Marine viruses interact with microbial hosts in dynamic environments shaped by variation in abiotic factors, including temperature. However, the impacts of temperature on viral infection of ...phytoplankton are not well understood. Here we coupled mathematical modelling with experiments to explore the effect of temperature on virus‐phytoplankton interactions. Our model shows the negative consequences of high temperatures on infection and suggests a temperature‐dependent threshold between viral production and degradation. Modelling long‐term dynamics in environments with different average temperatures revealed the potential for long‐term host‐virus coexistence, epidemic free or habitat loss states. We generalised our model to variation in global sea surface temperatures corresponding to present and future seas and show that climate change may differentially influence virus‐host dynamics depending on the virus‐host pair. Temperature‐dependent changes in the infectivity of virus particles may lead to shifts in virus‐host habitats in warmer oceans, analogous to projected changes in the habitats of macro‐, microorganisms and pathogens.
The impacts of temperature on viral infection of phytoplankton are not well understood. Here we coupled mathematical modelling with experimental data sets to explore the effect of temperature on virus‐phytoplankton dynamics. Our model shows the negative consequences of high temperatures on infection and suggests a temperature‐dependent threshold between viral production and degradation. Our study suggests that ocean warming may lead to shifts in virus‐host habitats in future oceans, analogous to projected changes in the habitats of macroorganisms, microorganisms and pathogens.
Major seasonal community reorganizations and associated biomass variations are landmarks of plankton ecology. However, the processes of plankton community turnover rates have not been fully ...elucidated so far. Here, we analyse patterns of planktonic protist community succession in temperate latitudes, based on quantitative taxonomic data from both microscopy counts (cells >10 μm) and ribosomal DNA metabarcoding (size fraction >3 μm, 18S rRNA gene) from plankton samples collected bimonthly over 8 years (2009–2016) at the SOMLIT‐Astan station (Roscoff, Western English Channel). Based on morphology, diatoms were clearly the dominating group all year round and over the study period. Metabarcoding uncovered a wider diversity spectrum and revealed the prevalence of Dinophyceae and diatoms but also of Cryptophyta, Chlorophyta, Cercozoa, Syndiniales and Ciliophora in terms of read counts and or richness. The use of morphological and molecular analyses in combination allowed improving the taxonomic resolution and to identify the sequence of the dominant species and OTUs (18S V4 rDNA‐derived taxa) that drive annual plankton successions. We detected that some of these dominant OTUs were benthic as a result of the intense tidal mixing typical of the French coasts in the English Channel. Our analysis of the temporal structure of community changes point to a strong seasonality and resilience. The temporal structure of environmental variables (especially Photosynthetic Active Radiation, temperature and macronutrients) and temporal structures generated by species life cycles and or species interactions, are key drivers of the observed cyclic annual plankton turnover.
Viruses influence microbial community structure and biogeochemical cycles in marine environments. Viral attachment to nonhost surfaces could influence host viral infection rates; however, the ...prevalence of such viral attachment is not investigated quantitatively. We used coastal seawater viral assemblages and, as models, marine vibriophage (SIO-2) and enterobacteriophages (T2 and T4) to investigate their attachment to probable nonhost marine bacteria. We also studied viral attachment to colloids and other abiotic surfaces in seawater. Centrifugation experiments with bacterium-virus mixtures showed substantial viral loss in the supernatant presumably due to the viral attachment to bacteria. This attachment (0.04 to 24 viruses μm
bacterial surface area) varied with bacterium-virus combinations. Surprisingly, filtering seawater on 0.2-μm Anodisc or polycarbonate filters retained ∼12 to 84% of viruses presumably attached to ≥0.2-μm-sized particles and/or the filter surface. Enzymatic digestion followed by epifluorescence and atomic force microscopy suggested that 7 to 25% of the total viruses were attached via β-glycosidic linkages. Furthermore, a substantial proportion (7 to 48%) of viruses became attached to model abiotic surfaces (polycarbonate, polypropylene, and glass), and this has significance for laboratory protocols as well as studies of virus ecology in particle-rich marine environments. Substantial attachment of viruses to nonhost surfaces could influence virus-driven biogeochemical cycles and microbial community structure.
Viruses play important roles in altering microbial community structure and biogeochemical cycles in marine environments. Viral attachment to nonhost surfaces can influence host viral infection rates; however, the prevalence of viral attachment to nonhost surfaces and the ratio of attached viruses to total viruses are little known. We used coastal seawater viral assemblages and used marine vibriophage (SIO-2) and enterobacteriophages (T2 and T4) as models to investigate their attachment to abiotic and biotic surfaces in seawater. Viral attachment was observed on several surfaces, such as nonhost bacteria, polymers, filters, cover glasses, and tube surfaces. This study cautions against commonly used protocols that require viral incubation and seawater fractionation. More importantly, these results could influence virus-driven biogeochemical cycles and microbial community structure in the ocean.
Photosynthetic picoeukaryotesx in the genus Micromonas show among the widest latitudinal distributions on Earth, experiencing large thermal gradients from poles to tropics. Micromonas comprises at ...least four different species often found in sympatry. While such ubiquity might suggest a wide thermal niche, the temperature response of the different strains is still unexplored, leaving many questions as for their ecological success over such diverse ecosystems. Using combined experiments and theory, we characterize the thermal response of eleven Micromonas strains belonging to four species. We demonstrate that the variety of specific responses to temperature in the Micromonas genus makes this environmental factor an ideal marker to describe its global distribution and diversity. We then propose a diversity model for the genus Micromonas, which proves to be representative of the whole phytoplankton diversity. This prominent primary producer is therefore a sentinel organism of phytoplankton diversity at the global scale. We use the diversity within Micromonas to anticipate the potential impact of global warming on oceanic phytoplankton. We develop a dynamic, adaptive model and run forecast simulations, exploring a range of adaptation time scales, to probe the likely responses to climate change. Results stress how biodiversity erosion depends on the ability of organisms to adapt rapidly to temperature increase.
In the ocean, Bacillariophyta are one of the most successful protistan groups. Due to their considerable biogeochemical implications, diatom diversity, development, and seasonality have been at the ...center of research, specifically large-sized species. In comparison, nanoplanktonic diatoms are mostly disregarded from routine monitoring and are often underrepresented in genetic reference databases. Here, we identified and investigated the temporal dynamics of relevant nanodiatoms occurring in the Western English Channel (SOMLIT-Astan station). Coupling in situ and laboratory approaches, we revealed that nano-species from the genera Minidiscus and Thalassiosira are key components of the phytoplankton community that thrive in these coastal waters, but they display different seasonal patterns. Some species formed recurrent blooms whilst others were persistent year round. These results raise questions about their regulation in the natural environment. Over a full seasonal cycle at the monitoring station, we succeeded in isolating viruses which infect these minute diatoms, suggesting that these mortality agents may contribute to their control. Overall, our study points out the importance of considering nanodiatom communities within time-series surveys to further understand their role and fate in marine systems.
The genus Micromonas comprises phytoplankton that show among the widest latitudinal distributions on Earth, and members of this genus are recurrently infected by prasinoviruses in contrasted thermal ...ecosystems. In this study, we assessed how temperature influences the interplay between the main genetic clades of this prominent microalga and their viruses. The growth of three Micromonas strains (Mic-A, Mic-B, Mic-C) and the stability of their respective lytic viruses (MicV-A, MicV-B, MicV-C) were measured over a thermal range of 4-32.5 °C. Similar growth temperature optima (T
) were predicted for all three hosts but Mic-B exhibited a broader thermal tolerance than Mic-A and Mic-C, suggesting distinct thermoacclimation strategies. Similarly, the MicV-C virus displayed a remarkable thermal stability compared with MicV-A and MicV-B. Despite these divergences, infection dynamics showed that temperatures below T
lengthened lytic cycle kinetics and reduced viral yield and, notably, that infection at temperatures above T
did not usually result in cell lysis. Two mechanisms operated depending on the temperature and the biological system. Hosts either prevented the production of viral progeny or maintained their ability to produce virions with no apparent cell lysis, pointing to a possible switch in the viral life strategy. Hence, temperature changes critically affect the outcome of Micromonas infection and have implications for ocean biogeochemistry and evolution.
L’océan est le réservoir le plus important de virus sur la planète avec des abondances allant jusqu’à plusieurs milliards par litre. Ces virus sont une force directrice majeure pour l’évolution et la ...structuration du monde microbien, mais aussi pour le fonctionnement des grands cycles biogéochimiques dans les écosystèmes marins. Grâce aux techniques de séquençage à haut débit, nous commençons à entrevoir la diversité et la complexité de cette virosphère marine. Cette synthèse décrit les découvertes importantes dans le domaine de l’écologie virale marine et aborde la diversité de ces micro-organismes fascinants, leur impact sur la mortalité microbienne et les cycles de nutriments et d’énergie dans l’océan.
The ocean is the largest reservoir of viruses on the planet with estimates of up to several billions per liter. These viruses represent a major driving force not only for the evolution and for structuring the microbial world, but also for the functioning and the balance of marine ecosystems. With the advances in high throughput sequencing techniques, we are beginning to uncover the diversity and the complexity of this marine virosphere. This review synthesizes milestones in the field of marine viral ecology, including the diversity of these fascinating microorganisms, their impact on microbial mortality and cycling of nutrients and energy in the ocean.
Biological control using bacteriophages is a promising approach for mitigating the devastating effects of coral diseases. Several phages that infect
, a widespread coral pathogen, have been isolated, ...suggesting that this bacterium is permissive to viral infection and is, therefore, a suitable candidate for treatment by phage therapy. In this study, we combined functional and genomic approaches to evaluate the therapeutic potential of BONAISHI, a novel
phage, which was isolated from the coral reef in Van Phong Bay (Vietnam). BONAISHI appears to be strictly lytic for several pathogenic strains of
and remains infectious over a broad range of environmental conditions. This candidate has an unusually large dsDNA genome (303 kb), with no genes that encode known toxins or implicated in lysogeny control. We identified several proteins involved in host lysis, which may offer an interesting alternative to the use of whole bacteriophages for controlling
. A preliminary therapy test showed that adding BONAISHI to an infected culture of
sp. cells reduced the impact of
on
sp. photosynthetic activity. This study showed that BONAISHI is able to mitigate
infections, making it a good candidate for phage therapy for coral disease.
Most of studied bacteriophages (phages) are terrestrial viruses. However, marine phages are shown to be highly involved in all levels of oceanic regulation. They are, however, still largely ...overlooked by the scientific community. By inducing cell lysis on half of the bacterial population daily, their role and influence on the bacterial biomass and evolution, as well as their impact in the global biogeochemical cycles, is undeniable. Cobetia marina
(Carin-1) is a member of the
family infecting the γ
. marina. Here, we present the almost complete, nearly-atomic resolution structure of Carin-1 comprising capsid, portal, and tail machineries at 3.5 Å, 3.8 Å and 3.9 Å, respectively, determined by cryo-electron microscopy (cryo-EM). Our experimental results, combined with AlphaFold2 (AF), allowed us to obtain the nearly-atomic structure of Carin-1 by fitting and refining the AF atomic models in the high resolution cryo-EM map, skipping the bottleneck of
manual building and speeding up the structure determination process. Our structural results highlighted the T7-like nature of Carin1, as well as several novel structural features like the presence of short spikes on the capsid, reminiscent those described for Rhodobacter capsulatus gene transfer agent (RcGTA). This is, to our knowledge, the first time such assembly is described for a bacteriophage, shedding light into the common evolution and shared mechanisms between gene transfer agents and phages. This first full structure determined for a marine podophage allowed to propose an infection mechanism different than the one proposed for the archetypal podophage T7.
Oceans play a central role in the carbon cycle on Earth and on the climate regulation (half of the planet's CO2 is absorbed by phytoplankton photosynthesis in the oceans and just as much O2 is liberated). The understanding of the biochemical equilibriums of marine biology represents a major goal for our future. By lysing half of the bacterial population every day, marine bacteriophages are key actors of these equilibriums. Despite their importance, these marine phages have, so far, only been studied a little and, in particular, structural insights are currently lacking, even though they are fundamental for the understanding of the molecular mechanisms of their mode of infection. The structures described in our manuscript allow us to propose an infection mechanism that differs from the one proposed for the terrestrial T7 virus, and might also allow us to, in the future, better understand the way bacteriophages shape the global ecosystem.
The marine diatom
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
.
. Viruses were isolated from the Western English Channel (SOMLIT-Astan station) during the late summer bloom decline of
.
. 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
, a monophyletic genus belonging to the order
. GdelRNAV are specific to several strains of
.
. They were rapidly and largely produced (<12 h, 9.34 × 10
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
.
developed important blooms. While our study suggests that viruses do contribute to the decline of
.
'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
's blooms to understand the fate of these prominent organisms in marine systems.
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