Adaptation to sub-optimal hosts is a driver of viral diversification in the ocean

Enav, Hagay; Kirzner, Shay; Lindell, Debbie; Mandel-Gutfreund, Yael; Béjà, Oded

doi:10.1038/s41467-018-07164-3

Cited by 47 publications

(41 citation statements)

References 65 publications

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“…In line with these observations, many actinobacterial MAGs show short-lived maxima in the epilimnion followed by lower abundances in the hypolimnion as observed earlier via fluorescence in situ hybridization with species to genus-specific probes [30]. It has also been shown recently that in the absence of the optimal host phages may switch to sub-optimal hosts [58], further driving diversification and likely helping extend the longevity of phage lineages.…”

Section: Resultssupporting

confidence: 65%

Phage-centric ecological interactions in aquatic ecosystems revealed through ultra-deep metagenomics

Kavagutti

Andrei

Mehrshad

et al. 2019

Preprint

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19The persistent inertia in the ability to culture environmentally abundant microbes from aquatic 20 ecosystems represents an obstacle in disentangling the complex web of ecological 21 interactions spun by a diverse assortment of participants (pro-and eukaryotes and their 22 viruses). In aquatic microbial communities, the numerically most abundant actors, the 23 viruses, remain the most elusive, and especially in freshwaters their identities and ecology 24 remain obscure. Here, using ultra-deep metagenomic sequencing from freshwater habitats Supplementary Table S1). While most samples we sequenced were ca. 54 Gb in size 87 (ranging from 190-482 million reads, average 368 million reads), two Římov samples (epi 88 and hypolimnion) we sequenced ca. 380 Gb each (2.5 billion reads each). An overview of the 89 microbial community using 16S rRNA abundances for both sites is shown in Supplementary 90 Figure S2. 91We also collected an additional 149 publicly available freshwater metagenomes 92 ( Supplementary Table S1, total of 4.04 billion reads, 1.09 Tb data) to search for complete 93 phage genomes. All datasets were assembled independently (no co-assembly). In total, we 94 analyzed ca. 3 Tb of metagenomic sequences from freshwater (ca. 17 billion reads). 95The number of complete phage genomes recovered from any sample increased with 96 sequencing depth, but with diminishing returns (Figure 1a), with genome recovery 97 maintaining linearity up to 100 Gb (ca. 1 phage genome for every additional Gb) before 98 tapering off at a maximum of 160 genomes from 400 Gb sequence data. While a total of 99 1677 genomes were assembled from the sequence data generated from the two study sites, 100(Římov and Jiřická), 357 genomes were recovered from all other available freshwater 101 metagenomes. This suggests that the potential of ultra-deep sequencing to recover far more 102 phage genomes has not yet been fully realized. We also recovered a number of 103 metagenome-assembled genomes (MAGs) from the Římov metagenome time-series dataset 104 (see below). We denominate this entire collection of genomes as the Uncultured Freshwater 105 Organisms (UFO) dataset, where the UFOv subset refers to viruses and the UFOp subset to 106 prokaryotic genomes. 107Phage genome analyses 108 A total of 598 complete phage genomes were recovered from the Římov epilimnion (10 109 samples), 800 from the hypolimnion (8 samples) and 279 from Jiřická (5 samples). Upon 110 dereplication (genomes with >95% identity and >95% coverage treated as one, see 111 methods), these numbers reduced by nearly three-fold for the hypolimnion suggesting 112 repeated capture of nearly identical genomes from multiple samplings. We found only a 113 single instance of a phage that was nearly identical in two habitats (Římov and Jiřická). 114The comparison of recovered freshwater phage genomes to representative sets of phages 115 from Viral RefSeq (1996 genomes) and the marine habitat (1335 genomes) [23-25] is shown 116 in Fig. 1c. Intriguingly, the genome size distributions of marin...

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Section: Resultssupporting

confidence: 65%

Phage-centric ecological interactions in aquatic ecosystems revealed through ultra-deep metagenomics

Kavagutti

Andrei

Mehrshad

et al. 2019

Preprint

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“…Culture clearing in particular can be performed in multi-well plates in an automated system for high-throughput monitoring [99]. Finally, the original isolation host, especially as it typically will not have been isolated from the same sample as the virus isolate, is not always a primary host of a virus but instead may represent a sub-optimal host, leading to inaccurate estimation of growth parameters [100,101]. These various limitations on growing virus hosts in the laboratory make the isolation, propagation, and also ecological characterization of viral isolates in the laboratory challenging.…”

Section: Techniques For Isolating Virusesmentioning

confidence: 99%

Coming-of-Age Characterization of Soil Viruses: A User’s Guide to Virus Isolation, Detection within Metagenomes, and Viromics

et al. 2020

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The study of soil viruses, though not new, has languished relative to the study of marine viruses. This is particularly due to challenges associated with separating virions from harboring soils. Generally, three approaches to analyzing soil viruses have been employed: (1) Isolation, to characterize virus genotypes and phenotypes, the primary method used prior to the start of the 21st century. (2) Metagenomics, which has revealed a vast diversity of viruses while also allowing insights into viral community ecology, although with limitations due to DNA from cellular organisms obscuring viral DNA. (3) Viromics (targeted metagenomics of virus-like-particles), which has provided a more focused development of ‘virus-sequence-to-ecology’ pipelines, a result of separation of presumptive virions from cellular organisms prior to DNA extraction. This separation permits greater sequencing emphasis on virus DNA and thereby more targeted molecular and ecological characterization of viruses. Employing viromics to characterize soil systems presents new challenges, however. Ones that only recently are being addressed. Here we provide a guide to implementing these three approaches to studying environmental viruses, highlighting benefits, difficulties, and potential contamination, all toward fostering greater focus on viruses in the study of soil ecology.

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“…This arms race necessarily results in an increase in the genomic diversity of both partners to ensure population survival, 8,9 as seen in aquatic ecosystems. 10,11 However, most studies of this type are limited to single pairs of bacteria and bacteriophages and are frequently performed in laboratory settings.…”

Section: Introductionmentioning

confidence: 99%

“I will survive”: A tale of bacteriophage-bacteria coevolution in the gut

2018

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Viruses that infect bacteria, or bacteriophages, are among the most abundant entities in the gut microbiome. However, their role and the mechanisms by which they infect bacteria in the intestinal tract remain poorly understood. We recently reported that intestinal bacteria are an evolutionary force, driving the expansion of the bacteriophage host range by boosting the genetic variability of these viruses. Here, we expand these observations by studying antagonistic bacteriophage-bacteria coevolution dynamics and revealing that bacterial genetic variability is also increased under the pressure of bacteriophage predation. We propose a model showing how the expansion of bacteriophage-bacteria infection networks is relative to the opportunities for coevolution encountered in the intestinal tract. Our data suggest that predator-prey dynamics are perpetuated and differentiated in parallel, to generate and maintain intestinal microbial diversity and equilibrium.

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Adaptation to sub-optimal hosts is a driver of viral diversification in the ocean

Cited by 47 publications

References 65 publications

Phage-centric ecological interactions in aquatic ecosystems revealed through ultra-deep metagenomics

Phage-centric ecological interactions in aquatic ecosystems revealed through ultra-deep metagenomics

Coming-of-Age Characterization of Soil Viruses: A User’s Guide to Virus Isolation, Detection within Metagenomes, and Viromics

“I will survive”: A tale of bacteriophage-bacteria coevolution in the gut

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