During the PEeCE III mesocosm experiment in 2005 we investigated how the virioplankton community responded to increased levels of nutrients (N and P) and CO2. We applied a combination of flow cytometry, Pulsed Field Gel Electrophoresis and degenerated PCR primers to categorize and quantify individual viral populations, and to investigate their temporal dynamics. Species specific and degenerated primers enabled us to identify two specific large dsDNA viruses, EhV and CeV, infecting the haptophytes Emiliania huxleyi and Crysochromulina ericina, respectively. Some of the viral populations detected and enumerated by flow cytometry did not respond to altered CO2-levels, but the abundance of EhV and an unidentified dsDNA virus decreased with increasing CO2 levels. Our results thus indicate that CO2 conditions may affect the marine pelagic food web at the viral level. Our results also demonstrate that in order to unravel ecological problems as how CO2 and nutrient levels affect the relationship between marine algal viruses and their hosts, we need to continue the effort to develop molecular markers used to identify both hosts and viruses.
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.
Microbial mats are compacted, surface-associated microbial ecosystems reminiscent of the first living communities on early Earth. While often considered predominantly prokaryotic, recent findings show that both fungi and viruses are ubiquitous in microbial mats, albeit their functional roles remain unknown. Fungal research has mostly focused on terrestrial and freshwater ecosystems where fungi are known as important recyclers of organic matter, whereas viruses are exceptionally abundant and important in aquatic ecosystems. Here, viruses have shown to affect organic matter cycling and the diversity of microbial communities by facilitating horizontal gene transfer and cell lysis. We hypothesise fungi and viruses to have similar roles in microbial mats. Based on the analysis of previous research in terrestrial and aquatic ecosystems, we outline novel hypotheses proposing strong impacts of fungi and viruses on element cycling, food web structure and function in microbial mats, and outline experimental approaches for studies needed to understand these interactions.
We investigated the relationship between viruses and co-occurring bacterial communities in the Sognefjord, a deep-silled fjord in Western Norway. A combination of flow cytometry and automated ribosomal intergenic spacer analysis (ARISA) was used to assess prokaryote and viral abundances, and bacterial diversity and community composition, respectively, in depth profiles and at two different sampling seasons (November and May). With one exception, bacterial diversity did not vary between samples regardless of depth or season. The virus and prokaryote abundances as well as bacterial community composition, however, varied significantly with season and depth, suggesting a link between the Sognefjord viral community and potential bacterial host community diversity. To our knowledge, these findings provide the first description of microbial communities in the unique Sognefjord ecosystem, and in addition are in agreement with the simple model version of the 'Killing the Winner' theory (KtW), which postulates that microbial community diversity is a feature that is essentially top-down controlled by viruses, while community composition is bottom-up controlled by competition for limiting growth substrates.
P-transport through the microbial food web was investigated in a mesocosm experiment in which orthophosphate was added to oligotrophic Cretan Sea water. As non-exclusive alternatives to traditional phytoplankton–zooplankton succession, two mechanisms for P-transport have previously been proposed: a stoichiometric shift in food quality (Tunnelling); and a transport through a predatory food chain from heterotrophic bacteria, bypassing phytoplankton (Bypass). Following P-addition, particulate C:P-ratio dropped from 436 to 44 (molar) within 1 day, and egg production increased after 2 days. This confirms the hypothesized stoichiometric shift and rapid copepod response of a "Tunnelling" scenario. Bacterial abundance responded positively to P-addition on Day 1, ciliates increased after Day 5 and new egg production peaks occurred on Days 5 and 9; a succession suggesting additional Bypass transport although the response expected in heterotrophic flagellate abundance was not confirmed. A small, but statistically not significant, increase in Chl a in the 0.6- to 2-µm size fraction also suggests possible additional P-transport through a phytoplankton–zooplankton succession. On the basis of the magnitude of the stoichiometric change and the short delay in egg production response, we consider the Tunnelling mechanism to be the most likely signal initiating egg production, but a Bypass, and possibly a traditional succession, may have contributed to maintain the elevated egg production.
Abstract Viruses have long been viewed as entities possessing extremely limited metabolic capacities. Over the last decade, however, this view has been challenged, as metabolic genes have been identified in viruses possessing large genomes and virions—the synthesis of which is energetically demanding. Here, we unveil peculiar phenotypic and genomic features of Prymnesium kappa virus RF01 (PkV RF01), a giant virus of the Mimiviridae family. We found that this virus encodes an unprecedented number of proteins involved in energy metabolism, such as all four succinate dehydrogenase (SDH) subunits (A–D) as well as key enzymes in the β -oxidation pathway. The SDHA gene was transcribed upon infection, indicating that the viral SDH is actively used by the virus— potentially to modulate its host’s energy metabolism. We detected orthologous SDHA and SDHB genes in numerous genome fragments from uncultivated marine Mimiviridae viruses, which suggests that the viral SDH is widespread in oceans. PkV RF01 was less virulent compared with other cultured prymnesioviruses, a phenomenon possibly linked to the metabolic capacity of this virus and suggestive of relatively long co-evolution with its hosts. It also has a unique morphology, compared to other characterized viruses in the Mimiviridae family. Finally, we found that PkV RF01 is the only alga-infecting Mimiviridae virus encoding two aminoacyl-tRNA synthetases and enzymes corresponding to an entire base-excision repair pathway, as seen in heterotroph-infecting Mimiviridae . These Mimiviridae encoded-enzymes were found to be monophyletic and branching at the root of the eukaryotic tree of life. This placement suggests that the last common ancestor of Mimiviridae was endowed with a large, complex genome prior to the divergence of known extant eukaryotes. Importance Viruses on Earth are tremendously diverse in terms of morphology, functionality, and genomic composition. Over the last decade, the conceptual gap separating viruses and cellular life has tightened because of the detection of metabolic genes in viral genomes that express complex virus phenotypes upon infection. Here, we describe Prymnesium kappa virus RF01, a large alga-infecting virus with a unique morphology, an atypical infection profile, and an unprecedented number of genes involved in energy metabolism (such as the tricarboxylic (TCA) cycle and the β -oxidation pathway). Moreover, we show that the gene corresponding to one of these enzymes (the succinate dehydrogenase subunit A) is transcribed during infection and is widespread among marine viruses. This discovery provides evidence that a virus has the potential to actively regulate energy metabolism with its own gene.
Increasing temperatures, with pronounced effects at high latitudes, have raised questions about potential changes in species composition, as well as possible increased importance of small-celled phytoplankton in marine systems. In this study, we mapped out one of the smallest and globally most widespread primary producers, the picocyanobacterium Synechococcus, within the Atlantic inflow to the Arctic Ocean. In contrast to the general understanding that Synechococcus is almost absent in polar oceans due to low temperatures, we encountered high abundances (up to 21,000 cells mL-1) at 79 °N, and documented their presence as far north as 82.5 °N. Covering an annual cycle in 2014, we found that during autumn and winter, Synechococcus was often more abundant than picoeukaryotes, which usually dominate the picophytoplankton communities in the Arctic. Synechococcus community composition shifted from a quite high genetic diversity during the spring bloom to a clear dominance of two specific operational taxonomic units (OTUs) in autumn and winter. We observed abundances higher than 1,000 cells mL-1 in water colder than 2 °C at seven distinct stations and size-fractionation experiments demonstrated a net growth of Synechococcus at 2 °C in the absence of nano-sized grazers at certain periods of the year. Phylogenetic analysis of petB sequences demonstrated that these high latitude Synechococcus group within the previously described cold-adapted clades I and IV, but also contributed to unveil novel genetic diversity, especially within clade I.
Phaeoviruses (Phycodnaviridae) are large icosahedral viruses in the phylum Nucleocytoviricota with dsDNA genomes ranging from 160 to 560 kb, infecting multicellular brown algae (Phaeophyceae). The phaeoviral host range is broader than expected, not only infecting algae from the Ectocarpales but also from the Laminariales order. However, despite phaeoviral infections being reported globally, Norwegian kelp species have not been screened. A molecular analysis of cultured and wild samples of two economically important kelp species in Norway (Saccharina latissima and Laminaria hyperborea) revealed that phaeoviruses are recurrently present along the Norwegian coast. We found the viral prevalence in S. latissima to be significantly higher at the present time compared to four years ago. We also observed regional differences within older samples, in which infections were significantly lower in northern areas than in the south or the fjords. Moreover, up to three different viral sequences were found in the same algal individual, one of which does not belong to the Phaeovirus genus and has never been reported before. This master variant therefore represents a putative new member of an unclassified phycodnavirus genus.
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