Coordination of cohabiting phage elements supports bacteria–phage cooperation

Argov, Tal; Sapir, Shai Ran; Pasechnek, Anna; Azulay, Gil; Stadnyuk, Olga; Rabinovich, Lev; Sigal, Nadejda; Borovok, Ilya; Herskovits, Anat A.

doi:10.1038/s41467-019-13296-x

Cited by 49 publications

(62 citation statements)

References 52 publications

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“…However, the comK prophage is absent from the L. monocytogenes 6179 genome. It is tempting to speculate that the simultaneous induction of the three L. monocytogenes 6179 prophages and the lma locus may be coordinated in a similar mechanism suggested by Argov et al 2019 [57] in response to Psychrobacter L7. Therefore, the global induction of L. monocytogenes 6179 prophage genes observed in this study suggests a possible benefit during exposure to stresses that co-cultivation conditions may elicit; however, further experiments are required to verify this hypothesis.…”

Section: Gene Expression Results Unique To Each Co-culture Condition mentioning

confidence: 72%

“…Recently, Argov et al 2019 [57] discovered that the lma prophage controls the induction of the lytic comK prophage in L. monocytogenes 10403S, thus synchronizing their lysis modules. Argov et al 2019 [57] further suggest that the co-induction of the active lytic phage and the monocin may enhance bacterial fitness under stress. Additionally, bacteriocins are known to provide a competitive advantage by killing neighboring cells.…”

Section: Gene Expression Results Unique To Each Co-culture Condition mentioning

confidence: 99%

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The transcriptome of Listeria monocytogenes during co-cultivation with cheese rind bacteria suggests adaptation by induction of ethanolamine and 1,2-propanediol catabolism pathway genes

Anast

Schmitz‐Esser

2020

PLoS ONE

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The survival of Listeria (L.) monocytogenes in foods and food production environments (FPE) is dependent on several genes that increase tolerance to stressors; this includes competing with intrinsic bacteria. We aimed to uncover genes that are differentially expressed (DE) in L. monocytogenes sequence type (ST) 121 strain 6179 when co-cultured with cheese rind bacteria. L. monocytogenes was cultivated in broth or on plates with either a Psychrobacter or Brevibacterium isolate from cheese rinds. RNA was extracted from cocultures in broth after two or 12 hours and from plates after 24 and 72 hours. Broth co-cultivations with Brevibacterium or Psychrobacter yielded up to 392 and 601 DE genes, while plate co-cultivations significantly affected the expression of up to 190 and 485 L. monocytogenes genes, respectively. Notably, the transcription of virulence genes encoding the Listeria adhesion protein and Listeriolysin O were induced during plate and broth cocultivations. The expression of several systems under the control of the global stress gene regulator, σ B , increased during co-cultivation. A cobalamin-dependent gene cluster, responsible for the catabolism of ethanolamine and 1,2-propanediol, was upregulated in both broth and plate co-cultures conditions. Finally, a small non-coding (nc)RNA, Rli47, was induced after 72 hours of co-cultivation on plates and accounted for 50-90% of the total reads mapped to L. monocytogenes. A recent study has shown that Rli47 may contribute to L. monocytogenes stress survival by slowing growth during stress conditions through the suppression of branch-chained amino acid biosynthesis. We hypothesize that Rli47 may have an impactful role in the response of L. monocytogenes to co-cultivation by regulating a complex network of metabolic and virulence mechanisms.

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Section: Gene Expression Results Unique To Each Co-culture Condition mentioning

confidence: 72%

Section: Gene Expression Results Unique To Each Co-culture Condition mentioning

confidence: 99%

The transcriptome of Listeria monocytogenes during co-cultivation with cheese rind bacteria suggests adaptation by induction of ethanolamine and 1,2-propanediol catabolism pathway genes

Anast

Schmitz‐Esser

2020

PLoS ONE

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“…RepA-family proteins mediate replication of plasmids by interacting with host DnaG primases [62], suggesting that the RepA-like protein coopts the host primase during replication, triggering the loss of the phage-encoded dnaG in this lineage. Consistent with a RepA-mediated episomal replication strategy, no integrase is identi able in the genomes on this branch yet the phages encode numerous antirepressors, proteins involved in the lysis-lysogeny decision of temperate phages [63,64]. The rest of the Quimby-like phages harbor a full-length integrase, indicating that these phages integrate into their host cell genome (Fig.…”

Section: Selection Of Candidate Families For Comparative Genomicsmentioning

confidence: 88%

Thousands of Previously Unknown Phages Discovered in Whole-community Human Gut Metagenomes

Benler

Yutin

Antipov

et al. 2020

Preprint

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Background: Double-stranded DNA bacteriophages (dsDNA phages) play pivotal roles in structuring human gut microbiomes; yet, the gut phageome is far from being fully characterized, and additional groups of phages, including highly abundant ones, continue to be discovered by metagenome mining. A multilevel framework for taxonomic classification of viruses was recently adopted, facilitating the classification of phages into evolutionary informative taxonomic units based on hallmark genes. Together with advanced approaches for sequence assembly and powerful methods of sequence analysis, this revised framework offers the opportunity to discover and classify unknown phage taxa in the human gut.Results:A search of human gut metagenomes for circular contigs encoding phage hallmark genes resulted in the identification of 3,738 apparently complete phage genomes that represent 451 putative genera. Several of these phage genera are only distantly related to previously identified phages and are likely to found new families. Two of the candidate families, “Flandersviridae” and “Quimbyviridae”, include some of the most common and abundant members of the human gut virome that infect Bacteroides, Parabacteroides and Prevotella. The third proposed family, “Gratiaviridae”, consists of less abundant phages that are distantly related to the families Autographiviridae, Drexlerviridae and Chaseviridae. Analysis of CRISPR spacers indicates that phages of all three putative families infect bacteria of the phylum Bacteroidetes. Comparative genomic analysis of the three candidate phage families revealed features without precedent in phage genomes. Some “Quimbyviridae” phages possess Diversity-Generating Retroelements (DGRs) that generate hypervariable target genes nested within defense-related genes, whereas the previously known targets of phage-encoded DGRs are structural genes. Several “Flandersviridae” phages encode enzymes of the isoprenoid pathway, a lipid biosynthesis pathway that so far has not been known to be manipulated by phages. The “Gratiaviridae” phages encode a HipA-family protein kinase and glycosyltransferase, suggesting these phages modify the host cell wall, preventing superinfection by other phages. Hundreds of phages in these three and other families are shown to encode catalases and iron-sequestering enzymes that can be predicted to enhance cellular tolerance to reactive oxygen species.Conclusions:Analysis of phage genomes identified in whole-community human gut metagenomes resulted in the delineation of at least three new candidate families of Caudovirales and revealed diverse putative mechanisms underlying phage-host interactions in the human gut. Addition of these phylogenetically classified, diverse and distinct phages to public databases will facilitate taxonomic decomposition and functional characterization of human gut viromes.

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“…In many mastitis-causing microbiomes, BarA/UvrY is important for regulation and coordination of pathogenicity and group behaviors 51,64 . The relative overrepresentation of filamentous phage-related genes in mastitis-pathogens may suggest that bacteriophages participate in the horizontal gene transfer among the members of bovine milk microbiome and eventually to mammary gland pathogens 65 .…”

Section: Discussionmentioning

confidence: 99%

Microbiome Dynamics of Bovine Mastitis Progression and Genomic Determinants

Hoque

Istiaq

Rahman

et al. 2020

Preprint

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The milk of lactating cows presents a complex ecosystem of interconnected microbial communities which can impose a significant influence on the pathophysiology of mastitis. Previously, we reported the alteration of microbiome (bacteria, archaea, virus) composition between clinical mastitis (CM) and healthy (H) milk. We hypothesized possible dynamic shifts of microbiome compositions with the progress of different pathological states of mastitis (CM, Recurrent CM; RCM, Subclinical Mastitis; SCM) determined by its favoring genomic potentials. To evaluate this hypothesis, we employed whole metagenome sequencing (WMS) in 20 milk samples (CM = 5, RCM = 6, SCM = 4, H = 5) to unravel the microbiome dynamics, interrelation, and relevant metabolic functions. PathoScope (PS) and MG-RAST (MR) analyses mapped the WMS data to 442 bacterial, 58 archaeal and 48 viral genomes with distinct variation in microbiome composition and abundances across these metagenomes (CM>H>RCM>SCM). PS analysis identified 385, 65, 80 and 144 bacterial strains in CM, RCM, SCM, and H milk, respectively, with an inclusion of 67.19% previously unreported opportunistic strains in mastitis metagenomes. Moreover, MR detected 56, 13, 9 and 46 archaeal, and 40, 24, 11 and 37 viral genera in CM, RCM, SCM and H-milk metagenomes, respectively. The CM-microbiomes had closest association with RCM-microbiomes followed by SCM, and H-microbiomes. Furthermore, we identified 333, 304, 183 and 50 virulence factors-associated genes (VFGs), and 48, 31, 11 and 6 antibiotic resistance genes (AGRs) in CM, RCM, SCM, and H-microbiomes, respectively, showing a significant correlation between the relative abundances of VFGs (p = 0.001), ARGs (p = 0.0001), and associated bacterial taxa. We also detected correlated variations in the presence and abundance of several metabolic functional genes related to bacterial colonization, proliferation, chemotaxis, motility and invasion, oxidative stress, virulence and pathogenicity, phage integration and excision, biofilm-formation, and quorum-sensing to be associated with different episodes of mastitis. Therefore, profiling the dynamics of microbiome in different states of mastitis, concurrent VFGs, ARGs, and genomic functional correlations will contribute to developing microbiome-based diagnostics and therapeutics for bovine mastitis, and carries significant implications on curtailing the economic fallout from this disease.

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Coordination of cohabiting phage elements supports bacteria–phage cooperation

Cited by 49 publications

References 52 publications

The transcriptome of Listeria monocytogenes during co-cultivation with cheese rind bacteria suggests adaptation by induction of ethanolamine and 1,2-propanediol catabolism pathway genes

The transcriptome of Listeria monocytogenes during co-cultivation with cheese rind bacteria suggests adaptation by induction of ethanolamine and 1,2-propanediol catabolism pathway genes

Thousands of Previously Unknown Phages Discovered in Whole-community Human Gut Metagenomes

Microbiome Dynamics of Bovine Mastitis Progression and Genomic Determinants

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