Detecting patterns of accessory genome coevolution in Staphylococcus aureus using data from thousands of genomes

Mehta, Rohan S; Petit, Robert A.; Read, Timothy D.; Weissman, Daniel B.

doi:10.1186/s12859-023-05363-4

Cited by 7 publications

(5 citation statements)

References 41 publications

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“…One hypothesis is that these genes were gained or lost in a coordinated manner to drive the formation of the Asian clades. To confirm this, the top 31 genes, which did not include unannotated genes, were subjected to gene coevolution analysis using the R package Detecting Coevolving Traits Using Relatives (DeCoTUR) ( 29 ). The two interaction clusters are shown in Fig.…”

Section: Resultsmentioning

confidence: 99%

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Global genetic diversity and Asian clades evolution: a phylogeographic study of Staphylococcus aureus sequence type 5

Chen,

Yin,

Chen

et al. 2024

Antimicrob Agents Chemother

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Staphylococcus aureus sequence type (ST) 5 has spread worldwide; however, phylogeographic studies on the evolution of global phylogenetic and Asian clades of ST5 are lacking. This study included 368 ST5 genome sequences, including 111 newly generated sequences. Primary phylogenetic analysis suggested that there are five clades, and geographical clustering of ST5 methicillin-resistant S. aureus (MRSA) was linked to the acquisition of S. aureus pathogenicity islands (SaPIs; enterotoxin gene island) and integration of the prophage φSa3. The most recent common ancestor of global S. aureus ST5 dates back to the mid-1940s, coinciding with the clinical introduction of penicillin. Bayesian phylogeographic inference allowed to ancestrally trace the Asian ST5 MRSA clade to Japan, which may have spread to major cities in China and Korea in the 1990s. Based on a pan-genome-wide association study, the emergence of Asian ST5 clades was attributed to the gain of prophages, SaPIs, and plasmids, as well as the coevolution of resistance genes. Clade IV displayed greater genomic diversity than the Asian MRSA clades. Collectively, our study provides in-depth insights into the global evolution of S. aureus ST5 mainly in China and the United States and reveals that different S. aureus ST5 clades have arisen independently in different parts of the world, with limited geographic dispersal across continents.

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Section: Resultsmentioning

confidence: 99%

“…DeCoTUR was developed to detect coevolving genes in large datasets of bacterial genomes based on pairwise comparisons of closely related individuals, analogous to a pedigree study in eukaryotic populations ( 29 ). Here, DeCoTUR was used to perform gene association/dissociation analyses for the 146 S .…”

Section: Methodsmentioning

confidence: 99%

Global genetic diversity and Asian clades evolution: a phylogeographic study of Staphylococcus aureus sequence type 5

Chen,

Yin,

Chen

et al. 2024

Antimicrob Agents Chemother

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“…Second, our smaller data set (558 genomes) compared with other studies that number thousands of genomes may also limit the magnitude of accessory gene pool that we can identify. S. aureus is known to have an open pan-genome ( 40 – 42 ), that is, the pan-genome has no upper limit and new genes are discovered with the addition of new strains ( 18 , 43 ). It is therefore likely that the co-occurrence networks and history of gene gain and loss will be affected with the addition of genomes and novel genes.…”

Section: Discussionmentioning

confidence: 99%

Evolutionary dynamics of the accessory genomes of Staphylococcus aureus

Piper,

Ikhimiukor,

Souza

et al. 2024

mSphere

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Staphylococcus aureus is a ubiquitous commensal and opportunistic bacterial pathogen that can cause a wide gamut of infections, which are exacerbated by the presence of multidrug-resistant and methicillin-resistant S. aureus . S. aureus is genetically heterogeneous and consists of numerous distinct lineages. Using 558 complete genomes of S. aureus , we aim to determine how the accessory genome content among phylogenetic lineages of S. aureus is structured and has evolved. Bayesian hierarchical clustering identified 10 sequence clusters, of which seven contained major sequence types (ST 1, 5, 8, 30, 59, 239, and 398). The seven sequence clusters differed in their accessory gene content, including genes associated with antimicrobial resistance and virulence. Focusing on the two largest clusters, BAPS8 and BAPS10, and each consisting mostly of ST5 and ST8, respectively, we found that the structure and connected components in the co-occurrence networks of accessory genomes varied between them. These differences are explained, in part, by the variation in the rates at which the two sequence clusters gained and lost accessory genes, with the highest rate of gene accumulation occurring recently in their evolutionary histories. We also identified a divergent group within BAPS10 that has experienced high gene gain and loss early in its history. Together, our results show highly variable and dynamic accessory genomes in S. aureus that are structured by the history of the specific lineages that carry them. IMPORTANCE Staphylococcus aureus is an opportunistic, multi-host pathogen that can cause a variety of benign and life-threatening infections. Our results revealed considerable differences in the structure and evolution of the accessory genomes of major lineages within S. aureus . Such genomic variation within a species can have important implications on disease epidemiology, pathogenesis of infection, and interactions with the vertebrate host. Our findings provide important insights into the underlying genetic basis for the success of S. aureus as a highly adaptable and resistant pathogen, which will inform current efforts to control and treat staphylococcal diseases.

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“…While this provides important information about the long-term rates of recombination within gut commensal species, it is possible that much of this core-genome hybridization could be driven by positive selection on linked accessory genes (e.g., antibiotic resistance genes). Future applications of our methods on growing collections of clonal isolates [ 93 ] could shed light on these functional targets of horizontal transfer [ 94 ], and thereby provide a fuller picture of the landscape of bacterial recombination within the gut microbiota.…”

Section: Discussionmentioning

confidence: 99%

Dynamics of bacterial recombination in the human gut microbiome

Liu,

Good

2024

PLoS Biol

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Horizontal gene transfer (HGT) is a ubiquitous force in microbial evolution. Previous work has shown that the human gut is a hotspot for gene transfer between species, but the more subtle exchange of variation within species—also known as recombination—remains poorly characterized in this ecosystem. Here, we show that the genetic structure of the human gut microbiome provides an opportunity to measure recent recombination events from sequenced fecal samples, enabling quantitative comparisons across diverse commensal species that inhabit a common environment. By analyzing recent recombination events in the core genomes of 29 human gut bacteria, we observed widespread heterogeneities in the rates and lengths of transferred fragments, which are difficult to explain by existing models of ecological isolation or homology-dependent recombination rates. We also show that natural selection helps facilitate the spread of genetic variants across strain backgrounds, both within individual hosts and across the broader population. These results shed light on the dynamics of in situ recombination, which can strongly constrain the adaptability of gut microbial communities.

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Detecting patterns of accessory genome coevolution in Staphylococcus aureus using data from thousands of genomes

Cited by 7 publications

References 41 publications

Global genetic diversity and Asian clades evolution: a phylogeographic study of Staphylococcus aureus sequence type 5

Global genetic diversity and Asian clades evolution: a phylogeographic study of Staphylococcus aureus sequence type 5

Evolutionary dynamics of the accessory genomes of Staphylococcus aureus

Dynamics of bacterial recombination in the human gut microbiome

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