Seasonal dynamics of algae-infecting viruses and their inferred interactions with protists

Viruses are a highly abundant, dynamic, and diverse component of planktonic communities that have key roles in marine ecosystems. We aimed to reveal the diversity and dynamics of marine large dsDNA viruses infecting algae in the Northern Skagerrak, South Norway through the year by metabarcoding, targeting the major capsid protein (MCP) and its correlation to protist diversity and dynamics. Metabarcoding results demonstrated a high diversity of algal viruses compared to previous metabarcoding surveys in Norwegian coastal waters. We obtained 313 putative algal virus operational taxonomic units (vOTUs), all classified by phylogenetic analyses to either the Phycodnaviridae or Mimiviridae families, most of them in clades without any cultured or environmental reference sequences. The viral community showed a clear temporal variation, with some vOTUs persisting for several months. The results indicate co-occurrences between abundant viruses and potential hosts during long periods. This study gives new insights into the virus-algal host dynamics and provides a baseline for future studies of algal virus diversity and temporal dynamics.publishedVersio

Genome analyses of the microalga Picochlorum provide insights into the evolution of thermotolerance in the green lineage

While the molecular events involved in cell responses to heat stress have been extensively studied, our understanding of the genetic basis of basal thermotolerance, and particularly its evolution within the green lineage, remains limited. Here, we present the 13.3-Mb haploid genome and transcriptomes of a halotolerant and thermotolerant unicellular green alga, Picochlorum costavermella (Trebouxiophyceae) to investigate the evolution of the genomic basis of thermotolerance. Differential gene expression at high and standard temperatures revealed that more of the gene families containing up-regulated genes at high temperature were recently evolved, and less originated at the ancestor of green plants. Inversely, there was an excess of ancient gene families containing transcriptionally repressed genes. Interestingly, there is a striking overlap between the thermotolerance and halotolerance transcriptional rewiring, as more than one-third of the gene families up-regulated at 35 degrees C were also up-regulated under variable salt concentrations in Picochlorum SE3. Moreover, phylogenetic analysis of the 9,304 protein coding genes revealed 26 genes of horizontally transferred origin in P. costavermella, of which five were differentially expressed at higher temperature. Altogether, these results provide new insights about how the genomic basis of adaptation to halo- and thermotolerance evolved in the green lineage

Population genomics of picophytoplankton unveils novel chromosome hypervariability

Tiny photosynthetic microorganisms that form the picoplankton (between 0.3 and 3 mm in diameter) are at the base of the food web in many marine ecosystems, and their adaptability to environmental change hinges on standing genetic variation. Although the genomic and phenotypic diversity of the bacterial component of the oceans has been intensively studied, little is known about the genomic and phenotypic diversity within each of the diverse eukaryotic species present. We report the level of genomic diversity in a natural population of Ostreococcus tauri (Chlorophyta, Mamiellophyceae), the smallest photosynthetic eukaryote. Contrary to the expec- tations of clonal evolution or cryptic species, the spectrum of genomic polymorphism observed suggests a large panmictic population (an effective population size of 1.2 × 107) with pervasive evidence of sexual reproduction. De novo assemblies of low-coverage chromosomes reveal two large candidate mating-type loci with suppressed recom- bination, whose origin may pre-date the speciation events in the class Mamiellophyceae. This high genetic diversity is associated with large phenotypic differences between strains. Strikingly, resistance of isolates to large double- stranded DNA viruses, which abound in their natural environment, is positively correlated with the size of a single hypervariable chromosome, which contains 44 to 156 kb of strain-specific sequences. Our findings highlight the role of viruses in shaping genome diversity in marine picoeukaryotes

Community-Level Responses to Iron Availability in Open Ocean Plankton Ecosystems

Predicting responses of plankton to variations in essential nutrients is hampered by limited in situ measurements, a poor understanding of community composition, and the lack of reference gene catalogs for key taxa. Iron is a key driver of plankton dynamics and, therefore, of global biogeochemical cycles and climate. To assess the impact of iron availability on plankton communities, we explored the comprehensive bio-oceanographic and bio-omics data sets from Tara Oceans in the context of the iron products from two state-of-the-art global scale biogeochemical models. We obtained novel information about adaptation and acclimation toward iron in a range of phytoplankton, including picocyanobacteria and diatoms, and identified whole subcommunities covarying with iron. Many of the observed global patterns were recapitulated in the Marquesas archipelago, where frequent plankton blooms are believed to be caused by natural iron fertilization, although they are not captured in large-scale biogeochemical models. This work provides a proof of concept that integrative analyses, spanning from genes to ecosystems and viruses to zooplankton, can disentangle the complexity of plankton communities and can lead to more accurate formulations of resource bioavailability in biogeochemical models, thus improving our understanding of plankton resilience in a changing environment

Viruses of Polar Aquatic Environments

The poles constitute 14% of the Earth’s biosphere: The aquatic Arctic surrounded by land in the north, and the frozen Antarctic continent surrounded by the Southern Ocean. In spite of an extremely cold climate in addition to varied topographies, the polar aquatic regions are teeming with microbial life. Even in sub-glacial regions, cellular life has adapted to these extreme environments where perhaps there are traces of early microbes on Earth. As grazing by macrofauna is limited in most of these polar regions, viruses are being recognized for their role as important agents of mortality, thereby influencing the biogeochemical cycling of nutrients that, in turn, impact community dynamics at seasonal and spatial scales. Here, we review the viral diversity in aquatic polar regions that has been discovered in the last decade, most of which has been revealed by advances in genomics-enabled technologies, and we reflect on the vast extent of the still-to-be explored polar microbial diversity and its “enigmatic virosphere„

Visualization of Viral Infection Dynamics in a Unicellular Eukaryote and Quantification of Viral Production Using Virus Fluorescence in situ Hybridization

11 pages, 7 figures, supplementary material https://www.frontiersin.org/articles/10.3389/fmicb.2020.01559/full#supplementary-material.-- All datasets generated for this study are included in the article/Supplementary MaterialOne of the major challenges in viral ecology is to assess the impact of viruses in controlling the abundance of specific hosts in the environment. To this end, techniques that enable the detection and quantification of virus-host interactions at the single-cell level are essential. With this goal in mind, we implemented virus fluorescence in situ hybridization (VirusFISH) using as a model the marine picoeukaryote Ostreococcus tauri and its virus Ostreococcus tauri virus 5 (OtV5). VirusFISH allowed the visualization and quantification of the proportion of infected cells during an infection cycle in experimental conditions. We were also able to quantify the abundance of free viruses released during cell lysis, discriminating OtV5 from other mid-level fluorescence phages in our non-axenic infected culture that were not easily distinguishable with flow cytometry. Our results showed that although the major lysis of the culture occurred between 24 and 48 h after OtV5 inoculation, some new viruses were already produced between 8 and 24 h. With this work, we demonstrate that VirusFISH is a promising technique to study specific virus-host interactions in non-axenic cultures and establish a framework for its application in complex natural communitiesYC was supported by Ministerio de Economía, Industria y Competitividad, Gobierno de España (MINECO), grant number: BES-2014-067849 during her PhD. MS was supported by Agencia Canaria de Investigación, Innovación y Sociedad de la Información (ACIISI), grant: Viera y Clavijo 2016. Ministerio de Economía, Industria y Competitividad, Gobierno de España (MINECO), grant numbers: CTM2013‐43767‐P and CTM2016‐75083‐R supported the project and paid for the investigation (reagents, material, etc.). NG was supported by Agence Nationale de la Recherche (ANR), grant number: ANR-17-CE02-0012-03.With the funding support of the ‘Severo Ochoa Centre of Excellence’ accreditation (CEX2019-000928-S), of the Spanish Research Agency (AEI)Peer reviewe

Molecular microbial ecology of Antarctic lakes

The Vestfold Hills is a coastal Antarctic oasis, a rare ice-free region containing a high density of meromictic (permanently stratified) lakes. These lakes are ideal model ecosystems as their microbial communities exist along physico-chemical gradients, allowing populations to be correlated with geochemical factors. As extensive historic, physico-chemical and biological datasets exist for Ace Lake and Organic Lake, two marine-derived meromictic lakes, they were chosen as study sites for molecular-based analysis of their microbial communities.Analysis of genetic material randomly sequenced from the environment (metagenomics) was performed to determine taxonomic composition and metabolic potential. To support metagenomic inferences, methods were developed for performing microscopy on lake water samples and for the identification of proteins from the environment (metaproteomics). Metaproteomic analysis indicated active community members and processes, while microbial/viral abundances and morphology were determined by microscopy. An integrative approach combining metagenomic, metaproteomic and physico-chemical data enabled comprehensive descriptions of the lake ecosystems. This included the identification of taxa not previously known to inhabit the lakes and determination of biogeochemical cycles.A complete genome was reconstructed of a member of the newly described virophage viral family and near complete genomes of phycodnaviruses. The virophage likely preys on phycodnaviruses that infect eucaryotic phytoflagellates. A model of virophagephycodnavirusalgae population dynamics predicted the presence of a virophage increases the frequency of algal blooms and thus overall nutrient release. Virophage signatures were detected in other aquatic environments indicating they play a previously unrecognised role in other environments. In Organic Lake, genes associated with heterotrophic bacteria involved in DMSP cleavage, photoheterotrophy, lithoheterotrophy and nitrogen remineralisation were abundant, indicating these processes are adaptations to nutrient constraints. Photo- and lithoheterotrophy enables carbon to be used for biosynthesis rather than energy generation thereby conserving carbon in the lake, while recycling of nitrogen limits its loss. DMSP apppears to be significant carbon and energy source and also the origin of high DMS concentrations in Organic Lake. These molecular-based discoveries shed light on the role of previously unrecognised taxa and metabolic processes in unique Antarctic lake environments

Rapidity of Genomic Adaptations to Prasinovirus Infection in a Marine Microalga

International audiencePrasinoviruses are large dsDNA viruses commonly found in aquatic systems worldwide, where they can infect and lyse unicellular prasinophyte algae such as Ostreococcus. Host susceptibility is virus strain-specific, but resistance of susceptible Ostreococcus tauri strains to a virulent virus arises frequently. In clonal resistant lines that re-grow, viruses are usually present for many generations, and genes clustered on chromosome 19 show physical rearrangements and differential expression. Here, we investigated changes occurring during the first two weeks after inoculation of the prasinovirus OtV5. By serial dilutions of cultures at the time of inoculation, we estimated the frequency of resistant cells arising in virus-challenged O. tauri cultures to be 10 −3-10 −4 of the inoculated population. Re-growing resistant cells were detectable by flow cytometry 3 days post-inoculation (dpi), visible re-greening of cultures occurred by 6 dpi, and karyotypic changes were visually detectable at 8 dpi. Resistant cell lines showed a modified spectrum of host-virus specificities and much lower levels of OtV5 adsorption