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All sourcesNASA NTRSDOE OSTI
DOE OSTI2022

Sporophyte Stage Genes Exhibit Stronger Selection Than Gametophyte Stage Genes in Haplodiplontic Giant Kelp

Macrocystis pyrifera (giant kelp), a haplodiplontic brown macroalga that alternates between a macroscopic diploid (sporophyte) and a microscopic haploid (gametophyte) phase, provides an ideal system to investigate how ploidy background affects the evolutionary history of a gene. In M. pyrifera , the same genome is subjected to different selective pressures and environments as it alternates between haploid and diploid life stages. We assembled M. pyrifera gene models using available expression data and validated 8,292 genes models using the model alga Ectocarpus siliculosus . Differential expression analysis identified gene models expressed in either or both the haploid and diploid life stages while functional annotation identified processes enriched in each stage. Genes expressed preferentially or exclusively in the gametophyte stage were found to have higher nucleotide diversity (π = 2.3 × 10 –3 and 2.8 × 10 –3 , respectively) than those for sporophytes (π = 1.1 × 10 –3 and 1 × 10 –3 , respectively). While gametophyte-biased genes show faster sequence evolution, the sequence evolution exhibits less signatures of adaptations when compared to sporophyte-biased genes. Our findings contrast the standing masking hypothesis, which predicts higher standing genetic variation at the sporophyte stage, and support the strength of expression theory, which posits that genes expressed more strongly are expected to evolve slower. We argue that the sporophyte stage undergoes more stringent selection compared with the gametophyte stage, which carries a heavy genetic load associated with broadcast spawning. Furthermore, using whole-genome sequencing, we confirm the strong population structure in wild M. pyrifera populations previously established using microsatellite markers, and estimate population genetic parameters, such as pairwise genetic diversity and Tajima’s D , important for conservation and domestication of M. pyrifera .

Molano, Gary↗
DOE OSTI2022

Aerobic Methoxydotrophy: Growth on Methoxylated Aromatic Compounds by Methylobacteriaceae

Pink-pigmented facultative methylotrophs have long been studied for their ability to grow on reduced single-carbon (C 1 ) compounds. The C 1 groups that support methylotrophic growth may come from a variety of sources. Here, we describe a group of Methylobacterium strains that can engage in methoxydotrophy: they can metabolize the methoxy groups from several aromatic compounds that are commonly the product of lignin depolymerization. Furthermore, these organisms can utilize the full aromatic ring as a growth substrate, a phenotype that has rarely been described in Methylobacterium . We demonstrated growth on p -hydroxybenzoate, protocatechuate, vanillate, and ferulate in laboratory culture conditions. We also used comparative genomics to explore the evolutionary history of this trait, finding that the capacity for aromatic catabolism is likely ancestral to two clades of Methylobacterium , but has also been acquired horizontally by closely related organisms. In addition, we surveyed the published metagenome data to find that the most abundant group of aromatic-degrading Methylobacterium in the environment is likely the group related to Methylobacterium nodulans , and they are especially common in soil and root environments. The demethoxylation of lignin-derived aromatic monomers in aerobic environments releases formaldehyde, a metabolite that is a potent cellular toxin but that is also a growth substrate for methylotrophs. We found that, whereas some known lignin-degrading organisms excrete formaldehyde as a byproduct during growth on vanillate, Methylobacterium do not. This observation is especially relevant to our understanding of the ecology and the bioengineering of lignin degradation.

59 BASIC BIOLOGICAL SCIENCES↗
DOE OSTI2022

Evolutionary Divergence of Marinobacter Strains in Cryopeg Brines as Revealed by Pangenomics

Marinobacter spp. are cosmopolitan in saline environments, displaying a diverse set of metabolisms that allow them to competitively occupy these environments, some of which can be extreme in both salinity and temperature. Here, we introduce a distinct cluster of Marinobacter genomes, composed of novel isolates and in silico assembled genomes obtained from subzero, hypersaline cryopeg brines, relic seawater-derived liquid habitats within permafrost sampled near Utqiaġvik, Alaska. Using these new genomes and 45 representative publicly available genomes of Marinobacter spp. from other settings, we assembled a pangenome to examine how the new extremophile members fit evolutionarily and ecologically, based on genetic potential and environmental source. This first genus-wide genomic analysis revealed that Marinobacter spp. in general encode metabolic pathways that are thermodynamically favored at low temperature, cover a broad range of organic compounds, and optimize protein usage, e.g., the Entner–Doudoroff pathway, the glyoxylate shunt, and amino acid metabolism. The new isolates contributed to a distinct clade of subzero brine-dwelling Marinobacter spp. that diverged genotypically and phylogenetically from all other Marinobacter members. The subzero brine clade displays genomic characteristics that may explain competitive adaptations to the extreme environments they inhabit, including more abundant membrane transport systems (e.g., for organic substrates, compatible solutes, and ions) and stress-induced transcriptional regulatory mechanisms (e.g., for cold and salt stress) than in the other Marinobacter clades. We also identified more abundant signatures of potential horizontal transfer of genes involved in transcription, the mobilome, and a variety of metabolite exchange systems, which led to considering the importance of this evolutionary mechanism in an extreme environment where adaptation via vertical evolution is physiologically rate limited. Assessing these new extremophile genomes in a pangenomic context has provided a unique view into the ecological and evolutionary history of the genus Marinobacter , particularly with regard to its remarkable diversity and its opportunism in extremely cold and saline environments.

59 BASIC BIOLOGICAL SCIENCES↗
DOE OSTI2021

Multiple Wheat Genomes Reveal Novel Gli-2 Sublocus Location and Variation of Celiac Disease Epitopes in Duplicated α-Gliadin Genes

The seed protein α-gliadin is a major component of wheat flour and causes gluten-related diseases. However, due to the complexity of this multigene family with a genome structure composed of dozens of copies derived from tandem and genome duplications, little was known about the variation between accessions, and thus little effort has been made to explicitly target α-gliadin for bread wheat breeding. Here, we analyzed genomic variation in α-gliadins across 11 recently published chromosome-scale assemblies of hexaploid wheat, with validation using long-read data. We unexpectedly found that the Gli-B2 locus is not a single contiguous locus but is composed of two subloci, suggesting the possibility of recombination between the two during breeding. We confirmed that the number of immunogenic epitopes among 11 accessions varied. The D subgenome of a European spelt line also contained epitopes, in agreement with its hybridization history. Evolutionary analysis identified amino acid sites under diversifying selection, suggesting their functional importance. The analysis opens the way for improved grain quality and safety through wheat breeding.

59 BASIC BIOLOGICAL SCIENCES↗
DOE OSTI2023

Two major chromosome evolution events with unrivaled conserved gene content in pomegranate

Pomegranate has a unique evolutionary history given that different cultivars have eight or nine bivalent chromosomes with possible crossability between the two classes. Therefore, it is important to study chromosome evolution in pomegranate to understand the dynamics of its population. Here, we de novo assembled the Azerbaijani cultivar “Azerbaijan guloyshasi” (AG2017; 2n = 16) and re-sequenced six cultivars to track the evolution of pomegranate and to compare it with previously published de novo assembled and re-sequenced cultivars. High synteny was observed between AG2017, Bhagawa (2n = 16), Tunisia (2n = 16), and Dabenzi (2n = 18), but these four cultivars diverged from the cultivar Taishanhong (2n = 18) with several rearrangements indicating the presence of two major chromosome evolution events. Major presence/absence variations were not observed as >99% of the five genomes aligned across the cultivars, while >99% of the pan-genic content was represented by Tunisia and Taishanhong only. We also revisited the divergence between soft- and hard-seeded cultivars with less structured population genomic data, compared to previous studies, to refine the selected genomic regions and detect global migration routes for pomegranate. We reported a unique admixture between soft- and hard-seeded cultivars that can be exploited to improve the diversity, quality, and adaptability of local pomegranate varieties around the world. Our study adds body knowledge to understanding the evolution of the pomegranate genome and its implications for the population structure of global pomegranate diversity, as well as planning breeding programs aiming to develop improved cultivars.

59 BASIC BIOLOGICAL SCIENCES↗
DOE OSTI2024

Expanded Archaeal Genomes Shed New Light on the Evolution of Isoprenoid Biosynthesis

Isoprenoids and their derivatives, essential for all cellular life on Earth, are particularly crucial in archaeal membrane lipids, suggesting that their biosynthesis pathways have ancient origins and play pivotal roles in the evolution of early life. Despite all eukaryotes, archaea, and a few bacterial lineages being known to exclusively use the mevalonate (MVA) pathway to synthesize isoprenoids, the origin and evolutionary trajectory of the MVA pathway remain controversial. Here, we conducted a thorough comparison and phylogenetic analysis of key enzymes across the four types of MVA pathway, with the particular inclusion of metagenome assembled genomes (MAGs) from uncultivated archaea. Our findings support an archaeal origin of the MVA pathway, likely postdating the divergence of Bacteria and Archaea from the Last Universal Common Ancestor (LUCA), thus implying the LUCA’s enzymatic inability for isoprenoid biosynthesis. Notably, the Asgard archaea are implicated in playing central roles in the evolution of the MVA pathway, serving not only as putative ancestors of the eukaryote- and Thermoplasma-type routes, but also as crucial mediators in the gene transfer to eukaryotes, possibly during eukaryogenesis. Overall, this study advances our understanding of the origin and evolutionary history of the MVA pathway, providing unique insights into the lipid divide and the evolution of early life.

59 BASIC BIOLOGICAL SCIENCES↗
DOE OSTI2021

Comparative Genomic Analysis of Three Pseudomonas Species Isolated from the Eastern Oyster (Crassostrea virginica) Tissues, Mantle Fluid, and the Overlying Estuarine Water Column

The eastern oysters serve as important keystone species in the United States, especially in the Gulf of Mexico estuarine waters, and at the same time, provide unparalleled economic, ecological, environmental, and cultural services. One ecosystem service that has garnered recent attention is the ability of oysters to sequester impurities and nutrients, such as nitrogen (N), from the estuarine water that feeds them, via their exceptional filtration mechanism coupled with microbially-mediated denitrification processes. It is the oyster-associated microbiomes that essentially provide these myriads of ecological functions, yet not much is known on these microbiota at the genomic scale, especially from warm temperate and tropical water habitats. Among the suite of bacterial genera that appear to interplay with the oyster host species, pseudomonads deserve further assessment because of their immense metabolic and ecological potential. To obtain a comprehensive understanding on this aspect, we previously reported on the isolation and preliminary genomic characterization of three Pseudomonas species isolated from minced oyster tissue (P. alcaligenes strain OT69); oyster mantle fluid (P. stutzeri strain MF28) and the water collected from top of the oyster reef (P. aeruginosa strain WC55), respectively. In this comparative genomic analysis study conducted on these three targeted pseudomonads, native to the eastern oyster and its surrounding environment, provided further insights into their unique functional traits, conserved gene pools between the selected pseudomonads, as well as genes that render unique characteristics in context to metabolic traits recruited during their evolutionary history via horizontal gene transfer events as well as phage-mediated incorporation of genes. Moreover, the strains also supported extensively developed resistomes, which suggests that environmental microorganisms native to relatively pristine environments, such as Apalachicola Bay, Florida, have also recruited an arsenal of antibiotic resistant gene determinants, thus posing an emerging public health concern.

Pathak, Ashish↗
DOE OSTI2020

Variability in Proto-planetary Nebulae. VI. Multitelescope Light Curve Studies of Several Medium-bright (V = 13–15), Carbon-rich Objects

We present 10 years of new photometric monitoring of the light variability of five evolved stars with strong mid-infrared emission from surrounding dust. Three are known carbon-rich proto-planetary nebulae (PPNe) with F−G spectral types; the nature of the other two was previously unknown. For the three PPNe, we determine or refine the pulsation periods of IRAS 04296+3429 (71 days), 06530−0213 (80 days), and 23304+6147 (84 days). A secondary period was found for each, with a period ratio P {sub 2}/P {sub 1} of 0.9. The light variations are small, 0.1–0.2 mag. These are similar to values found in other PPNe. The other two are found to be giant stars. IRAS 09296+1159 pulsates with a period of only 47 days but reaches pulsational light variations of 0.5 mag. Supplemental spectroscopy reveals the spectrum of a CH carbon star. IRAS 08359−1644 is a G1 III star that does not display pulsational variability; rather, it shows nonperiodic decreases of brightness of up to 0.5 mag over this 10 year interval. These drops in brightness are reminiscent of the light curves of R Corona Borealis variables, but with much smaller decreases in brightness and are likely due to transient dust obscuration. Its spectral energy distribution is very similar to that of the unusual oxygen-rich giant star HDE 233517, which possesses mid-infrared hydrocarbon emission features. These two non-PPNe turn out to be members of the rare group of giant stars with large mid-infrared excesses due to dust, objects which presumably have interesting evolutionary histories.

79 ASTRONOMY AND ASTROPHYSICS↗
DOE OSTI2020

Bayesian Characterization of Main-sequence Binaries in the Old Open Cluster NGC 188

The binary fractions of open and globular clusters yield powerful constraints on their dynamical state and evolutionary history. We apply publicly available Bayesian analysis tools to a UBV RIJHK {sub S} photometric catalog of the open cluster NGC 188 to detect and characterize photometric binaries along the cluster main sequence. This technique has the advantage of self-consistently handling photometric errors, missing data in various bandpasses, and star-by-star prior constraints on cluster membership. Simulations are used to verify uncertainties and quantify selection biases in our analysis, illustrating that among binaries with mass ratios >0.5, we recover the binary fraction to better than 7% in the mean, with no significant dependence on binary fraction and a mild dependence on assumed mass-ratio distribution. Using our photometric catalog, we recover the majority (65% ± 11%) of spectroscopically identified main-sequence binaries, including eight of the nine with spectroscopically measured mass ratios. Accounting for incompleteness and systematics, we derive a mass-ratio distribution that rises toward lower mass ratios (within our q > 0.5 analysis domain). We observe a raw binary fraction for solar-type main-sequence stars with mass ratios q > 0.5 of 42% ± 4%, independent of the assumed mass-ratio distribution to within its uncertainties, consistent with literature values for old open clusters but significantly higher than the field solar-type binary fraction. We confirm that the binaries identified by our method are more concentrated than single stars, in agreement with previous studies, and we demonstrate that the binary nature of those candidates that remain unidentified spectroscopically is strongly supported by photometry from Gaia DR2.

79 ASTRONOMY AND ASTROPHYSICS↗
DOE OSTI2021

A Multiwavelength Look at the GJ 9827 System: No Evidence of Extended Atmospheres in GJ 9827b and d from HST and CARMENES Data

GJ 9827 is a bright star hosting a planetary system with three transiting planets. As a multiplanet system with planets that sprawl within the boundaries of the radius gap between terrestrial and gaseous planets, GJ 9827 is an optimal target to study the evolution of the atmospheres of close-in planets with a common evolutionary history and their dependence from stellar irradiation. Here we report on the Hubble Space Telescope (HST) and CARMENES transit observations of GJ 9827 planets b and d. We performed a stellar and ISM characterization from the ultraviolet HST spectra, obtaining fluxes for Lyα and Mg ii of F(Lyα) = (5.42{sub −0.75}{sup +0.96}) × 10{sup −13} erg cm{sup −2} s{sup −1} and F(Mgii) = (5.64 ± 0.24) × 10{sup −14} erg cm{sup −2} s{sup −1}. We also investigated a possible absorption signature in Lyα in the atmosphere of GJ 9827b during a transit event from HST spectra, as well as Hα and He i signature for the atmosphere of GJ 9827b and d from CARMENES spectra. We found no evidence of an extended atmosphere in either of the planets. This result is also supported by our analytical estimations of mass loss based on the measured radiation fields for all three planets of this system, which led to a mass-loss rate of 0.4, 0.3, and 0.1 planetary masses per Gyr for GJ 9827b, c, and d, respectively. These values indicate that the planets could have lost their volatiles quickly in their evolution and probably do not retain an atmosphere at the current stage.

47 OTHER INSTRUMENTATION↗
DOE OSTI2021

The Initial–Final Mass Relation for Hydrogen-deficient White Dwarfs

The initial–final mass relation represents the total mass lost by a star during the entirety of its evolution from the zero age main sequence to the white-dwarf cooling track. The semiempirical initial–final mass relation (IFMR) is largely based on observations of DA white dwarfs, the most common spectral type of white dwarf and the simplest atmosphere to model. We present a first derivation of the semiempirical IFMR for hydrogen-deficient (non-DA) white dwarfs in open star clusters. We identify a possible discrepancy between the DA and non-DA IFMRs, with non-DA white dwarfs ≈0.07 M {sub ⊙} less massive at a given initial mass. Such a discrepancy is unexpected based on theoretical models of non-DA formation and observations of field white dwarf mass distributions. If real, the discrepancy is likely due to enhanced mass loss during the final thermal pulse and renewed post-AGB evolution of the star. However, we are dubious that the mass discrepancy is physical and instead is due to the small sample size, to systematic issues in model atmospheres of non-DAs, and to the uncertain evolutionary history of Procyon B (spectral type DQZ). A significantly larger sample size is needed to test these assertions. In addition, we also present Monte Carlo models of the correlated errors for DA and non-DA white dwarfs in the initial–final mass plane. We find the uncertainties in initial–final mass determinations for individual white dwarfs can be significantly asymmetric, but the recovered functional form of the IFMR is grossly unaffected by the correlated errors.

79 ASTRONOMY AND ASTROPHYSICS↗
DOE OSTI2021

Improve the Search of Very Metal-poor Stars Using the Deep Learning Method

Very metal-poor (VMP) stars have [Fe/H] < -2.0 dex. They are among the oldest stars in the universe, and their unique metallicity can help explore the enrichment mechanism and evolutionary history of the chemical elements of stars in the early universe. However, most current stellar parameter estimation methods do not perform well in determining the stellar parameters of VMP stars, which limits our ability to discover and exploit the properties of VMP stars. In this study, we propose a new model based on a convolutional neural network to determine the stellar atmospheric parameters of VMP stars. We tested our model on the LAMOST spectra; our model can determine the effective temperature (T {sub eff}), surface gravity (log g), metallicity ([Fe/H]), and carbon abundance ([C/Fe]) of the LAMOST spectra with precisions σ(T {sub eff}) = 134.82 K, σ(log g) = 0.33 dex, σ ([Fe/H]) = 0.20 dex, and σ([C/Fe]) = 0.35 dex. Furthermore, our model can distinguish VMP stars from normal stars with an accuracy of 88.65%. We also compared this model with other widely used methods, and found that this method performs better than other methods. It can be applied to the stellar parameter pipelines of upcoming large surveys such as 4MOST, WEAVES, and MOONS to search for VMP stars and identify carbon-enhanced metal-poor stars.

36 MATERIALS SCIENCE↗
DOE OSTI2025

Aggressively Dissipative Dark Dwarfs: The Effects of Atomic Dark Matter on the Inner Densities of Isolated Dwarf Galaxies

We present the first suite of cosmological hydrodynamical zoom-in simulations of isolated dwarf galaxies for a dark sector that consists of cold dark matter and a strongly dissipative subcomponent. The simulations are implemented in GIZMO and include standard baryons following the FIRE-2 galaxy formation physics model. The dissipative dark matter is modeled as atomic dark matter (aDM), which forms a dark hydrogen gas that cools in direct analogy to the Standard Model. Our suite includes seven different simulations of ∼10 10 M ⊙ systems that vary over the aDM microphysics and the dwarf’s evolutionary history. We identify a region of aDM parameter space where the cooling rate is aggressive and the resulting halo density profile is universal. In this regime, the aDM gas cools rapidly at high redshifts, and only a small fraction survives in the form of a central dark gas disk; the majority collapses centrally into collisionless dark “clumps,” which are clusters of subresolution dark compact objects. These dark clumps rapidly equilibrate in the inner galaxy, resulting in an approximately isothermal distribution that can be modeled with a simple fitting function. Even when only a small fraction (∼5%) of the total dark matter is strongly dissipative, the central densities of classical dwarf galaxies can be enhanced by over an order of magnitude, providing a sharp prediction for observations.

cold dark matter↗
DOE OSTI2020

Software classification using phylogenetic techniques

Software, such as malware, may be classified using phylogenetic techniques. An evolutionary history of a representative set of software programs may be reconstructed to generate a reference phylogeny. Dynamic traces of the representative software programs may be obtained. The dynamic traces may include time-ordered sequences of execution commands extracted from running software binaries. Metrics may be developed using the dynamic traces. One or more unknown software programs may then be classified against the reference phylogeny using the metrics developed using the dynamic traces of the representative set of software programs.

97 MATHEMATICS AND COMPUTING↗
DOE OSTI2025

Comparative genomics reveals the high diversity and adaptation strategies of Polaromonas from polar environments

Abstract Background Bacteria from the genus Polaromonas are dominant phylotypes found in a variety of low-temperature environments in polar regions. The diversity and biogeographic distribution of Polaromonas have been largely expanded on the basis of 16 S rRNA gene amplicon sequencing. However, the evolution and cold adaptation mechanisms of Polaromonas from polar regions are poorly understood at the genomic level. Results A total of 202 genomes of the genus Polaromonas were analyzed, and 121 different species were delineated on the basis of average nucleotide identity (ANI) and phylogenomic placements. Remarkably, 8 genomes recovered from polar environments clustered into a separate clade (‘polar group’ hereafter). The genome size, coding density and coding sequences (CDSs) of the polar group were significantly different from those of other nonpolar Polaromonas . Furthermore, the enrichment of genes involved in carbohydrate and peptide metabolism was evident in the polar group. In addition, genes encoding proteins related to betaine synthesis and transport were increased in the genomes from the polar group. Phylogenomic analysis revealed that two different evolutionary scenarios may explain the adaptation of Polaromonas to cold environments in polar regions. Conclusions The global distribution of the genus Polaromonas highlights its strong adaptability in both polar and nonpolar environments. Species delineation significantly expands our understanding of the diversity of the Polaromonas genus on a global scale. In this study, a polar-specific clade was found, which may represent a specific ecotype well adapted to polar environments. Collectively, genomic insight into the metabolic diversity, evolution and adaptation of the genus Polaromonas at the genome level provides a genetic basis for understanding the potential response mechanisms of Polaromonas to global warming in polar regions.

54 ENVIRONMENTAL SCIENCES↗
DOE OSTI2021

Analyses of transcriptomes and the first complete genome of Leucocalocybe mongolica provide new insights into phylogenetic relationships and conservation

In this study, we report a de novo assembly of the first high-quality genome for a wild mushroom species Leucocalocybe mongolica (LM). We performed high-throughput transcriptome sequencing to analyze the genetic basis for the life history of LM. Our results show that the genome size of LM is 46.0 Mb, including 26 contigs with a contig N50 size of 3.6 Mb. In total, we predicted 11,599 protein-coding genes, of which 65.7% (7630) could be aligned with high confidence to annotated homologous genes in other species. We performed phylogenetic analyses using genes form 3269 single-copy gene families and showed support for distinguishing LM from the genus Tricholoma (L.) P.Kumm., in which it is sometimes circumscribed. We believe that one reason for limited wild occurrences of LM may be the loss of key metabolic genes, especially carbohydrate-active enzymes (CAZymes), based on comparisons with other closely related species. The results of our transcriptome analyses between vegetative (mycelia) and reproductive (fruiting bodies) organs indicated that changes in gene expression among some key CAZyme genes may help to determine the switch from asexual to sexual reproduction. Taken together, our genomic and transcriptome data for LM comprise a valuable resource for both understanding the evolutionary and life history of this species.

54 ENVIRONMENTAL SCIENCES↗
DOE OSTI2021

Geographic patterns of genomic diversity and structure in the C4 grass Panicum hallii across its natural distribution

Abstract Geographic patterns of within-species genomic diversity are shaped by evolutionary processes, life history and historical and contemporary factors. New genomic approaches can be used to infer the influence of such factors on the current distribution of infraspecific lineages. In this study, we evaluated the genomic and morphological diversity as well as the genetic structure of the C4 grass Panicum hallii across its complex natural distribution in North America. We sampled extensively across the natural range of P. hallii in Mexico and the USA to generate double-digestion restriction-associated DNA (ddRAD) sequence data for 423 individuals from 118 localities. We used these individuals to study the divergence between the two varieties of P. hallii, P. hallii var. filipes and P. hallii var. hallii as well as the genetic diversity and structure within these groups. We also examined the possibility of admixture in the geographically sympatric zone shared by both varieties, and assessed distribution shifts related with past climatic fluctuations. There is strong genetic and morphological divergence between the varieties and consistent genetic structure defining seven genetic clusters that follow major ecoregions across the range. South Texas constitutes a hotspot of genetic diversity with the co-occurrence of all genetic clusters and admixture between the two varieties. It is likely a recolonization and convergence point of populations that previously diverged in isolation during fragmentation events following glaciation periods.

54 ENVIRONMENTAL SCIENCES↗
DOE OSTI2023

Ploidy evolution in a wild yeast is linked to an interaction between cell type and metabolism

Ploidy is an evolutionarily labile trait, and its variation across the tree of life has profound impacts on evolutionary trajectories and life histories. The immediate consequences and molecular causes of ploidy variation on organismal fitness are frequently less clear, although extreme mating type skews in some fungi hint at links between cell type and adaptive traits. Here, we report an unusual recurrent ploidy reduction in replicate populations of the budding yeast Saccharomyces eubayanus experimentally evolved for improvement of a key metabolic trait, the ability to use maltose as a carbon source. We find that haploids have a substantial, but conditional, fitness advantage in the absence of other genetic variation. Using engineered genotypes that decouple the effects of ploidy and cell type, we show that increased fitness is primarily due to the distinct transcriptional program deployed by haploid-like cell types, with a significant but smaller contribution from absolute ploidy. The link between cell-type specification and the carbon metabolism adaptation can be traced to the noncanonical regulation of a maltose transporter by a haploid-specific gene. This study provides novel mechanistic insight into the molecular basis of an environment–cell type fitness interaction and illustrates how selection on traits unexpectedly linked to ploidy states or cell types can drive karyotypic evolution in fungi.

59 BASIC BIOLOGICAL SCIENCES↗