to alignment-based approaches, especially in the application of distance comparisons and taxonomic classification1,2,3,4. These methods are typically reliant on excising K-length substrings of the input sequence, called K-mers5. In the context of machine learning, K-mer based feature vectors have been used in applications ranging from amplicon sequencing classification to predictive modeling for antimicrobial resistance genes6,7,8. This can be seen as an analogy of the "bag-of-words" model successfully employed in natural language processing and computer vision for document and image classification9,10. Feature extraction techniques from natural language processing have previously been analogized to genomics data11; however, the "bag-of-words" approach is brittle in the RNA virus space due to the high intersequence variance and the exact matching requirement of K-mers. To reconcile the simplicity of "bag-of-words" methods with the complications presented by the intrinsic variance of RNA virus space, a method to resolve the fragility of extracted K-mers in a way that faithfully reflects an underlying biological phenomenon was devised. Our algorithm, Vorpal, allows the construction of interpretable linear models with clustered, representative degenerate K-mers as the input vector and, through regularization, sparse predictors of binary phenotypes as the output. Here, we demonstrate the utility of Vorpal by identifying nucleotide-level genomic motif predictors for binary phenotypes in three separate RNA virus clades; human pathogen vs. non-human pathogen in Orthocoronavirinae, hemorrhagic fever causing vs. non-hemorrhagic fever causing in Ebolavirus, and human-host vs. non-human host in Influenza A. The capacity of this approach for in silico identification of hypotheses which can be validated by direct experimentation, as well as identification of genomic targets for preemptive biosurveillance of emerging viruses, is discussed. The code is available for download at https://github.com/mriglobal/vorpal.

bioinformatics↗

bioRxiv2017

Unbiased Strain-Typing of Arbovirus Directly from Mosquitoes Using Nanopore Sequencing: A Field-forward Biosurveillance Protocol

The future of infectious disease surveillance and outbreak response is trending towards smaller hand-held solutions for point-of-need pathogen detection.1-4 Although recent advances have paved the way for these technologies to include sequencing of pathogens directly from clinical samples, the ability to carry out unbiased sequencing for pathogen discovery and subtyping directly from environmental samples has yet to be demonstrated with hand-held platforms.5 Products such as the two3 qPCR system from Biomeme Inc., as well as the MinION from Oxford Nanopore Technologies, have generated renewed prospects for point-of-need diagnostics and near real-time environmental testing and characterization of viral and microbial pathogens. Here, samples of Culex cedecei mosquitoes collected in Southern Florida, USA were tested for Venezuelan Equine Encephalitis Virus (VEEV), a previously-weaponized arthropod-borne RNA-virus capable of causing acute and fatal encephalitis in animal and human hosts. A single 20-mosquito pool tested positive for VEEV by real-time reverse transcription quantitative PCR (RT-qPCR) on the Biomeme two3. The virus-positive sample was then subjected to unbiased metatranscriptome sequencing on the MinION and determined to contain Everglades Virus (EVEV), a strain of VEEV transmitted exclusively by Culex cedecei in South Florida. The result was confirmed on \"gold standard\" thermocyclers and sequencing machines, and comparison to nanopore results is discussed. Our results demonstrate, for the first time, the use of unbiased sequence-based detection and subtyping of a high-consequence biothreat pathogen directly from an environmental sample using field-forward hardware and protocols. The further development and validation of methods designed for field-based diagnostic metagenomics and pathogen discovery, such as those suitable for use in mobile \"pocket laboratories\", will address a growing demand for public health teams to carry out their mission where it is most urgent: at the point-of-need.6

genomics↗

bioRxiv2016

The structured diversity of specialized gut symbionts of the New World army ants

Symbiotic bacteria play important roles in the biology of their arthropod hosts. Yet the microbiota of many diverse and influential groups remain understudied, resulting in a paucity of information on the fidelities and histories of these associations. Motivated by prior findings from a smaller scale, 16S rRNA-based study, we conducted a broad phylogenetic and geographical survey of microbial communities in the ecologically dominant New World army ants (Formicidae: Dorylinae). Amplicon sequencing of the 16S rRNA gene across 28 species spanning the five New World genera showed that the microbial communities of army ants consist of very few common and abundant bacterial species. The two most abundant microbes, referred to as Unclassified Firmicutes and Unclassified Entomoplasmatales, appear to be specialized army ant associates that dominate microbial communities in the gut lumen of three host genera, Eciton, Labidus and Nomamyrmex. Both are present in other army ant genera, including those from the Old World, suggesting that army ant symbioses date back to the Cretaceous. Extensive sequencing of bacterial protein-coding genes revealed multiple strains of these symbionts co-existing within colonies, but seldom within the same individual ant. Bacterial strains formed multiple host species-specific lineages on phylogenies, which often grouped strains from distant geographic locations. These patterns deviate from those seen in other social insects, and raise intriguing questions about the influence of army ant colony swarm-founding and within-colony genetic diversity on strain co-existence, and the effects of hosting a diverse suite of symbiont strains on colony ecology.

evolutionary biology↗