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Biology subjects

Miller, C. R.

Publications and source records attributed to Miller, C. R..

At least 19 recordsLinked to original sources

{Phi}X174 bacteriophage viability predicted by protein biophysical modeling

The relationship between genotype and phenotype underlies our ability to understand and predict evolution. Efforts to build genotype-phenotype (GP) maps have revealed several unifying rules: epistasis is pervasive, fitness effects are not normally distributed, and the GP map is non-linear and complicated for high-level phenotypes. A critical step in developing GP maps is evaluating how well predictive models do in explaining observed phenotypes. We utilize the simplicity of a bacteriophage ({Phi}X174) study system to test if an intermediate phenotype (predicted stability of the G capsid protein) explains more complex phenotypes. In doing so, we compare the predictive performance of free energies of folding and binding obtained using numerous molecular modeling methods as well as phylogenetic and basic biochemical/biophysical properties of amino acid substitutions. By creating a large mutational library, we find that {Phi}X174 tolerates about 50% of the amino acid substitutions we inserted into the G protein and that molecular modeling compliments other substitution models for predicting viability. Mutations predicted to have large destabilizing effects are especially informative and are almost universally detrimental. These large-effect substitutions often coincide with the most conserved residues in the G protein. Apart from large-effect mutations, our ability to predict {Phi}X174 phenotypes is fairly poor and we explore various potential confounding factors (e.g., codon bias) that could be considered to improve viability predictions.

molecular biology↗

Bacteriophage density influences the rate of resistance evolution

The antagonistic relationship between bacteria and bacteriophages (phages) drives genetic changes that result in phage resistance. Phage resistance mutations arise in natural microbial communities and during the treatment of diseases with phages (phage therapy), making it important to understand the dynamics of resistance acquisition. It is well-established that when bacteria are challenged with phages in dense liquid cultures, bacterial populations quickly become dominated by phage-resistant variants. However, these conditions--well-mixed liquid cultures with high phage concentrations--are not necessarily common in microbial ecosystems. We developed a simplified mathematical model of phage resistance evolution to explore how phage and host concentration impact the dynamics of resistance evolution. The model was parameterized with microbial growth data from two pathogens and their phages: Pseudomonas aeruginosa and Paenibacillus larvae. Our analyses revealed two fundamental discoveries about resistance evolution. First, phage resistance evolution is predictably governed by a core set of parameters that exhibited high resolution across all bacterial strains: intrinsic growth rate of susceptible bacteria, resistance acquisition rate, fitness cost of resistance, and phage adsorption rate. Second, competitive interactions and fitness costs are the primary drivers of resistance patterns rather than intrinsic mutation rates. We observed three distinct growth patterns--delayed growth, two phase growth, and complete suppression--corresponding to specific parameter regimes as initial phage concentration increased. Two phase growth patterns emerged when competitive dynamics remained balanced, enabling coexistence of susceptible and resistant populations. Complete suppression patterns occurred when low proliferation thresholds combined with extreme competitive asymmetries created unsustainable conditions for resistant bacteria. These findings demonstrate that phage resistance evolution is fundamentally an ecological process where competitive context determines outcomes independently of mutation capacity, with important implications for phage therapy design.

evolutionary biology↗

Modeling the Relationship between the Capsid Spike Protein Stability and Fitness in {varphi}X174 Bacteriophage

BackgroundProtein function depends on the stable folding or binding of peptide chains, and the extent to which an amino acid substitution disrupts this stability can be a strong predictor of the mutations impact on the proteins function and the organisms fitness. This study seeks to understand this relationship in bacteriophage {phi}X174 using an experimental technique of deep mutational scanning and computationally predicted protein stability. ResultsAnalyzing the viability data using a newly developed multistage binomial model confirms that highly destabilizing mutations predict inviability. For single-site variants, the model predicts that {Delta}{Delta}G of folding greater than ~3 kcal/mol and {Delta}{Delta}G of binding greater than ~6 kcal/mol cuts the probability of survival by half of the maximum. The maximum probability, even for minimal {Delta}{Delta}G values, plateaus at around 87%, reflecting the influence of unobserved factors. Fitting of double-site variants data shows similar results. In contrast, a linear regression analysis of viable mutants reveals that the effect of protein stability is too weak to be a reliable predictor of fitness. ConclusionIn this study, we introduce a novel modeling technique to explore the relationship between protein stability and survival outcomes. While large destabilization often indicates inviability, most destabilizing mutations exert only small to moderate effects and do not reliably predict survival. Although protein stability is a crucial biophysical property influencing biological systems, it represents just one of multiple factors that contribute to fitness and survival.

bioinformatics↗

Standardized methods for rearing a moth larva, Manduca sexta, in a laboratory setting

The larval tobacco hornworm, Manduca sexta, has been used in a laboratory setting for physiological studies and for pathogen virulence studies. This moth offers a much larger size than the commonly used wax moth (Galleria mellonella), and it can thus be used for a greater variety of assays, such as repeated sampling of the same individual, growth measurements, and tissue sampling. Yet their occasional use in research has led to a minimally documented set of rearing methods. To facilitate further adoption of this insect model, we expanded on previously reported protocols and developed our own rearing methods, which we report here. Our protocol requires little specialized equipment, with a cost less than $100/month for the feeding and maintenance of a laboratory colony of about five hundred larvae of differing instar phases. The low cost generalized equipment and supplies, and the simplification of the standardized protocols allows for an easy entry point for rearing tobacco hornworm populations. We also describe a few methods that are relevant to the uses of these organisms as infection models.

physiology↗

Viral adaptations to alternative hosts in the honey bee pathogen Paenibacillus larvae

Bacteriophages (phages) that are intended to be used to treat bacterial infections are often improved using genetic engineering or experimental evolution. A protocol called "Appelmans" utilizes evolution in microtiter plates to promote the evolution of phages that can infect nonpermissive hosts. We tested a modification of the Appelmans protocol using the honey bee pathogen, Paenibacillus larvae. Three phages evolved together on four P. larvae strains following the standard Appelmans protocol and a modified version to ensure high phage diversity throughout ten rounds of passaging. The host range of 360 plaques were characterized and six new phage lysis patterns were identified. These new phage lysis patterns included plaque formation on previously nonpermissive, phage-resistant isolates that were used to identify phage types. The modified protocol did not drastically change the rate or number of new phage types observed but did prevent the phage population from being dominated by one phage that tended to rapidly raise in frequency. These findings showed how a minor modification of the Appelmans protocol influenced the development of phages for phage therapy. The method also provided improved phages for the treatment of bacterial infections in honey bees.

microbiology↗

Directed evolution of bacteriophages: impacts of prolific prophage

Various directed evolution methods exist that seek to procure bacteriophages with expanded host ranges, typically targeting phage-resistant or non-permissive bacterial hosts. The general premise of these methods is to propagate phage on multiple bacterial hosts, pool the lysate, and repeat the propagation process until phage(s) can form plaques on the target host(s). In theory, this propagation process produces a phage lysate that contains input phages and their evolved phage progeny. However, in practice, this phage lysate can also include prophages originating from bacterial hosts. Here we describe our experience implementing one directed evolution method, the Appelmans protocol, to study phage evolution in the Pseudomonas aeruginosa phage-host system, in which we observed rapid host-range expansion of the phage cocktail. Further experimentation and sequencing analysis revealed that this observed host-range expansion was due to a Casadabanvirus prophage that originated from one of the Appelmans hosts. Host-range analysis of the prophage showed that it could infect five of eight bacterial hosts initially used, allowing it to proliferate and persist through the end of the experiment. This prophage was represented in half of the sequenced phage samples isolated from the Appelmans experiment. This work highlights the impact of prophages in directed evolution experiments and the importance of incorporating sequencing data in analyses to verify output phages, particularly for those attempting to procure phages intended for phage therapy applications. This study also notes the usefulness of intraspecies antagonism assays between bacterial host strains to establish a baseline for inhibitory activity and determine presence of prophage. IMPORTANCEDirected evolution is a common strategy for evolving phages to expand host range, often targeting pathogenic strains of bacteria. In this study we investigated phage host-range expansion using directed evolution in the Pseudomonas aeruginosa system. We show that prophage are active players in directed evolution and can contribute to observation of host-range expansion. Since prophage are prevalent in bacterial hosts, particularly pathogenic strains of bacteria, and all directed evolution approaches involve iteratively propagating phage on one or more bacterial hosts, the presence of prophage in phage preparations is a factor that needs to be considered in experimental design and interpretation of results. These results highlight the importance of screening for prophages either genetically or through intraspecies antagonism assays during selection of bacterial strains and will contribute to improving experimental design of future directed evolution studies.

microbiology↗

Rationally Minimizing Natural Product Libraries Using Mass Spectrometry

Natural product libraries are crucial to drug development, but large libraries drastically increase the time and cost during initial high throughput screens. Here, we developed a method that leverages liquid chromatography-tandem mass spectrometry spectral similarity to dramatically reduce library size, with minimal bioactive loss. This method offers a broadly applicable strategy for accelerated drug discovery with cost reductions, which enable implementation in resource-limited settings.

bioinformatics↗

Genomic and ecological factors shaping specialism and generalism across an entire subphylum

Organisms exhibit extensive variation in ecological niche breadth, from very narrow (specialists) to very broad (generalists). Paradigms proposed to explain this variation either invoke trade-offs between performance efficiency and breadth or underlying intrinsic or extrinsic factors. We assembled genomic (1,154 yeast strains from 1,049 species), metabolic (quantitative measures of growth of 843 species in 24 conditions), and ecological (environmental ontology of 1,088 species) data from nearly all known species of the ancient fungal subphylum Saccharomycotina to examine niche breadth evolution. We found large interspecific differences in carbon breadth stem from intrinsic differences in genes encoding specific metabolic pathways but no evidence of trade-offs and a limited role of extrinsic ecological factors. These comprehensive data argue that intrinsic factors driving microbial niche breadth variation. One-Sentence SummaryA nearly complete genomic catalog of the yeast subphylum illuminates the evolution of their diverse ecologies and metabolisms.

evolutionary biology↗

Cooperativity between H3.3K27M and PDGFRA poses multiple therapeutic vulnerabilities in human iPSC-derived diffuse midline glioma avatars

Diffuse midline glioma (DMG) is a leading cause of brain tumor death in children. In addition to hallmark H3.3K27M mutations, significant subsets also harbor alterations of other genes, such as TP53 and PDGFRA. Despite the prevalence of H3.3K27M, the results of clinical trials in DMG have been mixed, possibly due to the lack of models recapitulating its genetic heterogeneity. To address this gap, we developed human iPSC-derived tumor models harboring TP53R248Q with or without heterozygous H3.3K27M and/or PDGFRAD842V overexpression. The combination of H3.3K27M and PDGFRAD842V resulted in more proliferative tumors when gene-edited neural progenitor (NP) cells were implanted into mouse brains compared to NP with either mutation alone. Transcriptomic comparison of tumors and their NP cells of origin identified conserved JAK/STAT pathway activation across genotypes as characteristic of malignant transformation. Conversely, integrated genome-wide epigenomic and transcriptomic analyses, as well as rational pharmacologic inhibition, revealed targetable vulnerabilities unique to the TP53R248Q; H3.3K27M; PDGFRAD842V tumors and related to their aggressive growth phenotype. These include AREG-mediated cell cycle control, altered metabolism, and vulnerability to combination ONC201/trametinib treatment. Taken together, these data suggest that cooperation between H3.3K27M and PDGFRA influences tumor biology, underscoring the need for better molecular stratification in DMG clinical trials.

genomics↗

Assessment of treatment-specific tethering survival bias for the juvenile blue crab Callinectes sapidus in a simulated salt marsh

The blue crab (Callinectes sapidus) is ecologically and economically important in Chesapeake Bay. Nursery habitats, such as seagrass beds, disproportionately contribute individuals to the adult segment of populations. Spartina alterniflora salt marshes are intertidal nursery habitats which may serve as a refuge from predation for juvenile blue crabs. However, the effects of various characteristics of salt marshes on nursery metrics, such as survival, have not been quantified. Comparisons of juvenile survival between salt marshes and other habitats often employ tethering to assess survival. Although experimental bias when tethering juvenile prey is well recognized, the potential for habitat-specific bias in salt marshes has not been experimentally tested. Using mesocosm experiments, we tested if tethering in simulated salt marsh habitats produces a habitat-specific bias. Juvenile crabs were randomly tethered and un-tethered in mesocosms at varying simulated shoot densities. Tethering reduced survival, and its effect was not habitat specific, irrespective of shoot density, as evidenced by a non-significant interaction effect between tethering treatment and habitat. Thus, tethering juvenile blue crabs in salt marsh habitat did not produce treatment-specific bias relative to unvegetated habitat across a range of shoot densities and survival of tethered and untethered crabs was positively related to shoot density. These findings indicate that tethering is a useful method for assessing survival in salt marshes, as with other nursery habitats including seagrass beds, algae and unstructured sand.

ecology↗

PVT1, a YAP1 dependent stress responsive lncRNA drives ovarian cancer metastasis and chemoresistance

Metastatic growth of ovarian cancer cells into the peritoneal cavity requires adaptation to various cellular stress factors to facilitate cell survival and growth. Here we demonstrate the role of PVT1, one such stress induced long non-coding RNA, in ovarian cancer growth and metastasis. PVT1 is an amplified and overexpressed lncRNA in ovarian cancer with strong predictive value for survival and response to targeted therapeutics. We find that expression of PVT1 is regulated by ovarian tumor cells in response to cellular stress, particularly loss of cell-cell contacts and changes in matrix rigidity occurring in a YAP1 dependent manner. Induction of PVT1 promotes tumor cell survival, growth, and migration. Conversely, reducing PVT1 levels robustly abrogates metastatic behavior and tumor cell dissemination in cell lines and syngeneic transplantation models in vivo. We find that reducing PVT1 causes widespread transcriptome changes leading to alterations in cellular stress response and metabolic pathways including doxorubicin metabolism, which directly impacts chemosensitivity. Together, these findings implicate PVT1 as a promising therapeutic target to suppress metastasis and avoid chemoresistance in ovarian cancer. SUMMARY BLURBPVT1 is a stress-responsive IncRNA regulated by YAP1, leading to increased ovarian cancer metastasis and chemoresistance, making PVT1 a promising therapeutic target.

cancer biology↗

Reciprocal epigenetic Sox2 regulation by SMAD1-SMAD3 is critical for anoikis resistance and metastasis in cancer

Growth factors in the tumor environment are key regulators of cell survival and metastasis. Here we reveal, dichotomy between TGF-{beta} superfamily growth factors BMP and TGF-{beta}/activin, and their downstream SMAD effectors. Gene expression profiling uncovered Sox2 as a key signaling node regulated in an opposing manner by anoikis-promoting BMP2, 4 and 9, and anoikis-suppressing TGF-{beta} and activin A. We find that Sox2 repression by BMPs robustly inhibits intraperitoneal tumor burden and increases survival in multiple ovarian cancer models. Repression of Sox2 is driven by SMAD1 dependent histone H3K27me3 recruitment and DNA methylation at SOX2s promoter. Conversely, TGF-{beta} and activin A promote Sox2 expression, and anoikis resistance by SMAD3 mediated histone H3K4me3 recruitment. We find that balancing Sox2 levels is critical for anoikis, as transcriptomics reveals regulation of key cell death pathways. Moreover, BMP-driven SMAD1 signaling can override TGF-{beta} and activins effect on Sox2, which has clinical significance due to the high levels of TGF-{beta} we find in ovarian cancer patients. Together, our findings identify Sox2 as a contextual and contrastingly regulated key node, downstream of TGF-{beta} superfamily members controlling anoikis and metastasis in ovarian cancers. HighlightsO_LISox2 is a key node for anoikis resistance in cancer C_LIO_LISox2 is differentially regulated by TGF-{beta}/activin and BMPs in broad cancers C_LIO_LIBMP9 is a robust metastasis suppressor by lowering Sox2 C_LIO_LISox2 regulation is contextual, epigenetic and at the transcriptional level C_LI

cancer biology↗

Mutational switch-backs can accelerate evolution of Francisella to a combination of ciprofloxacin and doxycycline

Combination antimicrobial therapy has been considered a promising strategy to combat the evolution of antimicrobial resistance. Francisella tularensis is the causative agent of tularemia and in addition to being found in the nature, is recognized as a threat agent that requires vigilance. We investigated the evolutionary outcome of adapting the Live Vaccine Strain (LVS) of Francisella to two non-interacting drugs, ciprofloxacin and doxycycline, individually, sequentially, and in combination. Despite their individual efficacies and independence of mechanisms, evolution to the combination appeared to progress faster than evolution to the two drugs sequentially. We conducted a longitudinal mutational analysis of the populations evolving to the drug combination, genetically reconstructed the identified evolutionary pathway, and carried out biochemical validation. We discovered that, after the appearance of an initial weak generalist mutation (FupA/B), each successive mutation alternated between adaptation to one drug or the other. In combination, these mutations allowed the population to more efficiently ascend the fitness peak through a series of evolutionary switch-backs. Clonal interference, weak pleiotropy, and positive epistasis also contributed to combinatorial evolution. This finding suggests that, under some selection conditions, the use of non-interacting drug pairs as a treatment strategy may result in a more rapid ascent to multi-drug resistance and serves as a cautionary tale. Author summaryThe antimicrobial resistance crisis requires the use of novel treatment strategies to prevent or delay the emergence of resistance. Combinations of drugs offer one strategy to delay resistance, but the efficacy of such drug combinations depends on the evolutionary response of the organism. Using experimental evolution, we show that under some conditions, a potential drug combination does not delay the onset of resistance in bacteria responsible for causing tularemia, Francisella. In fact, they evolve resistance to the combination faster than when the two drugs are applied sequentially. This result is surprising and concerning: using this drug combination in a hospital setting could lead to simultaneous emergence of resistance to two antibiotics. Employing whole genome sequencing, we identified the molecular mechanism leading to evolution of resistance to the combination. The mechanism is similar to the switch-back route used by hikers while scaling steep mountains i.e., instead of simultaneously acquiring mutations conferring resistance to both drugs, the bacteria acquire mutations to each drug in alternating manner. Rather than scaling the steep mountain directly, the bacteria ascend the mountain by a series of evolutionary switch-backs to gain elevation and in doing so, they get to the top more efficiently.

evolutionary biology↗

Global composition of the bacteriophage community in honeybees

The microbial communities in animal digestive systems are critical to host development and health. These assemblages of primarily viruses, bacteria, and fungi stimulate the immune system during development, synthesize important chemical compounds like hormones, aid in digestion, competitively exclude pathogens, etc. The bacteriophages in animal microbiomes are harder to characterize than the bacterial or fungal components of the microbiome and thus we know comparatively little about the temporal and spatial dynamics of bacteriophage communities in animal digestive systems. Recently, the bacteriophages of the honeybee gut were characterized in two European bee populations. Most of the bacteriophages described in these two reports were novel, encoded many metabolic genes in their genomes, and had a community structure that suggests coevolution with their bacterial hosts. To describe the conservation of bacteriophages in bees and begin to understand their role in the bee microbiome, we sequenced the virome of Apis mellifera from Austin, Texas and compared bacteriophage composition between three locations around the world. We found that the majority of bacteriophages from Austin are novel, sharing no sequence similarity to anything in public repositories. However, many bacteriophages are shared among the three bee viromes, indicating specialization of bacteriophages in the bee gut. Our study along with the two previous bee virome studies shows that the bee gut bacteriophage community is simple compared to that of many animals, consisting of several hundred types of bacteriophages that primarily infect four of the dominant bacterial phylotypes in the bee gut.

microbiology↗

SARS-CoV-2 Viral Replication in a High Throughput Human Primary Epithelial Airway Organ Model

COVID-19 emerged as a worldwide pandemic early in 2020, and at this writing has caused over 170 million cases and 3.7 million deaths worldwide, and almost 600,000 deaths in the United States. The rapid development of several safe and highly efficacious vaccines stands as one of the most extraordinary achievements in modern medicine, but the identification and administration of efficacious therapeutics to treat patients suffering from COVID-19 has been far less successful. A major factor limiting progress in the development of effective treatments has been a lack of suitable preclinical models for the disease, currently reliant upon various animal models and in vitro culture of immortalized cell lines. Here we report the first successful demonstration of SARS-CoV-2 infection and viral replication in a human primary cell-based organ-on-chip, leveraging a recently developed tissue culture platform known as PREDICT96. This successful demonstration of SARS-CoV-2 infection in human primary airway epithelial cells derived from a living donor represents a powerful new pathway for disease modeling and an avenue for screening therapeutic candidates in a high throughput platform.

bioengineering↗

Rhinovirus reduces the severity of subsequent respiratory viral infections, which is associated with dampened inflammatory responses

Coinfection by unrelated viruses in the respiratory tract is common and can result in changes in disease severity compared to infection by individual virus strains. We have previously shown that inoculation of mice with rhinovirus (RV) two days prior to inoculation with a lethal dose of influenza A virus (PR8), provides complete protection against mortality and reduces morbidity. In this study, we extended that finding to a second lethal respiratory virus, pneumonia virus of mice (PVM) and analyzed potential mechanisms whereby RV reduces lethal viral pneumonia caused by PR8 and PVM. RV prevented mortality and weight loss associated with PVM infection, suggesting that RV-mediated protection is more effective against PVM than PR8. Major changes in host gene expression upon PVM infection were delayed compared to PR8, which likely provides a larger time frame for RV-induced gene expression to alter the course of disease. Overall, RV induced earlier recruitment of inflammatory cells, while these populations were reduced at later times in RV-inoculated mice. Findings common to both virus pairs included upregulated expression of mucin-associated genes and dampening of inflammation-related genes in mice that were inoculated with RV prior to lethal virus infection. However, type I IFN signaling was required for RV-mediated protection against PR8, but not PVM. IFN signaling had minor effects on PR8 replication and contributed to controlling neutrophilic inflammation and subsequent hemorrhagic lung pathology in RV/PR8 infected mice. These findings, combined with differences in virus replication levels and disease severity, suggest that the suppression of inflammation in RV/PVM infected mice may be due to early, IFN-independent suppression of viral replication, while in RV/PR8 infected mice may be due to IFN-dependent modulation of immune responses. Thus, a mild upper respiratory viral infection can reduce the severity of a subsequent severe viral infection in the lungs through virus-dependent mechanisms. Author SummaryRespiratory viruses from diverse families co-circulate in human populations and are frequently detected within the same host. Though clinical studies suggest that infection by more than one unrelated respiratory virus may alter disease severity, animal models in which we can control the doses, timing, and strains of coinfecting viruses are critical to understand how coinfection affects disease severity. In this study, we compared gene expression and immune cell recruitment between two pairs of viruses (RV/PR8 and RV/PVM) inoculated sequentially in mice that both result in reduced severity compared to lethal infection by PR8 or PVM alone. Reduced disease severity was associated with suppression of inflammatory responses in the lungs. However, differences in disease kinetics and host and viral gene expression suggest that protection by coinfection with RV may be due to distinct molecular mechanisms. Indeed, we found that antiviral cytokine signaling was required for RV-mediated protection against lethal infection by PR8, but not PVM.

microbiology↗

High-Throughput Human Primary Cell-Based Airway Model for Evaluating Influenza, Coronavirus, or other Respiratory Viruses in vitro

Influenza and other respiratory viruses represent a significant threat to public health, national security, and the world economy, and can lead to the emergence of global pandemics such as the current COVID-19 crisis. One of the greatest barriers to the development of effective therapeutic agents to treat influenza, coronaviruses, and many other infections of the respiratory tract is the absence of a robust preclinical model. Preclinical studies currently rely on high-throughput, low-fidelity in vitro screening with cell lines and/or low-throughput animal models that often provide a poor correlation to human clinical responses. Here, we introduce a human primary airway epithelial cell-based model integrated into a high-throughput platform where tissues are cultured at an air-liquid interface (PREDICT96-ALI). We present results on the application of this platform to influenza and coronavirus infections, providing multiple readouts capable of evaluating viral infection kinetics and potentially the efficacy of therapeutic agents in an in vitro system. Several strains of influenza A virus are shown to successfully infect the human primary cell-based airway tissue cultured at an air-liquid interface (ALI), and as a proof-of-concept, the effect of the antiviral oseltamivir on one strain of Influenza A is evaluated. Human coronaviruses NL63 (HCoV-NL63) and SARS-CoV-2 enter host cells via ACE2 and utilize the protease TMPRSS2 for protein priming, and we confirm expression of both in our ALI model. We also demonstrate coronavirus infection in this system with HCoV-NL63, observing sufficient viral propagation over 96 hours post-infection to indicate successful infection of the primary cell-based model. This new capability has the potential to address a gap in the rapid assessment of therapeutic efficacy of various small molecules and antiviral agents against influenza and other respiratory viruses including coronaviruses.

microbiology↗

{Phi}X174 Attenuation by Whole Genome Codon Deoptimization

Natural selection acting on synonymous mutations in protein-coding genes influences genome composition and evolution. In viruses, introducing synonymous mutations in genes encoding structural proteins can drastically reduce viral growth, providing a means to generate potent, live attenuated vaccine candidates. However, an improved understanding of what compositional features are under selection and how combinations of synonymous mutations affect viral growth is needed to predictably attenuate viruses and make them resistant to reversion. We systematically recoded all non-overlapping genes of the bacteriophage {Phi}X174 with codons rarely used in its E. coli host. The fitness of recombinant viruses decreases as additional deoptimizing mutations are made to the genome, although not always linearly, and not consistently across genes. Combining deoptimizing mutations may reduce viral fitness more or less than expected from the effect size of the constituent mutations and we point out difficulties in untangling correlated compositional features. We test our model by optimizing the same genes and find that the relationship between codon usage and fitness does not hold for optimization, suggesting that wild-type {Phi}X174 is at a fitness optimum. This work highlights the need to better understand how selection acts on patterns of synonymous codon usage across the genome and provides a convenient system to investigate the genetic determinants of virulence.

genomics↗