Selection-based model of prokaryote pangenomes

AbstractThe genomes of different individuals of the same prokaryote species can vary widely in gene content, displaying different proportions of core genes, which are present in all genomes, and accessory genes, whose presence varies between genomes. Together, these core and accessory genes make up a species’ pangenome. The reasons behind this extensive diversity in gene content remain elusive, and there is an ongoing debate about the contribution of accessory genes to fitness, that is, whether their presence is on average advantageous, neutral, or deleterious. In order to explore this issue, we developed a mathematical model to simulate the gene content of prokaryote genomes and pangenomes. Our model focuses on testing how the fitness effects of genes and their rates of gene gain and loss would affect the properties of pangenomes. We first show that pangenomes with large numbers of low-frequency genes can arise due to the gain and loss of neutral and nearly neutral genes in a population. However, pangenomes with large numbers of highly beneficial, low-frequency genes can arise as a consequence of genotype-by-environment interactions when multiple niches are available to a species. Finally, pangenomes can arise, irrespective of the fitness effect of the gained and lost genes, as long as gene gain and loss rates are high. We argue that in order to understand the contribution of different mechanisms to pangenome diversity, it is crucial to have empirical information on population structure, gene-by-environment interactions, the distributions of fitness effects and rates of gene gain and loss in different prokaryote groups.

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A Genomic Survey of Signalling in the Myxococcaceae

Microorganisms ◽

10.3390/microorganisms8111739 ◽

2020 ◽

Vol 8 (11) ◽

pp. 1739

Author(s):

David E. Whitworth ◽

Allison Zwarycz

Keyword(s):

Core Genome ◽

Gene Gain ◽

Fruiting Body Formation ◽

Two Component System ◽

Genome Sequences ◽

The Core ◽

Accessory Genes ◽

Two Component ◽

Gain Loss ◽

Core Genes

As prokaryotes diverge by evolution, essential ‘core’ genes required for conserved phenotypes are preferentially retained, while inessential ‘accessory’ genes are lost or diversify. We used the recently expanded number of myxobacterial genome sequences to investigate the conservation of their signalling proteins, focusing on two sister genera (Myxococcus and Corallococcus), and on a species within each genus (Myxococcus xanthus and Corallococcus exiguus). Four new C. exiguus genome sequences are also described here. Despite accessory genes accounting for substantial proportions of each myxobacterial genome, signalling proteins were found to be enriched in the core genome, with two-component system genes almost exclusively so. We also investigated the conservation of signalling proteins in three myxobacterial behaviours. The linear carotenogenesis pathway was entirely conserved, with no gene gain/loss observed. However, the modular fruiting body formation network was found to be evolutionarily plastic, with dispensable components in all modules (including components required for fruiting in the model myxobacterium M. xanthus DK1622). Quorum signalling (QS) is thought to be absent from most myxobacteria, however, they generally appear to be able to produce CAI-I (cholerae autoinducer-1), to sense other QS molecules, and to disrupt the QS of other organisms, potentially important abilities during predation of other prokaryotes.

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Selection Is a Significant Driver of Gene Gain and Loss in the Pangenome of the Bacterial Genus Sulfurovum in Geographically Distinct Deep-Sea Hydrothermal Vents

mSystems ◽

10.1128/msystems.00673-19 ◽

2020 ◽

Vol 5 (2) ◽

Cited By ~ 4

Author(s):

Alief Moulana ◽

Rika E. Anderson ◽

Caroline S. Fortunato ◽

Julie A. Huber

Keyword(s):

Natural Selection ◽

Nutrient Limitation ◽

Deep Sea ◽

Hydrothermal Vent ◽

Hydrothermal Vents ◽

Gene Content ◽

Microbial Populations ◽

Gene Gain ◽

Microbial Genomes ◽

Gain And Loss

ABSTRACT Microbial genomes have highly variable gene content, and the evolutionary history of microbial populations is shaped by gene gain and loss mediated by horizontal gene transfer and selection. To evaluate the influence of selection on gene content variation in hydrothermal vent microbial populations, we examined 22 metagenome-assembled genomes (MAGs) (70 to 97% complete) from the ubiquitous vent Epsilonbacteraeota genus Sulfurovum that were recovered from two deep-sea hydrothermal vent regions, Axial Seamount in the northeastern Pacific Ocean (13 MAGs) and the Mid-Cayman Rise in the Caribbean Sea (9 MAGs). Genes involved in housekeeping functions were highly conserved across Sulfurovum lineages. However, genes involved in environment-specific functions, and in particular phosphate regulation, were found mostly in Sulfurovum genomes from the Mid-Cayman Rise in the low-phosphate Atlantic Ocean environment, suggesting that nutrient limitation is an important selective pressure for these bacteria. Furthermore, genes that were rare within the pangenome were more likely to undergo positive selection than genes that were highly conserved in the pangenome, and they also appeared to have experienced gene-specific sweeps. Our results suggest that selection is a significant driver of gene gain and loss for dominant microbial lineages in hydrothermal vents and highlight the importance of factors like nutrient limitation in driving microbial adaptation and evolution. IMPORTANCE Microbes can alter their gene content through the gain and loss of genes. However, there is some debate as to whether natural selection or neutral processes play a stronger role in molding the gene content of microbial genomes. In this study, we examined variation in gene content for the Epsilonbacteraeota genus Sulfurovum from deep-sea hydrothermal vents, which are dynamic habitats known for extensive horizontal gene transfer within microbial populations. Our results show that natural selection is a strong driver of Sulfurovum gene content and that nutrient limitation in particular has shaped the Sulfurovum genome, leading to differences in gene content between ocean basins. Our results also suggest that recently acquired genes undergo stronger selection than genes that were acquired in the more distant past. Overall, our results highlight the importance of natural selection in driving the evolution of microbial populations in these dynamic habitats.

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Analysis of gene gain and loss in the evolution of predatory bacteria

Gene ◽

10.1016/j.gene.2016.10.039 ◽

2017 ◽

Vol 598 ◽

pp. 63-70 ◽

Cited By ~ 6

Author(s):

Nan Li ◽

Kai Wang ◽

Henry N Williams ◽

Jun Sun ◽

Changling Ding ◽

...

Keyword(s):

Gene Gain ◽

Predatory Bacteria ◽

Gain And Loss

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Patterns and Implications of Gene Gain and Loss in the Evolution of Prochlorococcus

PLoS Genetics ◽

10.1371/journal.pgen.0030231.eor ◽

2005 ◽

Vol preprint (2007) ◽

pp. e231

Author(s):

Gregory C Kettler ◽

Adam C. Martiny ◽

Katherine Huang ◽

Jeremy Zucker ◽

Maureen Coleman ◽

...

Keyword(s):

Gene Gain ◽

Gain And Loss

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Patterns of gene content and co-occurrence constrain the evolutionary path toward animal association in CPR bacteria

10.1101/2021.03.03.433784 ◽

2021 ◽

Author(s):

Alexander L. Jaffe ◽

Christine He ◽

Ray Keren ◽

Luis E. Valentin-Alvarado ◽

Patrick Munk ◽

...

Keyword(s):

Acid Metabolism ◽

Gene Content ◽

Gene Gain ◽

Protein Families ◽

Bacterial Host ◽

Genomic Change ◽

Symbiotic Associations ◽

Genomic Signatures ◽

Host Relationships ◽

Candidate Phyla Radiation

ABSTRACTCandidate Phyla Radiation (CPR) bacteria are small, likely episymbiotic organisms found across Earth’s ecosystems. Despite their prevalence, the distribution of CPR lineages across habitats and the genomic signatures of transitions amongst these habitats remain unclear. Here, we expand the genome inventory for Absconditabacteria (SR1), Gracilibacteria, and Saccharibacteria (TM7), CPR bacteria known to occur in both animal-associated and environmental microbiomes, and investigate variation in gene content with habitat of origin. By overlaying phylogeny with habitat information, we show that bacteria from these three lineages have undergone multiple transitions from environmental habitats into animal microbiomes. Based on co-occurrence analyses of hundreds of metagenomes, we extend the prior suggestion that certain Saccharibacteria have broad bacterial host ranges and constrain possible host relationships for Absconditabacteria and Gracilibacteria. Full-proteome analyses show that animal-associated Saccharibacteria have smaller gene repertoires than their environmental counterparts and are enriched in numerous protein families, including those likely functioning in amino acid metabolism, phage defense, and detoxification of peroxide. In contrast, some freshwater Saccharibacteria encode a putative rhodopsin. For protein families exhibiting the clearest patterns of differential habitat distribution, we compared protein and species phylogenies to estimate the incidence of lateral gene transfer and genomic loss occurring over the species tree. These analyses suggest that habitat transitions were likely not accompanied by large transfer or loss events, but rather were associated with continuous proteome remodeling. Thus, we speculate that CPR habitat transitions were driven largely by availability of suitable host taxa, and were reinforced by acquisition and loss of some capacities.IMPORTANCEStudying the genetic differences between related microorganisms from different environment types can indicate factors associated with their movement among habitats. This is particularly interesting for bacteria from the Candidate Phyla Radiation because their minimal metabolic capabilities require symbiotic associations with microbial hosts. We found that shifts of Absconditabacteria, Gracilibacteria, and Saccharibacteria between environmental ecosystems and mammalian mouths/guts probably did not involve major episodes of gene gain and loss; rather, gradual genomic change likely followed habitat migration. The results inform our understanding of how little-known microorganisms establish in the human microbiota where they may ultimately impact health.

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Dissociable oscillatory networks support gain and loss processing in human orbitofrontal cortex

10.1101/2021.02.25.432874 ◽

2021 ◽

Author(s):

Ignacio Saez ◽

Jack Lin ◽

Edward Chang ◽

Josef Parvizi ◽

Robert T. Knight ◽

...

Keyword(s):

Neural Activity ◽

Orbitofrontal Cortex ◽

Low Frequency ◽

Brain Regions ◽

Reward Processing ◽

Neural Oscillations ◽

Beta Band ◽

Neuronal Ensembles ◽

Gain And Loss

AbstractHuman neuroimaging and animal studies have linked neural activity in orbitofrontal cortex (OFC) to valuation of positive and negative outcomes. Additional evidence shows that neural oscillations, representing the coordinated activity of neuronal ensembles, support information processing in both animal and human prefrontal regions. However, the role of OFC neural oscillations in reward-processing in humans remains unknown, partly due to the difficulty of recording oscillatory neural activity from deep brain regions. Here, we examined the role of OFC neural oscillations (<30Hz) in reward processing by combining intracranial OFC recordings with a gambling task in which patients made economic decisions under uncertainty. Our results show that power in different oscillatory bands are associated with distinct components of reward evaluation. Specifically, we observed a double dissociation, with a selective theta band oscillation increase in response to monetary gains and a beta band increase in response to losses. These effects were interleaved across OFC in overlapping networks and were accompanied by increases in oscillatory coherence between OFC electrode sites in theta and beta band during gain and loss processing, respectively. These results provide evidence that gain and loss processing in human OFC are supported by distinct low-frequency oscillations in networks, and provide evidence that participating neuronal ensembles are organized functionally through oscillatory coherence, rather than local anatomical segregation.

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A TEST FOR RARE MALE MATING ADVANTAGE WITH DROSOPHILA PSEUDOOBSCURA KARYOTYPES

Genetics ◽

10.1093/genetics/107.4.577 ◽

1984 ◽

Vol 107 (4) ◽

pp. 577-589

Author(s):

Wyatt W Anderson ◽

Celeste J Brown

Keyword(s):

Mating Success ◽

Low Frequency ◽

Behavioral Observation ◽

Drosophila Pseudoobscura ◽

Male Mating ◽

Frequency Dependent ◽

Mating Advantage ◽

Large Numbers ◽

Laboratory Populations ◽

Statistical Artifact

ABSTRACT Recent work has called into question the reality of the rare male mating advantage, pointing out that it could be a statistical artifact of marking flies for behavioral observation or of experimental bias in collecting males. We designed an experiment to test for rare male mating advantage that avoids these sources of bias. Large numbers of males of three Drosophila pseudoobscura karyotypes were allowed to mate with females of one karyotype in population cages. The females were then isolated before multiple mating occurred and their progeny used to diagnose the males that mated them. Populations were studied at five sets of male karyotypic frequencies. The mating success of the male homokaryotypes ST/ST and CH/CH, relative to that of the heterokaryotype ST/CH, was frequency dependent. Both ST/ST and CH/CH males displayed a statistically significant mating advantage at low frequency by comparision with their mating success in the midrange of karyotypic frequencies. Both male homokaryotypes also showed a significantly greater mating success at high homokaryotypic frequency than at intermediate frequencies, which is the same as saying that the heterokaryotype not only failed to show a rare male advantage but actually suffered a mating disadvantage at low frequency. We conclude that rare male mating advantage is not always an experimental or methodological artifact but does occur in laboratory populations of D. pseudoobscura. It may occur for some genotypes and not for others, however, and it may be only one of several forms of frequency-dependent mating behavior operating in a population.

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