Roles of bacteriophages, plasmids and CRISPR immunity in microbial community dynamics revealed using time-series integrated meta-omics

Arbas, Susana Martínez; Narayanasamy, Shaman; Herold, Malte; Lebrun, Laura; Hoopmann, Michael R.; Li, Sujun; Lam, Tony J.; Kunath, Benoît J.; Hicks, Nathan D.; Liu, Cindy M.; Price, Lance B.; Laczny, Cédric Christian; Gillece, John D.; Schupp, James M.; Keim, Paul; Moritz, Robert L.; Faust, Karoline; Tang, Haixu; Ye, Yuzhen; Skupin, Alexander; May, Patrick; Muller, Emilie; Wilmes, Paul

doi:10.1038/s41564-020-00794-8

Cited by 51 publications

(53 citation statements)

References 90 publications

(88 reference statements)

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“…We hypothesize that phage predation may contribute to the maintenance of low levels of strain diversity in the analyzed cheese starter culture, similar as suggested for mesophilic cheese starter cultures 11 . We can infer such interactions from genomic data, as bacteria store a memory of past phage encounters in their genome by integrating short spacer sequences into CRISPR arrays 28 . We found three previously described CRISPR-regions (CR) in the analyzed Streptococcus genomes, namely CR1 (type IIA), CR2 (type IIIA) and CR3…”

Section: Highly Variable Phage Resistance Mechanisms In Isolated Genomesmentioning

confidence: 99%

Functional strain redundancy and persistent phage infection in Swiss hard cheese starter cultures

Somerville

Berthoud

Schmidt

et al. 2021

Preprint

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Undefined starter cultures are poorly characterized bacterial communities from environmental origin used in cheese making. They are phenotypically stable and have evolved through domestication by repeated propagation in closed and highly controlled environments over centuries. This makes them interesting for understanding eco-evolutionary dynamics governing microbial communities. While cheese starter cultures are known to be dominated by a few bacterial species, little is known about the composition, functional relevance, and temporal dynamics of strain-level diversity. Here, we applied shotgun metagenomics to an important Swiss cheese starter culture and analyzed historical and experimental samples reflecting 82 years of starter culture propagation. We found that the bacterial community is highly stable and dominated by only a few coexisting strains of Streptococcus thermophilus and Lactobacillus delbrueckii subsp. lactis. Genome sequencing, metabolomics analysis, and co-culturing experiments of 43 isolates show that these strains are functionally redundant, but differ tremendously in their phage resistance potential. Moreover, we identified two highly abundant Streptococcus phages that seem to stably coexist in the community without any negative impact on bacterial growth or strain persistence, and despite the presence of a large and diverse repertoire of matching CRISPR spacers. Our findings show that functionally equivalent strains can coexist in domesticated microbial communities and highlight an important role of bacteria-phage interactions that are different from kill-the-winner dynamics.

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Section: Highly Variable Phage Resistance Mechanisms In Isolated Genomesmentioning

confidence: 99%

Functional strain redundancy and persistent phage infection in Swiss hard cheese starter cultures

Somerville

Berthoud

Schmidt

et al. 2021

Preprint

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“…Sampling frequency may be determined by the dynamics and/or generational-timescale of a given system. For instance, the human gut microbiome is known to exhibit daily fluctuations, and therefore could be sampled on a daily basis within a given temporal study ( David et al, 2014 ), while activated sludge systems are known to exhibit (approximately) weekly doubling periods and thus could be sampled on a weekly basis ( Herold et al, 2020 ; Martínez Arbas et al, 2021 ). Based on the recommendations of Sefer et al (2016) , if biological replicates are either not feasible (i.e., n = 1) or limited (i.e., low n ) ( Herold et al, 2020 ), one should ideally opt for higher frequency (dense) longitudinal sampling, and less dense sampling if biological replicates were available (i.e., high n ), e.g., a cohort of patients ( Lloyd-Price et al, 2019 ).…”

Section: Multi-omic Considerations and Experimental Design For Longitudinal Studiesmentioning

confidence: 99%

“…However, various aspects must be considered when conducting longitudinal multi-omic microbiome studies, ranging from experimental design, bioinformatic processing, modeling, and validation. In this article, we explore challenges, considerations, and potential solutions for such studies, based on recent advances and reports ( Law et al, 2016 ; Lloyd-Price et al, 2019 ; Herold et al, 2020 ; Martínez Arbas et al, 2021 ), which are applicable to both microbe-centric (e.g., soil, water) or host-centric (e.g., human gut) systems. Finally, although this article focuses on specifically longitudinal multi-omic microbiome studies, the content is generally applicable to any large-scale microbiome studies.…”

Section: Introductionmentioning

confidence: 99%

Challenges, Strategies, and Perspectives for Reference-Independent Longitudinal Multi-Omic Microbiome Studies

et al. 2021

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In recent years, multi-omic studies have enabled resolving community structure and interrogating community function of microbial communities. Simultaneous generation of metagenomic, metatranscriptomic, metaproteomic, and (meta) metabolomic data is more feasible than ever before, thus enabling in-depth assessment of community structure, function, and phenotype, thus resulting in a multitude of multi-omic microbiome datasets and the development of innovative methods to integrate and interrogate those multi-omic datasets. Specifically, the application of reference-independent approaches provides opportunities in identifying novel organisms and functions. At present, most of these large-scale multi-omic datasets stem from spatial sampling (e.g., water/soil microbiomes at several depths, microbiomes in/on different parts of the human anatomy) or case-control studies (e.g., cohorts of human microbiomes). We believe that longitudinal multi-omic microbiome datasets are the logical next step in microbiome studies due to their characteristic advantages in providing a better understanding of community dynamics, including: observation of trends, inference of causality, and ultimately, prediction of community behavior. Furthermore, the acquisition of complementary host-derived omics, environmental measurements, and suitable metadata will further enhance the aforementioned advantages of longitudinal data, which will serve as the basis to resolve drivers of community structure and function to understand the biotic and abiotic factors governing communities and specific populations. Carefully setup future experiments hold great potential to further unveil ecological mechanisms to evolution, microbe-microbe interactions, or microbe-host interactions. In this article, we discuss the challenges, emerging strategies, and best-practices applicable to longitudinal microbiome studies ranging from sampling, biomolecular extraction, systematic multi-omic measurements, reference-independent data integration, modeling, and validation.

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“…2c), were relatively abundant in nearly all samples that contained Absconditabacteria. Members of the Chitinophagales, Pseudomonadales, and Acidimicrobiales were detected in high abundance in three wastewater samples from similar treatment plants (40) and one dairy pond sample containing Absconditabacteria. No clear patterns of co-occurrence were observed for Gracilibacteria, with the potential exception of Campylobacterales, which co-occurred in 8 of 10 groundwater samples where Gracilibacteria were found (Fig.…”

Section: Resultsmentioning

confidence: 99%

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

Jaffe¹,

Keren³

et al. 2021

Preprint

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Bacteria from the Candidate Phyla Radiation (CPR) 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 combining phylogeny and habitat information, we show that bacteria from these three lineages have undergone multiple transitions from environmental habitats into animal microbiomes. Using computational co-occurrence analyses based on 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 Saccharibacteria from animal-associated microbiomes have, on average, 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 bacteriorhodopsin. For protein families that exhibited the clearest patterns of differential habitat distribution, we compared protein and species phylogenies to estimate the incidence of lateral gene transfer and genomic loss that occurred 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.

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Roles of bacteriophages, plasmids and CRISPR immunity in microbial community dynamics revealed using time-series integrated meta-omics

Cited by 51 publications

References 90 publications

Functional strain redundancy and persistent phage infection in Swiss hard cheese starter cultures

Functional strain redundancy and persistent phage infection in Swiss hard cheese starter cultures

Challenges, Strategies, and Perspectives for Reference-Independent Longitudinal Multi-Omic Microbiome Studies

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

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