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Dona, J.

Publications and source records attributed to Dona, J..

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Designing AI-programmable therapeutics with the EDEN family of foundation models

The ability to interpret, modify, and design DNA has driven many of the most significant advances in modern medicine, from diagnostics, biologics, and vaccines to cell and gene therapies. However, the inherent complexity of biological systems means that most modern medicines are still engineered using bespoke, labor-intensive processes. To address the need for a generalisable and programmable approach to therapeutic design, we introduce the EDEN (environmentally-derived evolutionary network) family of metagenomic foundation models, including a 28 billion parameter model trained on 9.7 trillion nucleotide tokens from BaseData1. This dataset, at the time of training, contained more than 10 billion novel genes from over 1 million new species, and is intentionally enriched for environmental and host-associated metagenomes, phage sequences, and mobile genetic elements, enabling the model to learn from diverse and novel cross-species evolutionary mechanisms and apply them to key challenges in human health. EDEN achieves state-of-the-art performance across a series of predictive and generative genomic and protein benchmarks. To demonstrate the models broad applicability across biology, we evaluate EDENs capacity for programmable therapeutic design by challenging a single architecture to design biological novelty across three distinct therapeutic modalities, disease areas and biological scales: (i) large gene insertion, (ii) antibiotic peptide design, and (iii) microbiome design. First, we demonstrate AI-programmable Gene Insertion (aiPGI), in which EDEN designs de novo large serine recombinases (LSRs) capable of inserting large pieces of DNA at desired target sites in the human genome when prompted only on 30 nucleotides of DNA sequence from the desired target site. In low-N experimental validation, EDEN generated multiple active recombinases for all tested disease-associated genomic loci (ATM, DMD, F9, FANCC, GALC, IDS, P4HA1, PHEX, RYR2, USH2A) and 4 potential safe harbor sites in the human genome. EDEN achieves an overall functional hit rate of 63.2% across diverse DNA prompts when prompted on only 30bp of DNA from outside the training data. 50% of EDEN-generated LSRs were active in human cells, achieving therapeutically relevant levels of CAR insertion in primary human T cells. We also show that EDEN can generate active bridge recombinases when prompted on the associated guide RNA alone, with sequence identities to training and public data as low as 65%. These results pave the way for a new generation of cell and gene therapies by opening the door to rapid, programmable and site-specific integration of large genetic payloads without double-strand breaks. This offers an alternative to the safety, efficiency and payload limitations inherent in viral or nuclease-based editing at thousands of currently intractable human therapeutic targets. Second, we use the same model to generate a focused low-N library of novel antimicrobial peptides where 97% showed activity, with top candidates achieving single-digit micromolar potency against critical-priority multidrug-resistant pathogens. Third, to demonstrate that EDEN captures inter-genomic features, we design a gigabase-scale microbiome with over 94,000 synthetic metagenomic assemblies, including prophage genomes and correct cross-species metabolic pathway completions. The EDEN-generated synthetic microbiome covers 9,067 species with a biome-specific taxonomic accuracy of 99%. Over 1,500 of the generated species were outside the fine-tuning dataset while retaining the correct microecological properties and biome association, thus significantly expanding genetic and taxonomic diversity. Together, these results establish a new strategic direction for AI-programmable therapeutics, in which a single foundation model architecture designs candidate therapeutics across diverse modalities and disease areas. This suggests that the combination of billions of years of evolutionary data with specific therapeutic records offers a clear, scaling-driven path to making therapeutic design a predictable engineering discipline. O_FIG O_LINKSMALLFIG WIDTH=141 HEIGHT=200 SRC="FIGDIR/small/699009v2_ufig1.gif" ALT="Figure 1"> View larger version (59K): org.highwire.dtl.DTLVardef@68c20borg.highwire.dtl.DTLVardef@19b8e8corg.highwire.dtl.DTLVardef@1ab9362org.highwire.dtl.DTLVardef@1592cb7_HPS_FORMAT_FIGEXP M_FIG C_FIG

genomics↗

A phylogenomic framework for avian feather lice (Phthiraptera: Ischnocera)

Comprehensive phylogenies serve as foundations for taxonomic, comparative, and coevolutionary studies. Avian feather lice comprise the most diverse Parvorder (Ischnocera) of parasitic lice (Phthiraptera). Convergence and reduction of morphological features in this group have made past attempts at understanding the evolutionary relationships of feather lice challenging. Several recent phylogenomic studies have begun shedding light on the broader scale evolutionary tree of this group. However, additional taxonomic sampling is needed for a more complete understanding of the phylogeny and for higher statistical power in comparative studies. Here we investigate the higher-level relationships of feather lice based on the most comprehensive taxon sample to date. We leverage genome sequences of 260 samples of feather lice and 25 outgroup taxa to reconstruct a phylogenomic tree based on 2,395 target nuclear ortholog genes, using both concatenated and coalescent methods. These trees provide high support across nearly all branches of the topology, resolving backbone relationships as well as more detailed relationships within major groups. These phylogenies provide a framework for future comparative studies of feather lice, including comparisons with avian phylogeny and investigating patterns of diversification.

evolutionary biology↗

Independent and repeated acquisition of endosymbiotic bacteria across the diversification of feather lice

Many parasitic insects, including lice, form close relationships with endosymbiotic bacteria that are crucial for their survival. In this study, we used genomic sequencing to investigate the distribution and evolutionary history of the bacterial genus Sodalis across a broad range of feather louse species spanning 156 genera. Phylogenomic analysis revealed significant diversity among Sodalis lineages in feather lice, and robust evidence for their independent and repeated acquisition by different louse clades throughout their radiation. Among the 1,020 louse genomes analyzed, at least 22% contained Sodalis, distributed across 57 louse genera. Cophylogenetic analyses between the Sodalis and feather louse phylogenies indicated considerable mismatch. This phylogenetic incongruence between lice and Sodalis, along with the presence of distantly related Sodalis lineages in otherwise closely related louse species, strongly indicates repeated independent acquisition of this endosymbiont. Additionally, evidence of cospeciation among a few closely related louse species, coupled with frequent acquisition of these endosymbionts from free-living bacteria, further highlights the diverse evolutionary processes shaping Sodalis endosymbiosis in feather lice.

evolutionary biology↗

Origin and diversification of a globally distributed group of parasitic feather lice

Despite their extensive diversity and ecological importance, the history of diversification for most groups of parasitic organisms remains relatively understudied. Elucidating broad macroevolutionary patterns of parasites is challenging, often limited by the availability of samples, genetic resources, and knowledge about ecological relationships with their hosts. In this study, we explore the macroevolutionary history of parasites by focusing on parasitic body lice from doves. Building on extensive knowledge of ecological relationships and previous phylogenomic studies of their avian hosts, we tested specific questions about the evolutionary origins of the body lice of doves, leveraging whole genome data sets for phylogenomics. Specifically, we sequenced whole genomes from 68 samples of dove body lice, including representatives of all body louse genera from 51 host taxa. From these data, we assembled >2,300 nuclear genes to estimate dated phylogenetic relationships among body lice and several outgroup taxa. The resulting phylogeny of body lice was well supported, although some branches had conflicting signal across the genome. We then reconstructed ancestral biogeographic ranges of body lice and compared the body louse phylogeny to phylogeny of doves, and also to a previously published phylogeny of the wing lice of doves. Divergence estimates placed the origin of body lice in the late Oligocene. Body lice likely originated in Australasia and dispersed with their hosts during the early Miocene, with subsequent codivergence and host switching throughout the world. Notably, this evolutionary history is very similar to that of dove wing lice, despite the stronger dispersal capabilities of wing lice compared to body lice. Our results highlight the central role of hosts in driving macroevolutionary patterns of their parasites over long periods of time.

evolutionary biology↗

Phylogenomics and biogeography of the feather lice (Phthiraptera: Ischnocera) of parrots

Avian feather lice (Phthiraptera: Ischnocera) have undergone morphological diversification into ecomorphs based on the mechanism for escaping host preening defenses. Parrot lice are one prominent example of this phenomenon, with wing, body, or head louse ecomorphs occurring on various groups of parrots. Currently defined genera of parrot lice typically correspond to this ecomorphological variation. Here we explore the phylogenetic relationships among parrot feather lice by sequencing whole genomes and assembling a target set of 2,395 nuclear protein coding genes. Phylogenetic trees based on concatenated and coalescent analyses of these data reveal highly supported trees with strong agreement between methods of analysis. These trees reveal that parrot feather lice fall into two separate clades that form a grade with respect to the Brueelia-complex. All parrot louse genera sampled by more than one species were recovered as monophyletic. The evolutionary relationships among these lice showed evidence of strong biogeographic signal, which may also be related to the relationships among their hosts.

evolutionary biology↗

Mitogenome fragmentation evolves multiple times within a major group of parasitic lice

Animal mitochondrial genomes (mitogenomes) typically exhibit a highly conserved gene content and organisation, with genes encoded on a single circular chromosome. However, many species of parasitic lice (Insecta: Phthiraptera) are notable exceptions, having mitogenomes fragmented into multiple circular chromosomes. To understand the process of mitogenome fragmentation, we conducted a large-scale genomic study of a major group of lice, Amblycera, with extensive taxon sampling. Analyses of the evolution of mitogenome structure across a phylogenomic tree of 90 samples from 53 genera, revealed evidence for multiple independent origins of mitogenome fragmentation, some inferred to have occurred less than five million years ago. We leveraged these many independent origins of fragmentation to compare the rates of DNA substitution and gene rearrangement, specifically contrasting branches with fragmented and non-fragmented mitogenomes. We found that lineages with fragmented mitochondrial genomes had significantly higher rates of mitochondrial sequence evolution. In addition, lineages with fragmented mitochondrial genomes were more likely to have mitogenome gene rearrangements than those with single-chromosome mitochondrial genomes. By combining phylogenomics and mitochondrial genomics we provide a detailed portrait of mitogenome evolution across this group of insects with a remarkably unstable mitogenome structure, identifying processes of molecular evolution that are correlated with mitogenome fragmentation. Author SummaryMitochondria are organelles that play a key role in providing energy to cells essential for life. The structure of the mitochondrial genome is conserved across most animal groups, being a single circular chromosome containing 37 genes. Deviations from this structure are typically detrimental and associated with some human diseases. However, in very few animal groups, the mitochondrial genome is fragmented into multiple circular chromsomes. In one group of insects, parasitic lice, fragmentation varies among species, with some having a complete circular genome and others having their mitochondrial genome fragmented in two or more smaller chromosomes. Here, we use whole genome sequencing reads to analyze an unprecedented number of species from a diverse group of lice (Amblycera) that exhibits both single-chromosome and fragmented mitochondrial genomes to understand how this fragmentation evolved. We found that fragmentation evolved many times independently in this group and this fragmentation is correlated faster rates mitochondrial molecular evolution and with an increased frequency of gene rearrangement. We also provide evidence that the rate of mitochondrial genome fragmentation changes over time. Altogether, our combination of broad sampling and phylogenomic and comparative analyses provide new insights into the mechanisms and dynamics of mitochondrial genome fragmentation.

molecular biology↗

Host space, not energy or symbiont size, constrains feather mite abundance across passerine bird species

Comprehending symbiont abundance among host species is a major ecological endeavour, and the metabolic theory of ecology has been proposed to understand what constraints symbiont populations. We parameterized metabolic theory equations to predict how bird species body size and the body size of their feather mites relate to mite abundance according to four potential energy (microbial abundance, uropygial gland size) and space constraints (wing area, number of feather barbs). Predictions were compared with the empirical scaling of feather mite abundance from 26,604 birds of 106 passerine species, using phylogenetic modelling and quantile regression. Feather mite populations were strongly constrained by host space (number of feather barbs) and not energy. Moreover, feather mite species body size was unrelated to their abundance or to the body size of their host species. We discuss the implications of our results for our understanding of the bird-feather mite system and for symbiont abundance in general.

ecology↗

Nano-computed tomography reveals repeated phenotypic divergence in parasites to escape host defense

Understanding how selective pressures drive morphological change is a central question in evolutionary biology. Feather lice have repeatedly diversified into convergent ecomorphs, based on how they escape from host defenses in different microhabitats. Here, we used nano-computed tomography scan data of 89 specimens of feather lice, belonging to four ecomorph groups to quantify variation of functional traits, including mandibular muscle volume, limb length, and three-dimensional head shape data in these tiny insects. The results suggest that the shape of the head, the proportional volume of the chewing muscles, and the length of the leg segments in feather lice are all strongly associated with specific host-habitats. Further, species that co-occur on hosts have increased rates of morphological evolution, suggesting competition for host space is one of the drivers of morphology. This supports previous work indicating that the phenotypic diversity of feather lice is the result of repeated convergence resulting from resource partitioning, microhabitat specialization, and selection pressures imposed by host defense.

evolutionary biology↗

Host body size, not host population size, predicts genome-wide effective population size of parasites

The effective population size (Ne) of an organism is expected to be generally proportional to the total number of individuals in a population. In parasites, we might expect the effective population size to be proportional to host population size and host body size, because both are expected to increase the number of parasite individuals. However, among other factors, parasite populations are sometimes so extremely subdivided that high levels of inbreeding may distort these predicted relationships. Here, we used whole-genome sequence data from dove parasites (71 feather louse species of the genus Columbicola) and phylogenetic comparative methods to study the relationship between parasite effective population size and host population size and body size.We found that parasite effective population size is largely explained by host body size but not host population size. These results suggest the potential local population size (infrapopulation or deme size) is more predictive of the long-term effective population size of parasites than is the total number of potential parasite infrapopulations (i.e., host individuals). Impact SummaryParasites, among Earths most diverse, threatened, and under-protected animals, play a central role in ecosystem function. The effective population size (Ne) of an organism has a profound impact on evolutionary processes, such as the relative contributions of selection and genetic drift to genomic change. Population size is also one of the most important parameters in conservation biology. For free-living organisms, it is expected that Ne is generally proportional to the total number of individuals in a population. However, for parasites, among other factors, populations are sometimes so extremely subdivided that high levels of inbreeding may distort these relationships. In this study, we used whole-genome sequence data from dove parasites and phylogenetic comparative methods to investigate the relationship between parasite effective population size (Ne) and host population size and body size. Our results revealed a positive relationship between parasite effective population size (Ne) and host body size, but not host population size. These results suggest that the size of parasite infrapopulations may be the most important factor when considering parasite effective population size, and have important implications for conservation.

evolutionary biology↗

Genome-resolved metagenomic analyses reveal the presence of a bacterial endosymbiont in an avian nasal mite (Rhinonyssidae; Mesostigmata)

Rhinonyssidae (Mesostigmata) is a family of nasal mites only found in birds. All species are hematophagous endoparasites, which may damage the nasal cavities of birds, and also could be potential reservoirs or vectors of other infections. However, the role of members of Rhinonyssidae as disease vectors in wild bird populations remains uninvestigated, with studies of the microbiomes of Rhinonyssidae being almost non-existent. In the nasal mite (Tinaminyssus melloi) from rock doves (Columba livia), a previous study found evidence of a highly abundant putatively endosymbiotic bacteria from Class Alphaproteobacteria. Here, we expanded the sample size of this species, incorporated contamination controls, and increased sequencing depth in shotgun sequencing and genome-resolved metagenomic analyses. Our goal was to increase the information regarding this mite species with its putative endosymbiont. Our results support the endosymbiotic nature of this bacterial taxon, which is the first described for birds nasal mites to date, and improve the overall understanding of the microbiota inhabiting these mites.

molecular biology↗

The interplay between host biogeography and phylogeny in structuring diversification of the feather louse genus Penenirmus

Parasite diversification is influenced by many of the same factors that affect speciation of free-living organisms, such as biogeographic barriers. However, the ecology and evolution of the host lineage also has a major impact on parasite speciation. Here we explore the interplay between biogeography and host-association on the pattern of diversification in a group of ectoparasitic lice (Insecta: Phthiraptera: Penenirmus) that feeds on the feathers of woodpeckers, barbets, and honeyguides (Piciformes) and some songbirds (Passeriformes). We use whole genome sequencing of 41 ingroup and 12 outgroup samples to develop a phylogenomic dataset of DNA sequences from a reference set of 2,395 single copy ortholog genes, for a total of nearly four million aligned base positions. The phylogenetic trees resulting from both concatenated and gene-tree/species-tree coalescent analyses were nearly identical and highly supported. These trees recovered the genus Penenirmus as monophyletic and identified several major clades, which tended to be associated with one major host group. However, cophylogenetic analysis revealed that host-switching was a prominent process in the diversification of this group. This host-switching generally occurred within single major biogeographic regions. We did, however, find one case in which it appears that a rare dispersal event by a woodpecker lineage from North America to Africa allowed its associated louse to colonize a woodpecker in Africa, even though the woodpecker lineage from North America never became established there.

evolutionary biology↗

Patterns of microbiome variation among infrapopulations of permanent bloodsucking parasites

While interspecific variation in microbiome composition can often be readily explained by factors such as host species identity, there is still limited knowledge of how microbiomes vary at scales lower than the species level (e.g., between individuals or populations). Here, we evaluated variation in microbiome composition of individual parasites among infrapopulations (i.e., populations of parasites of the same species living on a single host individual). To address this question, we used genome-resolved and shotgun metagenomic data of 17 infrapopulations (balanced design) of the permanent, bloodsucking seal louse Echinophthirius horridus sampled from individual Saimaa ringed seals Pusa hispida saimensis. Both genome-resolved and read-based metagenomic classification approaches consistently show that parasite infrapopulation identity is a significant factor that explains both qualitative and quantitative patterns of microbiome variation at the intraspecific level. This study contributes to the general understanding of the factors driving patterns of intraspecific variation in microbiome composition, especially of bloodsucking parasites, and has implications for understanding how well-known processes occurring at higher taxonomic levels, such as phylosymbiosis, might arise in these systems.

ecology↗

Achromatic body markings as a widespread visual mechanism across group living animals

Grouping is a widespread form of predator defense, with individuals in groups often performing evasive collective movements in response to predators attacks. Individuals in these groups use behavioral rules to coordinate their movements, with visual cues about neighbors positions and orientations informing movement decisions. Although the exact visual cues individuals use to coordinate their movements with neighbors have not yet been decoded, some studies have suggested that stripes, lines or other body patterns may act as conspicuous conveyors of movement information that could promote coordinated group movement, or promote dazzle camouflage, thereby confusing predators. We used phylogenetic logistic regressions to test whether the contrasting achromatic stripes present in four different taxa vulnerable to predation, including species within two orders of birds (Anseriformes and Charadriiformes), a suborder of Artiodactyla (the ruminants) and several orders of marine fish (predominantly Perciformes) were associated with group living. Contrasting patterns were significantly more prevalent in social species, and tended to be absent in solitary species or species less vulnerable to predation. We suggest that stripes taking the form of light-colored lines on dark backgrounds, or vice versa, provide a widespread mechanism across taxa that serves either to inform conspecifics of neighbors directional movement, or to confuse predators, when moving in groups. Detection and processing of patterns and of motion in the visual channel is essentially colourblind. That diverse animal taxa with widely different vision systems (including di-, tri- and tetrachromats) appear to have converged on a similar use of achromatic patterns is therefore expected given signal-detection theory. This hypothesis would explain the convergent evolution of conspicuous achromatic patterns as an antipredator mechanism in numerous vertebrate species.

evolutionary biology↗

The Parasite Extinction Assessment & Red List: an open-source, online biodiversity database for neglected symbionts

Parasite conservation is a rapidly growing field at the intersection of ecology, epidemiology, parasitology, and public health. The overwhelming diversity of parasitic life on earth, and recent work showing that parasites and other symbionts face severe extinction risk, necessitates infrastructure for parasite conservation assessments. Here, we describe the release of the Parasite Extinction Assessment & Red List (PEARL) version 1.0, an open-access database of conservation assessments and distributional data for almost 500 macroparasitic invertebrates. The current approach to vulnerability assessment is based on range shifts and loss from climate change, and will be expanded as additional data (e.g., host-parasite associations and coextinction risk) is consolidated in PEARL. The web architecture is also open-source, scalable, and extensible, making PEARL a template for more eZcient red listing for other high-diversity, data-de1cient groups. Future iterations will also include new functionality, including a user-friendly open data pository and automated assessment and re-listing.

ecology↗