Cross-sectional study of the association of social relationship resources with Staphylococcus aureus colonization in naturally occurring social groups along the US/Mexico border

Barger, Steven D.; Lininger, Monica R.; Trotter, Robert T.; Mbegbu, Mimi; Kyman, Shari; Tucker-Morgan, Kara; Wood, Colin; Coyne, Briana; Russakoff, Benjamin; Ceniceros, Kathya; Padilla, Cristina Rodríguez; Maltinsky, Sara; Pearson, Talima

doi:10.1371/journal.pone.0284400

Cited by 3 publications

(1 citation statement)

References 55 publications

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“…We used samples from an ongoing research project designed to better understand community carriage and transmission among social groups in a population on the United States/Mexico border [25][26][27][28][29]. These samples were part of Project 1116783 that was approved by the Northern Arizona University Institutional Review Board.…”

Section: Empirical Example Of Population Sequencing Of S Aureus To De...mentioning

confidence: 99%

Population sequencing for diversity and transmission analyses

Pearson,

Furstenau,

Wood

et al. 2024

Preprint

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Genomic diversity in a pathogen population is the foundation for evolution and adaptations in virulence, drug resistance, pathogenesis, and immune evasion. Characterizing, analyzing, and understanding population-level diversity is also essential for epidemiological and forensic tracking of sources and revealing detailed pathways of transmission and spread. For bacteria, culturing, isolating, and sequencing the large number of individual colonies required to adequately sample diversity can be prohibitively time-consuming and expensive. While sequencing directly from a mixed population will show variants among reads, they cannot be linked to reveal allele combinations associated with particular traits or phylogenetic inheritance patterns. Here, we describe the theory and method of how population sequencing directly from a mixed sample can be used in conjunction with sequencing a very small number of colonies to describe the phylogenetic diversity of a population without haplotype reconstruction. To demonstrate the utility of population sequencing in capturing phylogenetic diversity, we compared isogenic clones to population sequences ofBurkholderia pseudomalleifrom the sputum of a single patient. We also analyzed population sequences ofStaphylococcus aureusderived from different people and different body sites. Sequencing results confirm our ability to capture and characterize phylogenetic diversity in our samples. Our analyses ofB. pseudomalleipopulations led to the surprising discovery that the pathogen population is highly structured in sputum, suggesting that for some pathogens, sputum sampling may preserve structuring in the lungs and thus present a non-invasive alternative to understanding colonization, movement, and pathogen/host interactions. Our analyses ofS. aureussamples show how comparing phylogenetic diversity across populations can reveal directionality of transmission between hosts and across body sites, demonstrating the power and utility for characterizing the spread of disease and identification of reservoirs at the finest levels. We anticipate that population sequencing and analysis can be broadly applied to accelerate research in a broad range of fields reliant on a foundational understanding of population diversity.Author SummaryThe ability to characterize diversity in a single bacterial population (i.e., a single host or even a single body site) is critical for understanding adaptation and evolution, with far-reaching implications on disease treatment and prevention that include revealing patterns of spread and persistence. While the scientific community has made great strides in sequencing methods to characterize single colonies and entire communities, there is a dearth of studies at the population level. This is because 1) the need to culture and sequence a sufficiently representative number of isogenic colonies is prohibitive, and 2) the theoretical foundation for characterizing a population by sequencing a single sample (as is done for microbiome and metagenomic analyses) has not been developed. Here, we introduce this theoretical foundation and validate its applicability by characterizing a lung infection caused byBurkholderia pseudomallei. We also demonstrate the utility of this method in determining the directionality of spread ofStaphylococcus aureusbetween people and across body sites within the same host (a level of spatial resolution that has not been previously performed). We anticipate that this work will open the door to a host of new studies and discoveries across a diverse set of microbiological fields.

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Section: Empirical Example Of Population Sequencing Of S Aureus To De...mentioning

confidence: 99%

Population sequencing for diversity and transmission analyses

Pearson,

Furstenau,

Wood

et al. 2024

Preprint

Self Cite

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Staphylococcus aureus infection disparities among Hispanics and non-Hispanics in Yuma, Arizona

Pearson,

Kramer,

Panisello Yagüe

et al. 2024

ASHE

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High-throughput targeted amplicon screening tool for characterizing intrahost diversity inStaphylococcus aureusdirectly from sample

Furstenau,

Whealy,

Timm

et al. 2024

Preprint

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A significant proportion of people are asymptomatic carriers of Staphylococcus aureus (SA), an important risk factor for development of opportunistic infections. SA colonization is dynamic, appearing and disappearing, with strains evolving and potentially shifting in composition over time and between body sites. These changes make detection challenging and the numerous potential sources of reintroduction from other people and even other body site reservoirs preclude efficient efforts to prevent transmission and spread. Identifying typical sources is therefore critical for mitigation. Whole-genome sequencing (WGS), ideally of multiple colonies from multiple body sites, is the gold standard for characterizing SA strains and confirming transmission. However, this is often too resource-intensive for initial assessments of transmission and not feasible for large-scale studies involving various body sites from multiple individuals over time. To address these challenges, we developed a low-cost, custom, species-specific amplicon sequencing (AmpSeq) assay, optimized to provide high resolution discrimination of SA genotypes directly from samples. We tested this approach on a subset of samples that were a part of a large-scale longitudinal study of SA carriage. Oral and nasal samples were collected from 9 participants every two weeks for up to 18 weeks and qPCR positive samples were analyzed using our AmpSeq assay directly from the sample without culturing. The longitudinal sampling strategy enabled us to characterize changes in SA colonization patterns over time, detect potential strain mixtures, and identify rare variants that may serve as signatures of transmission between different body sites or among individuals. Without using WGS, we were able to rapidly eliminate the possibility of transmission between sampled residents. Participants that had positive oral and nasal samples had no fixed SNP differences between the two body sites, suggesting likely within-person spread. In these cases, we were able to infer the most likely direction of spread (nasal to oral sites) by analyzing segregating rare variants. While WGS can be used to provide higher resolution to colonization patterns and validate these findings, our amplicon sequencing approach offers a rapid, cost-effective, direct-from-sample method for species-specific screening intended for population-level characterization that allows researchers to characterize strain types, identify or eliminate likely transmission cases, and identify potential reservoirs before resorting to more expensive WGS methods.

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Cross-sectional study of the association of social relationship resources with Staphylococcus aureus colonization in naturally occurring social groups along the US/Mexico border

Cited by 3 publications

References 55 publications

Population sequencing for diversity and transmission analyses

Population sequencing for diversity and transmission analyses

Staphylococcus aureus infection disparities among Hispanics and non-Hispanics in Yuma, Arizona

High-throughput targeted amplicon screening tool for characterizing intrahost diversity inStaphylococcus aureusdirectly from sample

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