Freshwater Metaviromics and Bacteriophages: A Current Assessment of the State of the Art in Relation to Bioinformatic Challenges

Bruder, Katherine; Malki, Kema; Cooper, Alexandria; Sible, Emily; Shapiro, Jason W.; Watkins, Siobhan C.; Putonti, Catherine

doi:10.4137/ebo.s38549

Cited by 22 publications

(23 citation statements)

References 88 publications

(130 reference statements)

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“…Despite these advances, phage biology is hampered by several knowledge gaps, which prevent the incorporation of phages into predictive ecosystem models or their use in biotechnological applications. First, phage-host model systems exist for few phyla and environments [6][7][8][9][10], thus severely limiting our understanding of naturally occurring phage-host interactions. Second, inefficient infections in nature are woefully understudied, despite that phages might attach to any encountered host [11], not just one where infection is efficient.…”

Section: Introductionmentioning

confidence: 99%

Multiple mechanisms drive phage infection efficiency in nearly identical hosts

et al. 2018

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Phage-host interactions are critical to ecology, evolution, and biotechnology. Central to those is infection efficiency, which remains poorly understood, particularly in nature. Here we apply genome-wide transcriptomics and proteomics to investigate infection efficiency in nature's own experiment: two nearly identical (genetically and physiologically) Bacteroidetes bacterial strains (host18 and host38) that are genetically intractable, but environmentally important, where phage infection efficiency varies. On host18, specialist phage phi18:3 infects efficiently, whereas generalist phi38:1 infects inefficiently. On host38, only phi38:1 infects, and efficiently. Overall, phi18:3 globally repressed host18's transcriptome and proteome, expressed genes that likely evaded host restriction/modification (R/M) defenses and controlled its metabolism, and synchronized phage transcription with translation. In contrast, phi38:1 failed to repress host18's transcriptome and proteome, did not evade host R/M defenses or express genes for metabolism control, did not synchronize transcripts with proteins and its protein abundances were likely targeted by host proteases. However, on host38, phi38:1 globally repressed host transcriptome and proteome, synchronized phage transcription with translation, and infected host38 efficiently. Together these findings reveal multiple infection inefficiencies. While this contrasts the single mechanisms often revealed in laboratory mutant studies, it likely better reflects the phage-host interaction dynamics that occur in nature.

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Section: Introductionmentioning

confidence: 99%

Multiple mechanisms drive phage infection efficiency in nearly identical hosts

et al. 2018

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“…High-throughput sequencing platforms have been instrumental in advancing current understanding of microbial community diversity [ 7 ]. Viral metagenomic studies of phage communities have significantly improved our ability to examine and understand viral diversity in the wild [ 8 , 9 , 10 ]. Meta-analyses have expanded the viral catalogue postulating new branches of the evolutionary tree for viruses [ 11 , 12 , 13 ].…”

Section: Introductionmentioning

confidence: 99%

Pseudomonas PB1-Like Phages: Whole Genomes from Metagenomes Offer Insight into an Abundant Group of Bacteriophages

Watkins

Sible

Putonti

2018

Viruses

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Despite the abundance, ubiquity and impact of environmental viruses, their inherent genomic plasticity and extreme diversity pose significant challenges for the examination of bacteriophages on Earth. Viral metagenomic studies have offered insight into broader aspects of phage ecology and repeatedly uncover genes to which we are currently unable to assign function. A combined effort of phage isolation and metagenomic survey of Chicago’s nearshore waters of Lake Michigan revealed the presence of Pbunaviruses, relatives of the Pseudomonas phage PB1. This prompted our expansive investigation of PB1-like phages. Genomic signatures of PB1-like phages and Pbunaviruses were identified, permitting the unambiguous distinction between the presence/absence of these phages in soils, freshwater and wastewater samples, as well as publicly available viral metagenomic datasets. This bioinformatic analysis led to the de novo assembly of nine novel PB1-like phage genomes from a metagenomic survey of samples collected from Lake Michigan. While this study finds that Pbunaviruses are abundant in various environments of Northern Illinois, genomic variation also exists to a considerable extent within individual communities.

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“…The results obtained from this study showed that phages related to P19250A, the first phage of the LD28 clade, may be abundant in diverse freshwater environments, and suggested that the characterization of the P19250A genome can lead to more appropriate interpretation of previously unidentified freshwater virome sequences, as demonstrated in marine environments by studies on phages infecting the SAR11 and SAR116 clades (Kang et al ., ; Zhao et al ., ). Furthermore, the finding that most of the highly assigned viruses in the binning of freshwater viromes were of marine origin, except for P19250A, Synechococcus phage S‐EIV1 (Table ) and putative actinobacteria phages (Supporting Information Table S5), demonstrates the paucity of cultured and identified representative freshwater phages in public genome databases (Bruder et al ., ), and emphasizes the need for isolation of phages infecting other major freshwater bacterial groups such as acI, acIV, Limnohabitans and Polynucleobacter .…”

Section: Resultsmentioning

confidence: 99%

Genome characteristics and environmental distribution of the first phage that infects the LD28 clade, a freshwater methylotrophic bacterial group

Moon

Kang

Kim

et al. 2017

Environmental Microbiology

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Bacteriophages infecting major groups of freshwater heterotrophic bacteria have been rarely isolated, hampering analyses of freshwater viromes. Here, we report the isolation and genomic characterization of P19250A, the first phage that infects the LD28 clade, an abundant freshwater methylotrophic bacterial group. P19250A was isolated from Lake Soyang, an oligotrophic reservoir, using an LD28 strain as a host. Morphological and genomic analyses revealed that P19250A is a lytic siphovirus with a ∼38.6-kb genome. To analyze the distribution of P19250A genome within its habitat, six seasonal viral metagenome (virome) samples were prepared from Lake Soyang. Through binning analysis of freshwater viromes, P19250A was shown to be the most highly assigned freshwater phage that infects heterotrophic bacteria (up to 8.21%) in five viromes. Furthermore, when freshwater virome data collected worldwide were analyzed, P19250A genome also showed high abundance, especially in Lough Neagh, UK, where P19250A genome was recorded as the most abundant bacteriophage. From metagenome analysis, the proportion of P19250A-assigned reads showed seasonal fluctuation following the abundance of the LD28 clade in Lake Soyang. These results showed that P19250A would be an essential resource for analyses of freshwater viromes, and also suggest that phages of other abundant freshwater bacteria need to be isolated for better understanding of freshwater viruses.

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Freshwater Metaviromics and Bacteriophages: A Current Assessment of the State of the Art in Relation to Bioinformatic Challenges

Cited by 22 publications

References 88 publications

Multiple mechanisms drive phage infection efficiency in nearly identical hosts

Multiple mechanisms drive phage infection efficiency in nearly identical hosts

Pseudomonas PB1-Like Phages: Whole Genomes from Metagenomes Offer Insight into an Abundant Group of Bacteriophages

Genome characteristics and environmental distribution of the first phage that infects the LD28 clade, a freshwater methylotrophic bacterial group

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