Ecological and functional biodiversity in a marine algal-virus system: genotypes, phenotypes and their ecological significance

Coccolithoviruses are large dsDNA viruses infecting the cosmopolitan calcifying marine phytoplankton Emiliania huxleyi. Therefore they are instrumental components of algal bloom demise and thus agents contributing significantly to biogeochemical cycling in the oceans. Several coccolithovirus strains exist in culture and have been used so far to study the co-evolutionary arms-race between them and their unicellular host in naturally occurring or induced blooms in the North Atlantic Ocean and the fjords of Norway. However, little is known of their distribution in non-bloom conditions, their natural diversity in times of reduced infectivity rates, and the role of functionally important genes found in natural coccolithovirus communities. Even less is known about their genetic differences and the phenotypic consequences of these differences on their infection dynamics. Hence here a three dimensional approach was undertaken, during which the genomes of several coccolithovirus strains were analysed, their diversity in the global ocean characterised, and their phenotypic properties as seen from their infection dynamics with their host established. It was revealed that although coccolithoviruses share a common subset of core genes, they differ in a large proportion of their genomic material, as seen from the presence and/or absence of large sub-clusters of functionally unknown genes. Moreover, a gene that encodes for a phosphate scavenging mechanism (phosphate permease) was truncated from the genome of the Norwegian isolate EhV-99B1 but not from any other strain, while a gene encoding for the virulence factor sialidase was truncated only in the genomes of the English Channel strains isolated in 2001. The discovery of an additional gene that is potentially involved in the regulation of sphingosine and ceramide intermediates during the de novo virus encoded sphingolipid biosynthesis pathway was also intriguing, and the extent of gene homology to host genes (i.e. almost 13% of the analyzed genomes) highlighted the importance of horizontal gene transfer events in the co-evolution between algal hosts and their viruses. Secondly, it was established that virus competition over its resource, the host-cell, is fierce and that during host coinfection, some viruses (i.e. EhV-207) were superior to others (i.e. EhV-86) in their quicker utilisation of the host metabolic machinery and possibly shorter latency period within the infected cells. The biogeochemical and evolutionary implications of these distinct phenotypic properties are far reaching as in the environment there would be hundreds of different virus strains fighting over a few dominant hosts, with “losers” and “winners” coming and going from a particular niche, affecting the recirculation of nutrients and carbon at different rates. Finally, by community fingerprinting cococlithoviruses in the global ocean with phylogenetic markers (major capsid protein) and functional markers (serine palmitoyltransferase) it was discovered that the diversity of these viruses increase with depth, and that the 3D structure of the SPT protein (involved in the propagation of host cell death) differs among strains, dictated by a variant amino acid linker region between the two domains of the protein, LCB1 and LCB2, potentially influencing the efficiency of the virus encoded sphingolipid biosynthesis pathway. This study is an important first step in understanding the role of coccolithoviruses, their evolution, their functional characteristics, and the possible implications of the latter to biogeochemical cycling and global climate and primary production predictions. Articles: Draft genome sequence of the coccolithovirus EhV-84 / Josef I. Nissimov ... [et al.]. Standards in Genomic Sciences, v. 5 (2011), p. 1-11 and Functional inferences of environmental coccolithovirus biodiversity / Josef I. Nissimov ... [et al.]. Virologica sinica (2013), doi: 10.1007/s12250-013-3362-1 have been removed from PDF for the copyright reasons

Ecological and functional biodiversity in a marine algal-virus system: genotypes, phenotypes and their ecological significance

Coccolithoviruses are large dsDNA viruses infecting the cosmopolitan calcifying marine phytoplankton Emiliania huxleyi. Therefore they are instrumental components of algal bloom demise and thus agents contributing significantly to biogeochemical cycling in the oceans. Several coccolithovirus strains exist in culture and have been used so far to study the co-evolutionary arms-race between them and their unicellular host in naturally occurring or induced blooms in the North Atlantic Ocean and the fjords of Norway. However, little is known of their distribution in non-bloom conditions, their natural diversity in times of reduced infectivity rates, and the role of functionally important genes found in natural coccolithovirus communities. Even less is known about their genetic differences and the phenotypic consequences of these differences on their infection dynamics. Hence here a three dimensional approach was undertaken, during which the genomes of several coccolithovirus strains were analysed, their diversity in the global ocean characterised, and their phenotypic properties as seen from their infection dynamics with their host established. It was revealed that although coccolithoviruses share a common subset of core genes, they differ in a large proportion of their genomic material, as seen from the presence and/or absence of large sub-clusters of functionally unknown genes. Moreover, a gene that encodes for a phosphate scavenging mechanism (phosphate permease) was truncated from the genome of the Norwegian isolate EhV-99B1 but not from any other strain, while a gene encoding for the virulence factor sialidase was truncated only in the genomes of the English Channel strains isolated in 2001. The discovery of an additional gene that is potentially involved in the regulation of sphingosine and ceramide intermediates during the de novo virus encoded sphingolipid biosynthesis pathway was also intriguing, and the extent of gene homology to host genes (i.e. almost 13% of the analyzed genomes) highlighted the importance of horizontal gene transfer events in the co-evolution between algal hosts and their viruses. Secondly, it was established that virus competition over its resource, the host-cell, is fierce and that during host coinfection, some viruses (i.e. EhV-207) were superior to others (i.e. EhV-86) in their quicker utilisation of the host metabolic machinery and possibly shorter latency period within the infected cells. The biogeochemical and evolutionary implications of these distinct phenotypic properties are far reaching as in the environment there would be hundreds of different virus strains fighting over a few dominant hosts, with “losers” and “winners” coming and going from a particular niche, affecting the recirculation of nutrients and carbon at different rates. Finally, by community fingerprinting cococlithoviruses in the global ocean with phylogenetic markers (major capsid protein) and functional markers (serine palmitoyltransferase) it was discovered that the diversity of these viruses increase with depth, and that the 3D structure of the SPT protein (involved in the propagation of host cell death) differs among strains, dictated by a variant amino acid linker region between the two domains of the protein, LCB1 and LCB2, potentially influencing the efficiency of the virus encoded sphingolipid biosynthesis pathway. This study is an important first step in understanding the role of coccolithoviruses, their evolution, their functional characteristics, and the possible implications of the latter to biogeochemical cycling and global climate and primary production predictions. Articles: Draft genome sequence of the coccolithovirus EhV-84 / Josef I. Nissimov ... [et al.]. Standards in Genomic Sciences, v. 5 (2011), p. 1-11 and Functional inferences of environmental coccolithovirus biodiversity / Josef I. Nissimov ... [et al.]. Virologica sinica (2013), doi: 10.1007/s12250-013-3362-1 have been removed from PDF for the copyright reasons

The mutual interplay between calcification and coccolithovirus infection

© The Author(s), 2019. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Johns, C. T., Grubb, A. R., Nissimov, J. I., Natale, F., Knapp, V., Mui, A., Fredricks, H. F., Van Mooy, B. A. S., & Bidle, K. D. The mutual interplay between calcification and coccolithovirus infection. Environmental Microbiology, 21(6), (2019): 1896-1915, doi:10.1111/1462-2920.14362.Two prominent characteristics of marine coccolithophores are their secretion of coccoliths and their susceptibility to infection by coccolithoviruses (EhVs), both of which display variation among cells in culture and in natural populations. We examined the impact of calcification on infection by challenging a variety of Emiliania huxleyi strains at different calcification states with EhVs of different virulence. Reduced cellular calcification was associated with increased infection and EhV production, even though calcified cells and associated coccoliths had significantly higher adsorption coefficients than non‐calcified (naked) cells. Sialic acid glycosphingolipids, molecules thought to mediate EhV infection, were generally more abundant in calcified cells and enriched in purified, sorted coccoliths, suggesting a biochemical link between calcification and adsorption rates. In turn, viable EhVs impacted cellular calcification absent of lysis by inducing dramatic shifts in optical side scatter signals and a massive release of detached coccoliths in a subpopulation of cells, which could be triggered by resuspension of healthy, calcified host cells in an EhV‐free, ‘induced media’. Our findings show that calcification is a key component of the E. huxleyi‐EhV arms race and an aspect that is critical both to the modelling of these host–virus interactions in the ocean and interpreting their impact on the global carbon cycle.We thank Liti Haramaty for her guidance and assistance in culturing and infection experiments. This research was funded by the Gordon and Betty Moore Foundation (GBMF3301 to BVM and KDB and GBMF3789 to KDB) and the National Science Foundation (OCE‐1537951 and OCE‐1559179 to KDB)

Temperate infection in a virus–host system previously known for virulent dynamics

The blooming cosmopolitan coccolithophore Emiliania huxleyi and its viruses (EhVs) are a model for density-dependent virulent dynamics. EhVs commonly exhibit rapid viral reproduction and drive host death in high-density laboratory cultures and mesocosms that simulate blooms. Here we show that this system exhibits physiology-dependent temperate dynamics at environmentally relevant E. huxleyi host densities rather than virulent dynamics, with viruses switching from a long-term non-lethal temperate phase in healthy hosts to a lethal lytic stage as host cells become physiologically stressed. Using this system as a model for temperate infection dynamics, we present a template to diagnose temperate infection in other virus–host systems by integrating experimental, theoretical, and environmental approaches. Finding temperate dynamics in such an established virulent host–virus model system indicates that temperateness may be more pervasive than previously considered, and that the role of viruses in bloom formation and decline may be governed by host physiology rather than by host–virus densities

A communal catalogue reveals Earth's multiscale microbial diversity

Our growing awareness of the microbial world's importance and diversity contrasts starkly with our limited understanding of its fundamental structure. Despite recent advances in DNA sequencing, a lack of standardized protocols and common analytical frameworks impedes comparisons among studies, hindering the development of global inferences about microbial life on Earth. Here we present a meta-analysis of microbial community samples collected by hundreds of researchers for the Earth Microbiome Project. Coordinated protocols and new analytical methods, particularly the use of exact sequences instead of clustered operational taxonomic units, enable bacterial and archaeal ribosomal RNA gene sequences to be followed across multiple studies and allow us to explore patterns of diversity at an unprecedented scale. The result is both a reference database giving global context to DNA sequence data and a framework for incorporating data from future studies, fostering increasingly complete characterization of Earth's microbial diversity.Peer reviewe

A communal catalogue reveals Earth’s multiscale microbial diversity

Our growing awareness of the microbial world’s importance and diversity contrasts starkly with our limited understanding of its fundamental structure. Despite recent advances in DNA sequencing, a lack of standardized protocols and common analytical frameworks impedes comparisons among studies, hindering the development of global inferences about microbial life on Earth. Here we present a meta-analysis of microbial community samples collected by hundreds of researchers for the Earth Microbiome Project. Coordinated protocols and new analytical methods, particularly the use of exact sequences instead of clustered operational taxonomic units, enable bacterial and archaeal ribosomal RNA gene sequences to be followed across multiple studies and allow us to explore patterns of diversity at an unprecedented scale. The result is both a reference database giving global context to DNA sequence data and a framework for incorporating data from future studies, fostering increasingly complete characterization of Earth’s microbial diversity

Temperate infection in a virus-host system previously known for virulent dynamics.

The blooming cosmopolitan coccolithophore Emiliania huxleyi and its viruses (EhVs) are a model for density-dependent virulent dynamics. EhVs commonly exhibit rapid viral reproduction and drive host death in high-density laboratory cultures and mesocosms that simulate blooms. Here we show that this system exhibits physiology-dependent temperate dynamics at environmentally relevant E. huxleyi host densities rather than virulent dynamics, with viruses switching from a long-term non-lethal temperate phase in healthy hosts to a lethal lytic stage as host cells become physiologically stressed. Using this system as a model for temperate infection dynamics, we present a template to diagnose temperate infection in other virus-host systems by integrating experimental, theoretical, and environmental approaches. Finding temperate dynamics in such an established virulent host-virus model system indicates that temperateness may be more pervasive than previously considered, and that the role of viruses in bloom formation and decline may be governed by host physiology rather than by host-virus densities