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Swafford, A. D.

Publications and source records attributed to Swafford, A. D..

9 recordsLinked to original sources

Reply to: Caution Regarding the Specificities of Pan-Cancer Microbial Structure

The cancer microbiome field tremendously accelerated following the release of our manuscript nearly three years ago1, including direct validation of our cancer type-specific conclusions in independent, international cohorts2,3 and the tumor microbiomes adoption into the hallmarks of cancer4. Disentangling contamination signals from biological signals is an important consideration for this research field. Therefore, despite numerous, high-impact, peer-reviewed research papers that either validated our conclusions or extended them using data we released2,5-13, we carefully considered criticism raised by Gihawi et al. about potential mishandling of contaminants, batch effects, and machine learning approaches--all of which were central topics in our manuscript. Nonetheless, a close examination of each concern alongside the original manuscript and re-analyses of our published data strongly demonstrates the robustness of the original findings. To remove all doubt, however, we have reproduced all key conclusions from the original manuscript using only overlapping bacterial genera identified in a highly decontaminated, multi-cancer, international cohort (Weizmann Institute of Science, WIS)2, with or without batch correction, and with multiclass machine learning analyses to mitigate class imbalances. Our published pan-cancer mycobiome manuscript3 also affirms these findings using updated, state-of-the-art methods. We also note that every analysis shown here was possible using public data and code that we had already provided.

bioinformatics↗

A comparison of six DNA extraction protocols for 16S, ITS, and shotgun metagenomic sequencing of microbial communities

Microbial communities contain a broad phylogenetic diversity of organisms, however the majority of methods center on describing bacteria and archaea. Fungi are important symbionts in many ecosystems, and are potentially important members of the human microbiome, beyond those that can cause disease. To expand our analysis of microbial communities to include fungal ITS data, we compared five candidate DNA extraction kits against our standardized protocol for describing bacteria and archaea using 16S rRNA gene amplicon- and shotgun metagenomics sequencing. We present results considering a diverse panel of host-associated and environmental sample types, and comparing the cost, processing time, well-to-well contamination, DNA yield, limit of detection, and microbial community composition among protocols. Across all criteria, we found the MagMAX Microbiome kit to perform best. The PowerSoil Pro kit performed comparably, but with increased cost per sample and overall processing time. The Zymo MagBead, NucleoMag Food, and Norgen Stool kits were included. Accession numbersRaw sequence data were deposited at the European Nucleotide Archive (accession#: ERP124610) and raw and processed data are available at Qiita (Study ID: 12201). All processing and analysis code is available on GitHub (github.com/justinshaffer/Extraction_kit_testing). Methods summaryTo allow for downstream applications involving fungi in addition to bacteria and archaea, we compared five DNA extraction kits with our previously established, standardized protocol for extracting DNA for microbial community analysis. Across ten diverse sample types, we found one extraction kit to perform comparably or better than our standardized protocol. Our conclusion is based on per-sample comparisons of DNA yield, the number of quality-filtered sequences generated, the limit of detection of microbial cells, microbial community alpha-diversity, beta-diversity, and taxonomic composition, and extent of well-to-well contamination.

microbiology↗

OGUs enable effective, phylogeny-aware analysis of even shallow metagenome community structures

We introduce Operational Genomic Unit (OGU), a metagenome analysis strategy that directly exploits sequence alignment hits to individual reference genomes as the minimum unit for assessing the diversity of microbial communities and their relevance to environmental factors. This approach is independent from taxonomic classification, granting the possibility of maximal resolution of community composition, and organizes features into an accurate hierarchy using a phylogenomic tree. The outputs are suitable for contemporary analytical protocols for community ecology, differential abundance and supervised learning while supporting phylogenetic methods, such as UniFrac and phylofactorization, that are seldomly applied to shotgun metagenomics despite being prevalent in 16S rRNA gene amplicon studies. As demonstrated in one synthetic and two real-world case studies, the OGU method produces biologically meaningful patterns from microbiome datasets. Such patterns further remain detectable at very low metagenomic sequencing depths. Compared with taxonomic unit-based analyses implemented in currently adopted metagenomics tools, and the analysis of 16S rRNA gene amplicon sequence variants, this method shows superiority in informing biologically relevant insights, including stronger correlation with body environment and host sex on the Human Microbiome Project dataset, and more accurate prediction of human age by the gut microbiomes in the Finnish population. We provide Woltka, a bioinformatics tool to implement this method, with full integration with the QIIME 2 package and the Qiita web platform, to facilitate OGU adoption in future metagenomics studies. ImportanceShotgun metagenomics is a powerful, yet computationally challenging, technique compared to 16S rRNA gene amplicon sequencing for decoding the composition and structure of microbial communities. However, current analyses of metagenomic data are primarily based on taxonomic classification, which is limited in feature resolution compared to 16S rRNA amplicon sequence variant analysis. To solve these challenges, we introduce Operational Genomic Units (OGUs), which are the individual reference genomes derived from sequence alignment results, without further assigning them taxonomy. The OGU method advances current read-based metagenomics in two dimensions: (i) providing maximal resolution of community composition while (ii) permitting use of phylogeny-aware tools. Our analysis of real-world datasets shows several advantages over currently adopted metagenomic analysis methods and the finest-grained 16S rRNA analysis methods in predicting biological traits. We thus propose the adoption of OGU as standard practice in metagenomic studies.

bioinformatics↗

A comparison of DNA/RNA extraction protocols for high-throughput sequencing of microbial communities

One goal among microbial ecology researchers is to capture the maximum amount of information from all organisms in a sample. The recent COVID-19 pandemic, caused by the RNA virus SARS-CoV-2, has highlighted a gap in traditional DNA-based protocols, including the high-throughput methods we previously established as field standards. To enable simultaneous SARS-CoV-2 and microbial community profiling, we compare the relative performance of two total nucleic acid extraction protocols and our previously benchmarked protocol. We included a diverse panel of environmental and host-associated sample types, including body sites commonly swabbed for COVID-19 testing. Here we present results comparing the cost, processing time, DNA and RNA yield, microbial community composition, limit of detection, and well-to-well contamination, between these protocols. Accession numbersRaw sequence data were deposited at the European Nucleotide Archive (accession#: ERP124610) and raw and processed data are available at Qiita (Study ID: 12201). All processing and analysis code is available on GitHub (github.com/justinshaffer/Extraction_test_MagMAX). Methods summaryTo allow for downstream applications involving RNA-based organisms such as SARS-CoV-2, we compared the two extraction protocols designed to extract DNA and RNA against our previously established protocol for extracting only DNA for microbial community analyses. Across 10 diverse sample types, one of the two protocols was equivalent or better than our established DNA-based protocol. Our conclusion is based on per-sample comparisons of DNA and RNA yield, the number of quality sequences generated, microbial community alpha- and beta-diversity and taxonomic composition, the limit of detection, and extent of well-to-well contamination.

ecology↗

EMPress enables tree-guided, interactive, and exploratory analyses of multi-omic datasets

Standard workflows for analyzing microbiomes often include the creation and curation of phylogenetic trees. Here we present EMPress, an interactive tool for visualizing trees in the context of microbiome, metabolome, etc. community data scalable beyond modern large datasets like the Earth Microbiome Project. EMPress provides novel functionality--including ordination integration and animations--alongside many standard tree visualization features, and thus simplifies exploratory analyses of many forms of omic data.

bioinformatics↗

Bacterial modification of the host glycosaminoglycan heparan sulfate modulates SARS-CoV-2 infectivity

The human microbiota has a close relationship with human disease and it remodels components of the glycocalyx including heparan sulfate (HS). Studies of the severe acute respiratory syndrome coronavirus (SARS-CoV-2) spike protein receptor binding domain suggest that infection requires binding to HS and angiotensin converting enzyme 2 (ACE2) in a codependent manner. Here, we show that commensal host bacterial communities can modify HS and thereby modulate SARS-CoV-2 spike protein binding and that these communities change with host age and sex. Common human-associated commensal bacteria whose genomes encode HS-modifying enzymes were identified. The prevalence of these bacteria and the expression of key microbial glycosidases in bronchoalveolar lavage fluid (BALF) was lower in adult COVID-19 patients than in healthy controls. The presence of HS-modifying bacteria decreased with age in two large survey datasets, FINRISK 2002 and American Gut, revealing one possible mechanism for the observed increase in COVID-19 susceptibility with age. In vitro, bacterial glycosidases from unpurified culture media supernatants fully blocked SARS-CoV-2 spike binding to human H1299 protein lung adenocarcinoma cells. HS-modifying bacteria in human microbial communities may regulate viral adhesion, and loss of these commensals could predispose individuals to infection. Understanding the impact of shifts in microbial community composition and bacterial lyases on SARS-CoV-2 infection may lead to new therapeutics and diagnosis of susceptibility. O_FIG O_LINKSMALLFIG WIDTH=200 HEIGHT=136 SRC="FIGDIR/small/238444v1_ufig1.gif" ALT="Figure 1"> View larger version (35K): org.highwire.dtl.DTLVardef@14ff1ecorg.highwire.dtl.DTLVardef@193d84corg.highwire.dtl.DTLVardef@15d6f9eorg.highwire.dtl.DTLVardef@14b16c6_HPS_FORMAT_FIGEXP M_FIG Graphical Abstract. Diagram of hypothesis for bacterial mediation of SARS-CoV-2 infection through heparan sulfate (HS).It is well known that host microbes groom the mucosa where they reside. Recent investigations have shown that HS, a major component of mucosal layers, is necessary for SARS-CoV-2 infection. In this study we examine the impact of microbial modification of HS on viral attachment. C_FIG

microbiology↗

Metabolome-informed microbiome analysis refines metadata classifications and reveals unexpected medication transfer in captive cheetahs

Structured AbstractEven high-quality collection and reporting of study metadata in microbiome studies can lead to various forms of inadvertently missing or mischaracterized information that can alter the interpretation or outcome of the studies, especially with non-model organisms. Metabolomic profiling of fecal microbiome samples can provide empirical insight into unanticipated confounding factors that are not possible to obtain even from detailed care records. We illustrate this point using data from cheetahs from the San Diego Zoo Safari Park. The metabolomic characterization indicated that one cheetah had to be moved from the non-antibiotic-exposed to the antibiotic-exposed group. The detection of the antibiotic in this second cheetah was likely due to grooming interactions with the cheetah that was administered antibiotics. Similarly, because transit time for stool is variable, early fecal samples within the first few days of antibiotic prescription do not all contain detectable antibiotics. Therefore, the microbiome is not affected by the antibiotics at those time points. These insights significantly altered the way the samples were grouped for analysis (antibiotic vs no antibiotic), and the subsequent understanding of the effect of the antibiotics on the cheetah microbiome. Metabolomics also revealed information about numerous other medications, and provided unexpected dietary insights that in turn improved our understanding of the molecular patterns on the impact on the community microbial structure. These results suggest that untargeted metabolomics data provide empirical evidence to correct records of non-model organisms in captivity, although we also expect these methods will be appropriate for experimental conditions typical in human studies.\n\nImportanceMetabolome-informed analyses can enhance omics studies by enabling the correct partitioning of samples by identifying hidden confounders inadvertently misrepresented or omitted from carefully curated metadata. We demonstrate the utility of metabolomics in a study characterizing the microbiome associated with liver disease in cheetahs. Metabolome-informed reinterpretation of metagenome and metabolome profiles factored in an unexpected transfer of antibiotics preventing misinterpretation of the data. Our work suggests that untargeted metabolomics can be used to verify, augment, and correct sample metadata to support improved grouping of sample data for microbiome analyses, here for non-model organisms in captivity. However, the techniques also suggest a path forward for correcting clinical information in human studies to enable higher-precision analyses.

systems biology↗

MASST: A Web-based Basic Mass Spectrometry Search Tool for Molecules to Search Public Data.

CorrespondenceWe introduce a web-enabled small-molecule mass spectrometry (MS) search engine. To date, no tool can query all the public small-molecule tandem MS data in metabolomics repositories, greatly limiting the utility of these resources in clinical, environmental and natural product applications. Therefore, we introduce a Mass Spectrometry Search Tool (MASST) (https://proteosafe-extensions.ucsd.edu/masst/), that enables the discovery of molecular relationships among accessible public metabolomics and natural product tandem mass spectrometry data (MS/MS).

bioinformatics↗

Age and sex-dependent patterns of gut microbial diversity in human adults

Gut microbial diversity changes throughout the human lifespan and is known to be affected by host sex. We investigated the association of age, sex and gut bacterial alpha diversity in three large cohorts of adults from four geographical regions: US and UK cohorts in the American Gut Project, and two independent cohorts of Colombians and Chinese. In three of the four cohorts, we observed a strong positive association between age and alpha diversity in young adults that plateaued after age 40. We also found pronounced sex-dependent differences in younger but not middle-aged adults, and women had higher alpha diversity than men. In contrast, no association of alpha diversity with age or sex was observed in the Chinese cohort. These associations were maintained after adjusting for cardiometabolic parameters in the Colombian cohort and antibiotic usage in the AGP cohort, suggesting that these factors do not affect the association of alpha diversity with age and sex. We also used a machine learning approach to predict individual age based on the gut microbiome. Consistent with our alpha diversity-based findings, women had significantly higher predicted age than men in the US and UK cohort, with a reduced difference above age 40. This was not observed in the Colombian cohort and only in the group of middle-age adults in the Chinese cohort. Together, our results provide new insights into the influence of age and sex on biodiversity of the human gut microbiota during adulthood while highlighting similarities and differences across diverse cohorts.

microbiology↗