Bacterial droplet-based single-cell RNA-seq reveals antibiotic-associated heterogeneous cellular states

Ma, Peijun; Amemiya, Haley M.; He, Lorrie L; Gandhi, Shivam J.; Nicol, Robert; Bhattacharyya, Roby P.; Smillie, Christopher S.; Hung, Deborah T.

doi:10.1016/j.cell.2023.01.002

Cited by 62 publications

(46 citation statements)

References 53 publications

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“…", and/or "To what extent do pleiotropic and epistatic interactions among genes underpin multidimensional changes in the niche?". While agglomerative strategies such as bulk physiological measurements (e.g., carbon flux in soil cores) or meta-genomes/metatranscriptomes of whole soils do not allow fine enough resolution to address these types of questions, the advent of new microfluidic sequencing and culturing technologies [37][38][39] could provide the fine-tuned resolution necessary to study the genetics and physiology of not just populations but the actual individual microbes that make up those populations. Additionally, some abiotic dimensions, such as oxygen availability, can vary at microhabitat levels and change dramatically along a single granule of soil 40,41 .…”

Section: Discussionmentioning

confidence: 99%

“…In particular, we advocate for studies asking: “Do multidimensional generalists have more genetic diversity in their populations allowing them to occupy greater multidimensional niche space?”, “Can specialization on one axis restrict the environmental conditions a taxon is exposed to thereby leading to specialization across additional axes through adaptation to those restricted conditions?”, and/or “To what extent do pleiotropic and epistatic interactions among genes underpin multidimensional changes in the niche?”. While agglomerative strategies such as bulk physiological measurements (e.g., carbon flux in soil cores) or meta-genomes/meta-transcriptomes of whole soils do not allow fine enough resolution to address these types of questions, the advent of new microfluidic sequencing and culturing technologies 37–39 could provide the fine-tuned resolution necessary to study the genetics and physiology of not just populations but the actual individual microbes that make up those populations. Additionally, some abiotic dimensions, such as oxygen availability, can vary at microhabitat levels and change dramatically along a single granule of soil 40, 41 .…”

Section: Discussionmentioning

confidence: 99%

See 1 more Smart Citation

Multidimensional specialization and generalization are pervasive in soil prokaryotes with generalists dominating communities and specialists more central in networks

Hernández

Kiesewetter

Almeida

et al. 2023

Preprint

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Habitat specialization underpins biological processes from species distributions to speciation. However, organisms are often described as specialists or generalists based on a single niche axis, despite facing complex, multidimensional environments. Here, we analyzed 236 prokaryotic communities across the United States demonstrating for the first time that 90% of >1,200 prokaryotes followed one of two trajectories: specialization on all niche axes (multidimensional specialization) or generalization on all axes (multidimensional generalization). We then documented that this pervasive multidimensional specialization/generalization had a wide range of ecological and evolutionary consequences. First, multidimensional specialization and generalization are highly conserved with very few transitions between these two trajectories. Second, multidimensional generalists dominated communities because they were 73 times more abundant than specialists. Lastly, multidimensional specialists played important roles in community structure with ~220% more connections in microbiome networks. These results indicate that multidimensional generalization and specialization are evolutionarily stable with multidimensional generalists supporting larger populations and multidimensional specialists playing important roles within communities likely stemming from their overrepresentation among pollutant detoxifiers and nutrient cyclers. Taken together, we demonstrate that the vast majority of soil prokaryotes are restricted to one of two multidimensional niche trajectories, multidimensional specialization or multidimensional generalization, which then has far-reaching consequences for evolutionary transitions, microbial dominance, and community roles.

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Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Multidimensional specialization and generalization are pervasive in soil prokaryotes with generalists dominating communities and specialists more central in networks

Hernández

Kiesewetter

Almeida

et al. 2023

Preprint

View full text Add to dashboard Cite

show abstract

“…This work represents only an initial effort in this direction, but provides a foundational framework for genome-wide exploration of novel bacterial regulatory phenomena. As bacterial scRNA-seq methods evolve in scale, capture efficiency, and cost [61][62][63][64] , we predict that these methods, in combination with microscopy and molecular genetics approaches that allow mechanistic dissection of these phenomena, will illuminate a diverse ecosystem of dynamic transcriptional processes.…”

Section: Discussionmentioning

confidence: 99%

Transcription-replication interactions reveal principles of bacterial genome regulation

Pountain

Jiang

Yao

et al. 2022

Preprint

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Regulation of gene activity during the cell cycle is fundamental to bacterial replication but is challenging to study in unperturbed, asynchronous bacterial populations. Using single cell RNA-sequencing of heterogeneousStaphylococcus aureuspopulations, we uncovered a global gene expression pattern dominated by chromosomal position. We show that this pattern results from the effect of DNA replication on gene expression, and inEscherichia coli, changes under different growth rates and modes of replication. By constructing a quantitative model in each species that links replication to cell cycle gene expression, we identified divergent genes that may be instead subject to distinct regulation, and applied this cell cycle framework to characterize heterogeneity in responses to antibiotic stress. Our approach reveals a highly dynamic cell cycle transcriptional landscape and may be broadly applicable across species.

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“…Recent advancement in fluorescence in situ hybridization (FISH) on living bacteria enables validation of bacterial viability and taxonomic rank at the species level, although at much lower throughput compared to NGS [ 87 ]. Emerging bacterial single-cell transcriptomics such as PETRI-seq [ 88 ], microSPLiT [ 89 ], MATQ-seq [ 90 ] and BacDrop [ 91 ] are powerful tools that outperform 16S rDNA-based microbiota profiling and provide inferred viability and functionality derived from transcriptomes. The drawbacks are also evident: high cost and computationally demanding.…”

Section: Controversies and Counterclaimsmentioning

confidence: 99%

The Blood Microbiome and Health: Current Evidence, Controversies, and Challenges

Cheng

Tan

Wong

et al. 2023

IJMS

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Blood is conventionally thought to be sterile. However, emerging evidence on the blood microbiome has started to challenge this notion. Recent reports have revealed the presence of genetic materials of microbes or pathogens in the blood circulation, leading to the conceptualization of a blood microbiome that is vital for physical wellbeing. Dysbiosis of the blood microbial profile has been implicated in a wide range of health conditions. Our review aims to consolidate recent findings about the blood microbiome in human health and to highlight the existing controversies, prospects, and challenges around this topic. Current evidence does not seem to support the presence of a core healthy blood microbiome. Common microbial taxa have been identified in some diseases, for instance, Legionella and Devosia in kidney impairment, Bacteroides in cirrhosis, Escherichia/Shigella and Staphylococcus in inflammatory diseases, and Janthinobacterium in mood disorders. While the presence of culturable blood microbes remains debatable, their genetic materials in the blood could potentially be exploited to improve precision medicine for cancers, pregnancy-related complications, and asthma by augmenting patient stratification. Key controversies in blood microbiome research are the susceptibility of low-biomass samples to exogenous contamination and undetermined microbial viability from NGS-based microbial profiling, however, ongoing initiatives are attempting to mitigate these issues. We also envisage future blood microbiome research to adopt more robust and standardized approaches, to delve into the origins of these multibiome genetic materials and to focus on host–microbe interactions through the elaboration of causative and mechanistic relationships with the aid of more accurate and powerful analytical tools.

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Bacterial droplet-based single-cell RNA-seq reveals antibiotic-associated heterogeneous cellular states

Cited by 62 publications

References 53 publications

Multidimensional specialization and generalization are pervasive in soil prokaryotes with generalists dominating communities and specialists more central in networks

Multidimensional specialization and generalization are pervasive in soil prokaryotes with generalists dominating communities and specialists more central in networks

Transcription-replication interactions reveal principles of bacterial genome regulation

The Blood Microbiome and Health: Current Evidence, Controversies, and Challenges

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