Virus-host relationships of marine single-celled eukaryotes resolved from metatranscriptomics

Moniruzzaman, Mohammad; Wurch, Louie L.; Alexander, Harriet; Dyhrman, Sonya T.; Gobler, Christopher J.; Wilhelm, Steven W.

doi:10.1038/ncomms16054

Cited by 103 publications

(128 citation statements)

References 60 publications

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“…A general prediction we may venture is that introducing RS microalgae in community models may increase the overall stability of the host-virus dynamics. This model is consistent with previously reported non 'boom and bust' dynamics in the natural environment [85] [86], including persistent infection [87]. Within the simplified one microalga one virus experimental set up our model makes two predictions.…”

Section: What Is the Prevalence Of The Rs Strategy In The Environment?supporting

confidence: 89%

Virus-host coexistence in phytoplankton through the genomic lens

Yau

Krasovec

Rombauts

et al. 2019

Preprint

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Phytoplankton-virus interactions are major determinants of geochemical cycles in the oceans. Viruses are responsible for the redirection of carbon and nutrients away from larger organisms back towards microorganisms via the lysis of microalgae in a process coined the 'viral shunt'. Virus-host interactions are generally expected to follow 'boom and bust' dynamics, whereby a numerically dominant strain is lysed and replaced by a virus resistant strain. Here, we isolated a microalga and its infective nucleo-cytoplasmic large DNA virus (NCLDV) concomitantly from the environment in the surface NW Mediterranean Sea, Ostreococcus mediterraneus, and show continuous growth in culture of both the microalga and the virus. Evolution experiments through single cell bottlenecks demonstrate that, in the absence of the virus, susceptible cells evolve from one ancestral resistant single cell, and vice-versa; that is that resistant cells evolve from one ancestral susceptible cell. This provides evidence that the observed sustained viral production is the consequence of a minority of virus-susceptible cells. The emergence of these cells is explained by low-level phase switching between virus-resistant and virus-susceptible phenotypes, akin to a bet hedging strategy. Whole genome sequencing and analysis of the ~14 Mb microalga and the ~200 kb virus points towards ancient speciation of the microalga within the Ostreococcus species complex and frequent gene exchanges between prasinoviruses infectingOstreococcus species. Re-sequencing of one susceptible strain demonstrated that the phase switch involved a large 60 Kb deletion of one chromosome. This chromosome is an outlier chromosome compared to the streamlined, gene dense, GC-rich standard chromosomes, as it contains many repeats and few orthologous genes. While this chromosome has been described in three different genera, its size increments have been previously associated to antiviral immunity and resistance in another species from the same genus. Mathematical modelling of this mechanism predicts microalga-virus population dynamics consistent with the observation of continuous growth of both virus and microalga. Altogether, our results suggest a previously overlooked strategy in phytoplankton-virus interactions.

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Section: What Is the Prevalence Of The Rs Strategy In The Environment?supporting

confidence: 89%

Virus-host coexistence in phytoplankton through the genomic lens

Yau

Krasovec

Rombauts

et al. 2019

Preprint

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“…Viral infection can be assessed by monitoring viral transcription in the host, for example by studying a marker gene for a specific virus (Kimura et al, 2012). However, metatranscriptomics targeting a whole range of viruses (Moniruzzaman et al, 2017;Stough et al, 2018) is likely the most powerful approach to evaluate viral population dynamics in natural communities. Currently, the Osaka Bay and North Pacific Subtropical Gyre highresolution temporal transcriptomic time-series are of great value for the viral ecology community (Aylward et al, 2017;Yoshida et al, 2018).…”

Section: Discussionmentioning

confidence: 99%

Diel cycling of the cosmopolitan abundant Pelagibacter virus 37‐F6: one of the most abundant viruses on earth

Martínez-Hernández

Luo

Tominaga

et al. 2020

Environ Microbiol Rep

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Summary The spatiotemporal dynamics for marine viral populations has only recently been explored. However, nothing is known about temporal activities of the uncultured Pelagibacter virus vSAG 37‐F6, which was discovered by single‐virus genomics as potentially the most abundant marine virus. Here, we investigate the diel cycling of 37‐F6 virus and the putative SAR11 host using coastal and oceanic transcriptomic and viromic time‐series data from Osaka Bay and North Pacific Subtropical Gyre. Virus 37‐F6 and relatives displayed diel cycling of transcriptional activities synchronized with its putative host. In both virus and host, the lowest transcription rates were observed at 14:00–15:00, coinciding roughly with maximum solar irradiance, while higher transcriptional rates were detected during the night/early morning and afternoon. Diel abundance of free viruses of 37‐F6 in seawater roughly mirrored the transcriptional activities of both virus and host. In Osaka Bay, among viral relatives (genus level), virus 37‐F6 specifically showed the highest ratio of transcriptional activity to virome abundance, a proxy for viral transcriptional activity relative to free viral particle abundance. This high ratio suggests high infection rate efficiencies in vSAG 37‐F6 virus compared to viral relatives. Thus, time‐series data revealed temporal transcript activities in one of the most abundant viruses in Earth.

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“…HPG substitution into specific proteins was confirmed by mass spectrometry from experiments using BONCAT‐positive T7 and EhV viruses, with many of the detected HPG‐labelled proteins involved in procapsid and capsid formation and DNA packaging (Table ). Moniruzzaman and colleagues () recently demonstrated the utility of the Major Capsid Protein (MCP) as a marker for infection dynamics and diversity in natural populations. Therefore, tracking changes in HPG‐labelled viral proteins over time in other cultures and extending this to natural environments (e.g., tracking HGP incorporation into MCP) provides us an exciting opportunity to characterize infection dynamics at the protein level.…”

Section: Discussionmentioning

confidence: 99%

Interrogating marine virus‐host interactions and elemental transfer with BONCAT and nanoSIMS‐based methods

Pasulka

Thamatrakoln

Kopf

et al. 2017

Environmental Microbiology

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Summary While the collective impact of marine viruses has become more apparent over the last decade, a deeper understanding of virus‐host dynamics and the role of viruses in nutrient cycling would benefit from direct observations at the single‐virus level. We describe two new complementary approaches – stable isotope probing coupled with nanoscale secondary ion mass spectrometry (nanoSIMS) and fluorescence‐based biorthogonal non‐canonical amino acid tagging (BONCAT) – for studying the activity and biogeochemical influence of marine viruses. These tools were developed and tested using several ecologically relevant model systems (Emiliania huxleyi/EhV207, Synechococcus sp. WH8101/Syn1 and Escherichia coli/T7). By resolving carbon and nitrogen enrichment in viral particles, we demonstrate the power of nanoSIMS tracer experiments in obtaining quantitative estimates for the total number of viruses produced directly from a particular production pathway (by isotopically labelling host substrates). Additionally, we show through laboratory experiments and a pilot field study that BONCAT can be used to directly quantify viral production (via epifluorescence microscopy) with minor sample manipulation and no dependency on conversion factors. This technique can also be used to detect newly synthesized viral proteins. Together these tools will help fill critical gaps in our understanding of the biogeochemical impact of viruses in the ocean.

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Virus-host relationships of marine single-celled eukaryotes resolved from metatranscriptomics

Cited by 103 publications

References 60 publications

Virus-host coexistence in phytoplankton through the genomic lens

Virus-host coexistence in phytoplankton through the genomic lens

Diel cycling of the cosmopolitan abundant Pelagibacter virus 37‐F6: one of the most abundant viruses on earth

Interrogating marine virus‐host interactions and elemental transfer with BONCAT and nanoSIMS‐based methods

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