The Diversity and Ecology of Aquatic Viruses from Headwaters to the Hadal

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Original Research
12 June 2019
Single Cell Genomics-Based Analysis of Gene Content and Expression of Prophages in a Diffuse-Flow Deep-Sea Hydrothermal System
Jessica M. Labonté
7 more and 
Ramunas Stepanauskas
Similarity of the SSU rRNA genes (phylogenetic trees), host genomes (average nucleotide identity), and the corresponding prophage genomes (overall similarity) of Spirochaetes (A) and Thermotogae (B). Maximum likelihood phylogenetic trees were generated using the GTR model with a gamma distribution (+G), estimated rates of variation among sites, and a proportion of invariable sites (+I). Bootstrap support by 100, ≥85, and ≥75% replicates out of 100 are shown by black, gray, and white dots at the nodes.

Phage–host interactions likely play a major role in the composition and functioning of many microbiomes, yet remain poorly understood. Here, we employed single cell genomics to investigate phage–host interactions in a diffuse-flow, low-temperature hydrothermal vent that may be reflective of a broadly distributed biosphere in the subseafloor. We identified putative prophages in 13 of 126 sequenced single amplified genomes (SAGs), with no evidence for lytic infections, which is in stark contrast to findings in the surface ocean. Most were distantly related to known prophages, while their hosts included bacterial phyla Campylobacterota, Bacteroidetes, Chlorobi, Proteobacteria, Lentisphaerae, Spirochaetes, and Thermotogae. Our results suggest the predominance of lysogeny over lytic interaction in diffuse-flow, deep-sea hydrothermal vents, despite the high activity of the dominant Campylobacteria that would favor lytic infections. We show that some of the identified lysogens have co-evolved with their host over geological time scales and that their genes are transcribed in the environment. Functional annotations of lysogeny-related genes suggest involvement in horizontal gene transfer enabling host’s protection against toxic metals and antibacterial compounds.

8,670 views
15 citations
Perspective
16 April 2019

Tools allowing for the identification of viral sequences in host-associated and environmental metagenomes allows for a better understanding of the genetics and ecology of viruses and their hosts. Recently, new approaches using machine learning methods to distinguish viral from bacterial signal using k-mer sequence signatures were published for identifying viral contigs in metagenomes. The promise of these content-based approaches is the ability to discover new viruses, with no or few known relatives. In this perspective paper, we examine the use of the content-based machine learning tool VirFinder for the identification of viral sequences in aquatic metagenomes and explore the possibility of using ecosystem-focused models targeted to marine metagenomes. We discuss the impact of the training set composition on the tool performance and the current limitation for the retrieval of low abundance viral sequences in metagenomes. We identify potential biases that could arise from machine learning approaches for viral hunting in real-world datasets and suggest possible avenues to overcome them.

7,132 views
42 citations
5,692 views
24 citations
Original Research
09 January 2019
First Viruses Infecting the Marine Diatom Guinardia delicatula
Laure Arsenieff
7 more and 
Anne-Claire Baudoux

The marine diatom Guinardia delicatula is a cosmopolitan species that dominates seasonal blooms in the English Channel and the North Sea. Several eukaryotic parasites are known to induce the mortality of this species. Here, we report the isolation and characterization of the first viruses that infect G. delicatula. Viruses were isolated from the Western English Channel (SOMLIT-Astan station) during the late summer bloom decline of G. delicatula. A combination of laboratory approaches revealed that these lytic viruses (GdelRNAV) are small tailless particles of 35–38 nm in diameter that replicate in the host cytoplasm where both unordered particles and crystalline arrays are formed. GdelRNAV display a linear single-stranded RNA genome of ~9 kb, including two open reading frames encoding for replication and structural polyproteins. Phylogenetic relationships based on the RNA-dependent-RNA-polymerase gene marker showed that GdelRNAV are new members of the Bacillarnavirus, a monophyletic genus belonging to the order Picornavirales. GdelRNAV are specific to several strains of G. delicatula. They were rapidly and largely produced (<12 h, 9.34 × 104 virions per host cell). Our analysis points out the host's variable viral susceptibilities during the early exponential growth phase. Interestingly, we consistently failed to isolate viruses during spring and early summer while G. delicatula developed important blooms. While our study suggests that viruses do contribute to the decline of G. delicatula's late summer bloom, they may not be the primary mortality agents during the remaining blooms at SOMLIT-Astan. Future studies should focus on the relative contribution of the viral and eukaryotic pathogens to the control of Guinardia's blooms to understand the fate of these prominent organisms in marine systems.

7,099 views
39 citations
Bayesian inference phylogenetic reconstruction of DNA polymerase I protein of TC-CHP58. Numbers indicate Bayesian posterior probabilities as percentage/ultra-fast bootstrap values. Only UFBoot values over 80 and Bayesian PP over 50 are shown. The sequence characterized in the present study is reported in bold letters. Scale bar: 0.4 amino acid substitutions per site.
5,966 views
27 citations
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