Saccharomycotina yeasts defy long-standing macroecological patterns.

The Saccharomycotina yeasts ("yeasts" hereafter) are a fungal clade of scientific, economic, and medical significance. Yeasts are highly ecologically diverse, found across a broad range of environments in every biome and continent on earth; however, little is known about what rules govern the macroecology of yeast species and their range limits in the wild. Here, we trained machine learning models on 12,816 terrestrial occurrence records and 96 environmental variables to infer global distribution maps at ~1 km2 resolution for 186 yeast species (~15% of described species from 75% of orders) and to test environmental drivers of yeast biogeography and macroecology. We found that predicted yeast diversity hotspots occur in mixed montane forests in temperate climates. Diversity in vegetation type and topography were some of the greatest predictors of yeast species richness, suggesting that microhabitats and environmental clines are key to yeast diversity. We further found that range limits in yeasts are significantly influenced by carbon niche breadth and range overlap with other yeast species, with carbon specialists and species in high-diversity environments exhibiting reduced geographic ranges. Finally, yeasts contravene many long-standing macroecological principles, including the latitudinal diversity gradient, temperature-dependent species richness, and a positive relationship between latitude and range size (Rapoport's rule). These results unveil how the environment governs the global diversity and distribution of species in the yeast subphylum. These high-resolution models of yeast species distributions will facilitate the prediction of economically relevant and emerging pathogenic species under current and future climate scenarios.

Functional and Evolutionary Integration of a Fungal Gene With a Bacterial Operon.

Siderophores are crucial for iron-scavenging in microorganisms. While many yeasts can uptake siderophores produced by other organisms, they are typically unable to synthesize siderophores themselves. In contrast, Wickerhamiella/Starmerella (W/S) clade yeasts gained the capacity to make the siderophore enterobactin following the remarkable horizontal acquisition of a bacterial operon enabling enterobactin synthesis. Yet, how these yeasts absorb the iron bound by enterobactin remains unresolved. Here, we demonstrate that Enb1 is the key enterobactin importer in the W/S-clade species Starmerella bombicola. Through phylogenomic analyses, we show that ENB1 is present in all W/S clade yeast species that retained the enterobactin biosynthetic genes. Conversely, it is absent in species that lost the ent genes, except for Starmerella stellata, making this species the only cheater in the W/S clade that can utilize enterobactin without producing it. Through phylogenetic analyses, we infer that ENB1 is a fungal gene that likely existed in the W/S clade prior to the acquisition of the ent genes and subsequently experienced multiple gene losses and duplications. Through phylogenetic topology tests, we show that ENB1 likely underwent horizontal gene transfer from an ancient W/S clade yeast to the order Saccharomycetales, which includes the model yeast Saccharomyces cerevisiae, followed by extensive secondary losses. Taken together, these results suggest that the fungal ENB1 and bacterial ent genes were cooperatively integrated into a functional unit within the W/S clade that enabled adaptation to iron-limited environments. This integrated fungal-bacterial circuit and its dynamic evolution determine the extant distribution of yeast enterobactin producers and cheaters.

Functional and evolutionary integration of a fungal gene with a bacterial operon.

Siderophores are crucial for iron-scavenging in microorganisms. While many yeasts can uptake siderophores produced by other organisms, they are typically unable to synthesize siderophores themselves. In contrast, Wickerhamiella/Starmerella (W/S) clade yeasts gained the capacity to make the siderophore enterobactin following the remarkable horizontal acquisition of a bacterial operon enabling enterobactin synthesis. Yet, how these yeasts absorb the iron bound by enterobactin remains unresolved. Here, we demonstrate that Enb1 is the key enterobactin importer in the W/S-clade species Starmerella bombicola. Through phylogenomic analyses, we show that ENB1 is present in all W/S clade yeast species that retained the enterobactin biosynthetic genes. Conversely, it is absent in species that lost the ent genes, except for Starmerella stellata, making this species the only cheater in the W/S clade that can utilize enterobactin without producing it. Through phylogenetic analyses, we infer that ENB1 is a fungal gene that likely existed in the W/S clade prior to the acquisition of the ent genes and subsequently experienced multiple gene losses and duplications. Through phylogenetic topology tests, we show that ENB1 likely underwent horizontal gene transfer from an ancient W/S clade yeast to the order Saccharomycetales, which includes the model yeast Saccharomyces cerevisiae, followed by extensive secondary losses. Taken together, these results suggest that the fungal ENB1 and bacterial ent genes were cooperatively integrated into a functional unit within the W/S clade that enabled adaptation to iron-limited environments. This integrated fungal-bacterial circuit and its dynamic evolution determines the extant distribution of yeast enterobactin producers and cheaters.

Saccharomycotina yeasts defy longstanding macroecological patterns.

The Saccharomycotina yeasts ("yeasts" hereafter) are a fungal clade of scientific, economic, and medical significance. Yeasts are highly ecologically diverse, found across a broad range of environments in every biome and continent on earth1; however, little is known about what rules govern the macroecology of yeast species and their range limits in the wild2. Here, we trained machine learning models on 12,221 occurrence records and 96 environmental variables to infer global distribution maps for 186 yeast species (~15% of described species from 75% of orders) and to test environmental drivers of yeast biogeography and macroecology. We found that predicted yeast diversity hotspots occur in mixed montane forests in temperate climates. Diversity in vegetation type and topography were some of the greatest predictors of yeast species richness, suggesting that microhabitats and environmental clines are key to yeast diversification. We further found that range limits in yeasts are significantly influenced by carbon niche breadth and range overlap with other yeast species, with carbon specialists and species in high diversity environments exhibiting reduced geographic ranges. Finally, yeasts contravene many longstanding macroecological principles, including the latitudinal diversity gradient, temperature-dependent species richness, and latitude-dependent range size (Rapoport's rule). These results unveil how the environment governs the global diversity and distribution of species in the yeast subphylum. These high-resolution models of yeast species distributions will facilitate the prediction of economically relevant and emerging pathogenic species under current and future climate scenarios.

Unsupervised Deep Learning Can Identify Protein Functional Groups from Unaligned Sequences.

Interpreting protein function from sequence data is a fundamental goal of bioinformatics. However, our current understanding of protein diversity is bottlenecked by the fact that most proteins have only been functionally validated in model organisms, limiting our understanding of how function varies with gene sequence diversity. Thus, accuracy of inferences in clades without model representatives is questionable. Unsupervised learning may help to ameliorate this bias by identifying highly complex patterns and structure from large datasets without external labels. Here we present DeepSeqProt, an unsupervised deep learning program for exploring large protein sequence datasets. DeepSeqProt is a clustering tool capable of distinguishing between broad classes of proteins while learning local and global structure of functional space. DeepSeqProt is capable of learning salient biological features from unaligned, unannotated sequences. DeepSeqProt is more likely to capture complete protein families and statistically significant shared ontologies within proteomes than other clustering methods. We hope this framework will prove of use to researchers and provide a preliminary step in further developing unsupervised deep learning in molecular biology.

Global gradients in the distribution of animal polyploids.

Whole genome duplications (WGDs) are one of the most dramatic mutations that can be found in nature. The effects of WGD vary dramatically but can have profound impacts on an organism's expression, cytotype, and phenotype, altering their evolutionary trajectory as a result. Despite the growing appreciation for the contribution of WGDs in animal evolution, the significant factors influencing how polyploid animal lineages are established and maintained are still not well understood. Many hypotheses have been proposed which predict how climate and environment may influence polyploid incidence and evolution. To test and distinguish between these hypotheses, I assembled a global dataset of polyploid occurrences in three animal clades (Amphibia, Actinopterygii, and Insecta). The dataset encompasses chromosomal, phylogenetic, environmental, and climatic data across 57,905 species in 2,223 terrestrial, freshwater, and marine ecoregions. My analysis reveals a strong latitudinal gradient in all three clades, with the tendency for polyploid taxa to occur more frequently at higher latitudes. Many variables were significant (phylogenetic ANOVA P < 0.05 after Bonferroni correction) between polyploids and diploids across taxa, notably those pertaining to temperature dynamics and glaciation. Glaciation in particular appears to be the most significant driver of polyploidy in animals, as these models had the highest relative likelihoods consistently across clades. These results contribute to a model of evolution wherein the broader genomic toolkit of polyploids facilitates adaptation and ecological resilience, enabling polyploids to colonize new or rapidly changing environments.

TIAMMAt: Leveraging Biodiversity to Revise Protein Domain Models, Evidence from Innate Immunity.

Sequence annotation is fundamental for studying the evolution of protein families, particularly when working with nonmodel species. Given the rapid, ever-increasing number of species receiving high-quality genome sequencing, accurate domain modeling that is representative of species diversity is crucial for understanding protein family sequence evolution and their inferred function(s). Here, we describe a bioinformatic tool called Taxon-Informed Adjustment of Markov Model Attributes (TIAMMAt) which revises domain profile hidden Markov models (HMMs) by incorporating homologous domain sequences from underrepresented and nonmodel species. Using innate immunity pathways as a case study, we show that revising profile HMM parameters to directly account for variation in homologs among underrepresented species provides valuable insight into the evolution of protein families. Following adjustment by TIAMMAt, domain profile HMMs exhibit changes in their per-site amino acid state emission probabilities and insertion/deletion probabilities while maintaining the overall structure of the consensus sequence. Our results show that domain revision can heavily impact evolutionary interpretations for some families (i.e., NLR's NACHT domain), whereas impact on other domains (e.g., rel homology domain and interferon regulatory factor domains) is minimal due to high levels of sequence conservation across the sampled phylogenetic depth (i.e., Metazoa). Importantly, TIAMMAt revises target domain models to reflect homologous sequence variation using the taxonomic distribution under consideration by the user. TIAMMAt's flexibility to revise any subset of the Pfam database using a user-defined taxonomic pool will make it a valuable tool for future protein evolution studies, particularly when incorporating (or focusing) on nonmodel species.

Patterns of gene evolution following duplications and speciations in vertebrates.

BACKGROUND: Eukaryotic genes typically form independent evolutionary lineages through either speciation or gene duplication events. Generally, gene copies resulting from speciation events (orthologs) are expected to maintain similarity over time with regard to sequence, structure and function. After a duplication event, however, resulting gene copies (paralogs) may experience a broader set of possible fates, including partial (subfunctionalization) or complete loss of function, as well as gain of new function (neofunctionalization). This assumption, known as the Ortholog Conjecture, is prevalent throughout molecular biology and notably plays an important role in many functional annotation methods. Unfortunately, studies that explicitly compare evolutionary processes between speciation and duplication events are rare and conflicting. METHODS: To provide an empirical assessment of ortholog/paralog evolution, we estimated ratios of nonsynonymous to synonymous substitutions (ω = dN/dS) for 251,044 lineages in 6,244 gene trees across 77 vertebrate taxa. RESULTS: Overall, we found ω to be more similar between lineages descended from speciation events (p < 0.001) than lineages descended from duplication events, providing strong support for the Ortholog Conjecture. The asymmetry in ω following duplication events appears to be largely driven by an increase along one of the paralogous lineages, while the other remains similar to the parent. This trend is commonly associated with neofunctionalization, suggesting that gene duplication is a significant mechanism for generating novel gene functions.

Genomic adaptations to chemosymbiosis in the deep-sea seep-dwelling tubeworm Lamellibrachia luymesi.

BACKGROUND: Symbiotic relationships between microbes and their hosts are widespread and diverse, often providing protection or nutrients, and may be either obligate or facultative. However, the genetic mechanisms allowing organisms to maintain host-symbiont associations at the molecular level are still mostly unknown, and in the case of bacterial-animal associations, most genetic studies have focused on adaptations and mechanisms of the bacterial partner. The gutless tubeworms (Siboglinidae, Annelida) are obligate hosts of chemoautotrophic endosymbionts (except for Osedax which houses heterotrophic Oceanospirillales), which rely on the sulfide-oxidizing symbionts for nutrition and growth. Whereas several siboglinid endosymbiont genomes have been characterized, genomes of hosts and their adaptations to this symbiosis remain unexplored. RESULTS: Here, we present and characterize adaptations of the cold seep-dwelling tubeworm Lamellibrachia luymesi, one of the longest-lived solitary invertebrates. We sequenced the worm's ~ 688-Mb haploid genome with an overall completeness of ~ 95% and discovered that L. luymesi lacks many genes essential in amino acid biosynthesis, obligating them to products provided by symbionts. Interestingly, the host is known to carry hydrogen sulfide to thiotrophic endosymbionts using hemoglobin. We also found an expansion of hemoglobin B1 genes, many of which possess a free cysteine residue which is hypothesized to function in sulfide binding. Contrary to previous analyses, the sulfide binding mediated by zinc ions is not conserved across tubeworms. Thus, the sulfide-binding mechanisms in sibgolinids need to be further explored, and B1 globins might play a more important role than previously thought. Our comparative analyses also suggest the Toll-like receptor pathway may be essential for tolerance/sensitivity to symbionts and pathogens. Several genes related to the worm's unique life history which are known to play important roles in apoptosis, cell proliferation, and aging were also identified. Last, molecular clock analyses based on phylogenomic data suggest modern siboglinid diversity originated in 267 mya (± 70 my) support previous hypotheses indicating a Late Mesozoic or Cenozoic origins of approximately 50-126 mya for vestimentiferans. CONCLUSIONS: Here, we elucidate several specific adaptations along various molecular pathways that link phenome to genome to improve understanding of holobiont evolution. Our findings of adaptation in genomic mechanisms to reducing environments likely extend to other chemosynthetic symbiotic systems.

Sequencing Disparity in the Genomic Era.

Advances in sequencing technology have resulted in the expectation that genomic studies will become more representative of organismal diversity. To test this expectation, we explored species representation of nonhuman eukaryotes in the Sequence Read Archive. Though species richness has been increasing steadily, species evenness is decreasing over time. Moreover, the top 1% most studied organisms increasingly represent a larger proportion of total experiments, demonstrating growing bias in favor of a small minority of species. To better understand molecular processes and patterns, genomic studies should reverse current trends by adopting more comparative approaches.

Pleistocene to holocene expansion of the black-belt cichlid in Central America, Vieja maculicauda (Teleostei: Cichlidae).

The distributions of many Northern Hemisphere organisms have been influenced by fluctuations in sea level and climatic conditions during Pleistocene interglacial periods. These cycles are associated with range contraction and refugia for northern-distributed organisms as a response to glaciers. However, lower sea levels in the tropics and sub-tropics created available habitat for expansion of the ranges of freshwater organisms. The goal of this study was to use ecological niche modeling to test the hypothesis of north to south range expansion of Vieja maculicauda associated with Pleistocene glacial cycles. Understanding the biogeography of this widespread species may help us better understand the geology and interconnectivity of Central American freshwaters. Occurrence data for V. maculicauda was based on georeferencing of all museum records of specimens recovered from FishNet2. General patterns of phylogeographic structure were assessed with mtDNA. Present day niche models were generated and subsequently projected onto paleoclimatic maps of the region during the Last Interglacial, Last Glacial Maximum, and mid-Holocene. Phylogenetic analysis of mtDNA sequence data showed no phylogeographic structure throughout the range of this widespread species. Present day niche models were congruent with the observed distribution of V. maculicauda in Central America. Results showed a lack of suitable freshwater habitat in northern Central America and Mexico during the Last Interglacial, with greatest range expansion during the Last Glacial Maximum and mid-Holocene. Results support the hypothesis of a north to south range expansion of V. maculicauda associated with glacial cycles. The wide distribution of this species compared to other closely related cichlids indicates the latter did not respond to the degree of V. maculicauda in expansion of their distributions. Future work aimed at comparisons with other species and modeling of future climatic scenarios will be a fruitful area of investigation.

Mitochondrial genome of Dinophilus gyrociliatus (Annelida: Dinophilidae).

Here we report the 14,678 bp mitochondrial genome of the annelid Dinophilus gyrociliatus, the first mitochondrial genome from Dinophilidae. We recovered 13 protein-coding genes, two rRNA, and 21 tRNA, the order of which is different from other annelid species. Interestingly, trnS1 was not recovered. The GC% across the genome was 34.20%.

Resource Availability Drives Mating Role Selection in a Simultaneous Hermaphrodite Aplysia californica.

In simultaneous hermaphrodites, a clear conflict exists between sperm donor and sperm recipient roles, and how such conflict is mediated remains up for debate. This study observed and recorded mating role selection as a function of resource availability in the simultaneous hermaphrodite Aplysia californica. When food was plentiful, animals assumed both sperm donor and recipient roles at relatively even frequency. However, when half of the mating pairs were placed on restricted diets, food-limited animals assumed the sperm donor role at significantly (P < 0.05) greater frequency than their ad libitum partners; nevertheless, the frequency of successful mating events remained the same. The mass and frequency of eggs laid were also significantly (P > 0.05) correlated with parental food intake. These results demonstrate how mating strategies can change within a mating season, as a result of shifting environmental conditions, and call for a diverse framework to address these issues in simultaneous hermaphroditic mating systems.