In natural environments, bacteria survive conditions of starvation and stress. Long-term batch cultures are an excellent laboratory system to study adaptation during nutrient stress because cells can incubate for months to years without the addition of nutrients. During long-term batch culture, cells adapt to acquire energy from cellular detritus, creating a complex and dynamic environment for mutants of increased relative fitness to exploit. Here, we analyzed the genomes of 1,117 clones isolated from a single long-term batch culture incubated for 1,200 days. A total of 679 mutations included single nucleotide polymorphisms, indels, mobile genetic element movement, large deletions up to 64 kbp, and amplifications up to ∼500 kbp. During the 3.3-year incubation, two main lineages diverged, evolving continuously. At least twice, a previously fixed mutation reverted back to the wild-type allele, suggesting beneficial mutations may later become maladaptive due to the dynamic environment and changing selective pressures. Most of the mutated genes encode proteins involved in metabolism, transport, or transcriptional regulation. Clones from the two lineages are physiologically distinct, based on outgrowth in fresh medium and competition against the parental strain. Similar population dynamics and mutations in hfq, rpoS, paaX, lrp, sdhB, and dtpA were detected in three additional parallel populations sequenced through day 60, providing evidence for positive selection. These data provide new insight into the population structure and mutations that may be beneficial during periods of starvation in evolving bacterial communities. IMPORTANCE Bacteria have remarkable metabolic capabilities and adaptive plasticity, enabling them to survive in changing environments. In nature, bacteria spend a majority of their time in a state of slow growth or maintenance, scavenging nutrients for survival. Here, a population of Escherichia coli cells was incubated for 1,200 days in long-term batch culture, without the addition of new medium, requiring cells to continuously recycle nutrients. Whole-genome resequencing of cells from the evolving population identified two dominant subpopulations that coexisted while continuously acquiring and fixing new mutations. The population dynamics and alleles identified provide insight into adaptation to nutrient stress. Elucidating mechanisms that allow bacteria to adapt through cycles of feast and famine deepens our understanding of their survival mechanisms in nature.
Sixty‐four genomic loci and seven genes that contribute to heritable variation in a model quantitative trait—resistance to oxidative stress—are identified across three yeast strains. The high‐resolution understanding of this phenotype provides new insight into the genetic and molecular basis of quantitative traits.
Genetic heterogeneity occurs when individuals express similar phenotypes as a result of different underlying mechanisms. Although such heterogeneity is known to be a potential source of unexplained heritability in genetic mapping studies, its prevalence and molecular basis are not fully understood. Here we show that substantial genetic heterogeneity underlies a model phenotype-the ability to grow invasively-in a cross of two Saccharomyces cerevisiae strains. The heterogeneous basis of this trait across genotypes and environments makes it difficult to detect causal loci with standard genetic mapping techniques. However, using selective genotyping in the original cross, as well as in targeted backcrosses, we detected four loci that contribute to differences in the ability to grow invasively. Identification of causal genes at these loci suggests that they act by changing the underlying regulatory architecture of invasion. We verified this point by deleting many of the known transcriptional activators of invasion, as well as the gene encoding the cell surface protein Flo11 from five relevant segregants and showing that these individuals differ in the genes they require for invasion. Our work illustrates the extensive genetic heterogeneity that can underlie a trait and suggests that regulatory rewiring is a basic mechanism that gives rise to this heterogeneity.KEYWORDS complex traits; genetic mapping; invasive growth; regulatory networks; yeast G ENETIC studies in humans and model organisms have reported unexplained heritability for many traits (Manolio et al. 2009). A possible contributor to this "missing" heritability is genetic heterogeneity-individuals exhibiting similar phenotypes owing to different genetic and molecular mechanisms (Risch 2000;McClellan and King 2010;Wray and Maier 2014). Genetic heterogeneity can reduce the statistical power of mapping studies (Manchia et al. 2013;Wray and Maier 2014) and may involve multiple variants segregating in the same gene (allelic heterogeneity) or different genes (nonallelic heterogeneity) (Risch 2000). Work to date has shown that allelic heterogeneity is widespread (e.g., McClellan and King 2010;Ehrenreich et al. 2012;Long et al. 2014) and often involves two or more null or partial loss-of-function variants segregating in a single phenotypically important gene (e.g., Nogee et al. 2000;Sutcliffe et al. 2005;Will et al. 2010). However, the prominence and underlying mechanisms of nonallelic heterogeneity are less understood.In this paper we describe an example of nonallelic heterogeneity using heritable variation in the ability of Saccharomyces cerevisiae strains to undergo haploid invasive growth as our model. Invasive growth is a phenotype that is triggered by low carbon or nitrogen availability and is thought to be an adaptive response that allows yeast cells to adhere to and penetrate surfaces (Cullen and Sprague 2000). Invasion typically requires expression of FLO11, which encodes a cell surface glycoprotein that facilitates cell-cell and cell-surface adhes...
Frogs and toads (anurans) are widely used to study many biological processes. Yet, few anuran genomes have been sequenced, limiting research on these organisms. Here, we produce a draft genome for the Mexican spadefoot toad, Spea multiplicata, which is a member of an unsequenced anuran clade. Atypically for amphibians, spadefoots inhabit deserts. Consequently, they possess many unique adaptations, including rapid growth and development, prolonged dormancy, phenotypic (developmental) plasticity, and adaptive, interspecies hybridization. We assembled and annotated a 1.07 Gb Sp. multiplicata genome containing 19,639 genes. By comparing this sequence to other available anuran genomes, we found gene amplifications in the gene families of nodal, hyas3, and zp3 in spadefoots, and obtained evidence that anuran genome size differences are partially driven by variability in intergenic DNA content. We also used the genome to identify genes experiencing positive selection and to study gene expression levels in spadefoot hybrids relative to their pure-species parents. Completion of the Sp. multiplicata genome advances efforts to determine the genetic bases of spadefoots' unique adaptations and enhances comparative genomic research in anurans.
Although chromosomal duplications are often deleterious, in some cases they enhance cells’ abilities to tolerate specific genetic or environmental challenges. Identifying the genes that confer these conditionally beneficial effects to particular chromosomal duplications can improve our understanding of the genetic and molecular mechanisms that enable certain aneuploidies to persist in cell populations and contribute to disease and evolution. Here, we perform a screen for spontaneous mutations that improve the tolerance of haploid Saccharomyces cerevisiae to hydrogen peroxide. Chromosome IV duplication is the most frequent mutation, as well as the only change in chromosomal copy number seen in the screen. Using a genetic mapping strategy that involves systematically deleting segments of a duplicated chromosome, we show that the chromosome IV’s duplication effect is largely due to the generation of a second copy of the stress-inducible cytoplasmic thioredoxin peroxidase TSA2. Our findings add to a growing body of literature that shows the conditionally beneficial effects of chromosomal duplication are typically mediated by a small number of genes that enhance tolerance to specific stresses when their copy numbers are increased.
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