Viruses of Aquatic Ecosystems

A special issue of Viruses (ISSN 1999-4915).

Deadline for manuscript submissions: closed (31 July 2020) | Viewed by 43072

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Guest Editor
LMGE, Laboratoire “Micro-organismes: Génome et Environnement”, CNRS UMR 6023, Université Clermont Auvergne, Clermont-Ferrand, France
Interests: aquatic viral ecology; phage–prokaryote interactions; phage- vs. grazer-induced bacterial mortality; nutrient effects on bacterivory vs. bacteriolysis; viral genomics; virome
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Guest Editor
Sorbonne Universités, UPMC, Université Paris 06, CNRS, Laboratoire d’Océanographie de Villefranche (LOV), 181 Chemin du Lazaret, 06230 Villefranche-sur-Mer, France
Interests: aquatic viral ecology; effect of aerosols on microorganisms; interactions between microorganisms and metazoans
Special Issues, Collections and Topics in MDPI journals

Special Issue Information

Dear Colleagues,

As biological entities of size between macromolecules and living cells, viruses are obligatory cellular parasites. Despite the difficulties of observing nanoscale particles and the lack of evolutionary tracers such as ribosomal RNA, viruses are considered to be the largest reservoirs of the uncharacterized genetic diversity of our planet. Omnipresent in aquatic ecosystems, some contain genes encoding biological functions, whose circulation makes host populations powerful vectors of genetic exchanges in the environment. Phages are abundant in aquatic ecosystems, generally more so than cellular microbes whose activity conditions their proliferation. Their role is essential in various processes structuring the dynamics of aquatic microbial biodiversity: cell mortality, biogeochemical cycles, horizontal gene transfer, etc. Viral studies are also sources of basic scientific questions cutting across environmental sciences, such as competitive exclusion, niche expansion, etc.

Indeed, recent advances in the study of viruses in aquatic ecosystems have given rise to a growing interest in the general context of environmental sciences, as sources of novel knowledge related to the biodiversity of living things, the functioning of ecosystems, the evolution of the cellular world, and the ecosystem services to the living beings, as well as to methodological innovations. This Special Issue is designed to provide an up-to-date view of all these processes and more, related to viruses and other nanoparticles in aquatic ecosystems.

Dr. Télesphore Sime-Ngando
Dr. Markus G. Weinbauer
Guest Editors

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Published Papers (9 papers)

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Research

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17 pages, 4927 KiB  
Article
Virome Variation during Sea Star Wasting Disease Progression in Pisaster ochraceus (Asteroidea, Echinodermata)
by Ian Hewson, Citlalli A. Aquino and Christopher M. DeRito
Viruses 2020, 12(11), 1332; https://doi.org/10.3390/v12111332 - 20 Nov 2020
Cited by 16 | Viewed by 4945
Abstract
Sea star wasting disease (SSWD) is a condition that has affected asteroids for over 120 years, yet mechanistic understanding of this wasting etiology remains elusive. We investigated temporal virome variation in two Pisaster ochraceus specimens that wasted in the absence of external stimuli [...] Read more.
Sea star wasting disease (SSWD) is a condition that has affected asteroids for over 120 years, yet mechanistic understanding of this wasting etiology remains elusive. We investigated temporal virome variation in two Pisaster ochraceus specimens that wasted in the absence of external stimuli and two specimens that did not experience SSWD for the duration of our study, and compared viromes of wasting lesion margin tissues to both artificial scar margins and grossly normal tissues over time. Global assembly of all SSWD-affected tissue libraries resulted in 24 viral genome fragments represented in >1 library. Genome fragments mostly matched densoviruses and picornaviruses with fewer matching nodaviruses, and a sobemovirus. Picornavirus-like and densovirus-like genome fragments were most similar to viral genomes recovered in metagenomic study of other marine invertebrates. Read recruitment revealed only two picornavirus-like genome fragments that recruited from only SSWD-affected specimens, but neither was unique to wasting lesions. Wasting lesion margin reads recruited to a greater number of viral genotypes (i.e., richness) than did either scar tissue and grossly normal tissue reads. Taken together, these data suggest that no single viral genome fragment was associated with SSWD. Rather, wasting lesion margins may generally support viral proliferation. Full article
(This article belongs to the Special Issue Viruses of Aquatic Ecosystems)
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21 pages, 2501 KiB  
Article
Significance of Viral Activity for Regulating Heterotrophic Prokaryote Community Dynamics along a Meridional Gradient of Stratification in the Northeast Atlantic Ocean
by Kristina D. A. Mojica and Corina P. D. Brussaard
Viruses 2020, 12(11), 1293; https://doi.org/10.3390/v12111293 - 12 Nov 2020
Cited by 11 | Viewed by 3109
Abstract
How microbial populations interact influences the availability and flux of organic carbon in the ocean. Understanding how these interactions vary over broad spatial scales is therefore a fundamental aim of microbial oceanography. In this study, we assessed variations in the abundances, production, virus [...] Read more.
How microbial populations interact influences the availability and flux of organic carbon in the ocean. Understanding how these interactions vary over broad spatial scales is therefore a fundamental aim of microbial oceanography. In this study, we assessed variations in the abundances, production, virus and grazing induced mortality of heterotrophic prokaryotes during summer along a meridional gradient in stratification in the North Atlantic Ocean. Heterotrophic prokaryote abundance and activity varied with phytoplankton biomass, while the relative distribution of prokaryotic subpopulations (ratio of high nucleic acid fluorescent (HNA) and low nucleic acid fluorescent (LNA) cells) was significantly correlated to phytoplankton mortality mode (i.e., viral lysis to grazing rate ratio). Virus-mediate morality was the primary loss process regulating the heterotrophic prokaryotic communities (average 55% of the total mortality), which may be attributed to the strong top-down regulation of the bacterivorous protozoans. Host availability, encounter rate, and HNA:LNA were important factors regulating viral dynamics. Conversely, the abundance and activity of bacterivorous protozoans were largely regulated by temperature and turbulence. The ratio of total microbial mediated mortality to total available prokaryote carbon reveals that over the latitudinal gradient the heterotrophic prokaryote community gradually moved from a near steady state system regulated by high turnover in subtropical region to net heterotrophic production in the temperate region. Full article
(This article belongs to the Special Issue Viruses of Aquatic Ecosystems)
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14 pages, 981 KiB  
Article
Seasonal Regime Shift in the Viral Communities of a Permafrost Thaw Lake
by Catherine Girard, Valérie Langlois, Adrien Vigneron, Warwick F. Vincent and Alexander I. Culley
Viruses 2020, 12(11), 1204; https://doi.org/10.3390/v12111204 - 22 Oct 2020
Cited by 6 | Viewed by 3590
Abstract
Permafrost thaw lakes including thermokarst lakes and ponds are ubiquitous features of Subarctic and Arctic landscapes and are hotspots of microbial activity. Input of terrestrial organic matter into the planktonic microbial loop of these lakes may greatly amplify global greenhouse gas emissions. This [...] Read more.
Permafrost thaw lakes including thermokarst lakes and ponds are ubiquitous features of Subarctic and Arctic landscapes and are hotspots of microbial activity. Input of terrestrial organic matter into the planktonic microbial loop of these lakes may greatly amplify global greenhouse gas emissions. This microbial loop, dominated in the summer by aerobic microorganisms including phototrophs, is radically different in the winter, when metabolic processes shift to the anaerobic degradation of organic matter. Little is known about the viruses that infect these microbes, despite evidence that viruses can control microbial populations and influence biogeochemical cycling in other systems. Here, we present the results of a metagenomics-based study of viruses in the larger than 0.22 µm fraction across two seasons (summer and winter) in a permafrost thaw lake in Subarctic Canada. We uncovered 351 viral populations (vOTUs) in the surface waters of this lake, with diversity significantly greater during the summer. We also identified and characterized several phage genomes and prophages, which were mostly present in the summer. Finally, we compared the viral community of this waterbody to other habitats and found unexpected similarities with distant bog lakes in North America. Full article
(This article belongs to the Special Issue Viruses of Aquatic Ecosystems)
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22 pages, 1505 KiB  
Article
Impact of Viral Lysis on the Composition of Bacterial Communities and Dissolved Organic Matter in Deep-Sea Sediments
by Mara E. Heinrichs, Dennis A. Tebbe, Bernd Wemheuer, Jutta Niggemann and Bert Engelen
Viruses 2020, 12(9), 922; https://doi.org/10.3390/v12090922 - 22 Aug 2020
Cited by 15 | Viewed by 5169
Abstract
Viral lysis is a main mortality factor for bacteria in deep-sea sediments, leading to changing microbial community structures and the release of cellular components to the environment. Nature and fate of these compounds and the role of viruses for microbial diversity is largely [...] Read more.
Viral lysis is a main mortality factor for bacteria in deep-sea sediments, leading to changing microbial community structures and the release of cellular components to the environment. Nature and fate of these compounds and the role of viruses for microbial diversity is largely unknown. We investigated the effect of viruses on the composition of bacterial communities and the pool of dissolved organic matter (DOM) by setting up virus-induction experiments using mitomycin C with sediments from the seafloor of the Bering Sea. At the sediment surface, no substantial prophage induction was detected, while incubations from 20 cm below seafloor showed a doubling of the virus-to-cell ratio. Ultra-high resolution mass spectrometry revealed an imprint of cell lysis on the molecular composition of DOM, showing an increase of molecular formulas typical for common biomolecules. More than 50% of these compounds were removed or transformed during incubation. The remaining material potentially contributed to the pool of refractory DOM. Next generation sequencing of the bacterial communities from the induction experiment showed a stable composition over time. In contrast, in the non-treated controls the abundance of dominant taxa (e.g., Gammaproteobacteria) increased at the expense of less abundant phyla. Thus, we conclude that viral lysis was an important driver in sustaining bacterial diversity, consistent with the “killing the winner” model. Full article
(This article belongs to the Special Issue Viruses of Aquatic Ecosystems)
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19 pages, 1704 KiB  
Article
Viral Metagenomic Content Reflects Seawater Ecological Quality in the Coastal Zone
by Anastasia Tsiola, Grégoire Michoud, Stilianos Fodelianakis, Ioannis Karakassis, Georgios Kotoulas, Alexandra Pavlidou, Christina Pavloudi, Paraskevi Pitta, Nomiki Simboura, Daniele Daffonchio and Manolis Tsapakis
Viruses 2020, 12(8), 806; https://doi.org/10.3390/v12080806 - 26 Jul 2020
Cited by 10 | Viewed by 4234
Abstract
Viruses interfere with their host’s metabolism through the expression of auxiliary metabolic genes (AMGs) that, until now, are mostly studied under large physicochemical gradients. Here, we focus on coastal marine ecosystems and we sequence the viral metagenome (virome) of samples with discrete levels [...] Read more.
Viruses interfere with their host’s metabolism through the expression of auxiliary metabolic genes (AMGs) that, until now, are mostly studied under large physicochemical gradients. Here, we focus on coastal marine ecosystems and we sequence the viral metagenome (virome) of samples with discrete levels of human-driven disturbances. We aim to describe the relevance of viromics with respect to ecological quality status, defined by the classic seawater trophic index (TRIX). Neither viral (family level) nor bacterial (family level, based on 16S rRNA sequencing) community structure correlated with TRIX. AMGs involved in the Calvin and tricarboxylic acid cycles were found at stations with poor ecological quality, supporting viral lysis by modifying the host’s energy supply. AMGs involved in “non-traditional” energy-production pathways (3HP, sulfur oxidation) were found irrespective of ecological quality, highlighting the importance of recognizing the prevalent metabolic paths and their intermediate byproducts. Various AMGs explained the variability between stations with poor vs. good ecological quality. Our study confirms the pivotal role of the virome content in ecosystem functioning, acting as a “pool” of available functions that may be transferred to the hosts. Further, it suggests that AMGs could be used as an ultra-sensitive metric of energy-production pathways with relevance in the vulnerable coastal zone and its ecological quality. Full article
(This article belongs to the Special Issue Viruses of Aquatic Ecosystems)
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17 pages, 2600 KiB  
Article
Beyond Cholera: Characterization of zot-Encoding Filamentous Phages in the Marine Fish Pathogen Vibrio anguillarum
by Jesper Juel Mauritzen, Daniel Castillo, Demeng Tan, Sine Lo Svenningsen and Mathias Middelboe
Viruses 2020, 12(7), 730; https://doi.org/10.3390/v12070730 - 6 Jul 2020
Cited by 16 | Viewed by 4754
Abstract
Zonula occludens toxin (Zot) is a conserved protein in filamentous vibriophages and has been reported as a putative toxin in Vibrio cholerae. Recently, widespread distribution of zot-encoding prophages was found among marine Vibrio species, including environmental isolates. However, little is known [...] Read more.
Zonula occludens toxin (Zot) is a conserved protein in filamentous vibriophages and has been reported as a putative toxin in Vibrio cholerae. Recently, widespread distribution of zot-encoding prophages was found among marine Vibrio species, including environmental isolates. However, little is known about the dynamics of these prophages beyond V. cholerae. In this study, we characterized and quantified the zot-encoding filamentous phage VAIϕ, spontaneously induced from the fish pathogen V. anguillarum. VAIϕ contained 6117 bp encoding 11 ORFs, including ORF8pVAI, exhibiting 27%–73% amino acid identity to Inovirus Zot-like proteins. A qPCR method revealed an average of four VAIϕ genomes per host genome during host exponential growth phase, and PCR demonstrated dissemination of induced VAIϕ to other V. anguillarum strains through re-integration in non-lysogens. VAIϕ integrated into both chromosomes of V. anguillarum by recombination, causing changes in a putative ORF in the phage genome. Phylogenetic analysis of the V. anguillarum Inoviridae elements revealed mosaic genome structures related to mainly V. cholerae. Altogether, this study contributes to the understanding of Inovirus infection dynamics and mobilization of zot-like genes beyond human pathogenic vibrios, and discusses their potential role in the evolution of the fish pathogen V. anguillarum. Full article
(This article belongs to the Special Issue Viruses of Aquatic Ecosystems)
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9 pages, 1032 KiB  
Article
Indigenous versus Lessepsian Hosts: Nervous Necrosis Virus (NNV) in Eastern Mediterranean Sea Fish
by Yael Lampert, Ran Berzak, Nadav Davidovich, Arik Diamant, Nir Stern, Aviad P. Scheinin, Dan Tchernov and Danny Morick
Viruses 2020, 12(4), 430; https://doi.org/10.3390/v12040430 - 10 Apr 2020
Cited by 6 | Viewed by 3440
Abstract
Viruses are among the most abundant and diverse biological components in the marine environment. In finfish, viruses are key drivers of host diversity and population dynamics, and therefore, their effect on the marine environment is far-reaching. Viral encephalopathy and retinopathy (VER) is a [...] Read more.
Viruses are among the most abundant and diverse biological components in the marine environment. In finfish, viruses are key drivers of host diversity and population dynamics, and therefore, their effect on the marine environment is far-reaching. Viral encephalopathy and retinopathy (VER) is a disease caused by the marine nervous necrosis virus (NNV), which is recognized as one of the main infectious threats for marine aquaculture worldwide. For over 140 years, the Suez Canal has acted as a conduit for the invasion of Red Sea marine species into the Mediterranean Sea. In 2016–2017, we evaluated the prevalence of NNV in two indigenous Mediterranean species, the round sardinella (Sardinella aurita) and the white steenbras (Lithognathus mormyrus) versus two Lessepsian species, the Randall’s threadfin bream (Nemipterus randalli) and the Lessepsian lizardfish (Saurida lessepsianus). A molecular method was used to detect NNV in all four fish species tested. In N. randalli, a relatively newly established invasive species in the Mediterranean Sea, the prevalence was significantly higher than in both indigenous species. In S. lessepsianus, prevalence varied considerably between years. While the factors that influence the effective establishment of invasive species are poorly understood, we suggest that the susceptibility of a given invasive fish species to locally acquired viral pathogens such as NVV may be important, in terms of both its successful establishment in its newly adopted environment and its role as a reservoir ‘host’ in the new area. Full article
(This article belongs to the Special Issue Viruses of Aquatic Ecosystems)
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21 pages, 5426 KiB  
Article
Diversity and Host Interactions among Virulent and Temperate Baltic Sea Flavobacterium Phages
by Emelie Nilsson, Oliver W. Bayfield, Daniel Lundin, Alfred A. Antson and Karin Holmfeldt
Viruses 2020, 12(2), 158; https://doi.org/10.3390/v12020158 - 30 Jan 2020
Cited by 8 | Viewed by 3946
Abstract
Viruses in aquatic environments play a key role in microbial population dynamics and nutrient cycling. In particular, bacteria of the phylum Bacteriodetes are known to participate in recycling algal blooms. Studies of phage–host interactions involving this phylum are hence important to understand the [...] Read more.
Viruses in aquatic environments play a key role in microbial population dynamics and nutrient cycling. In particular, bacteria of the phylum Bacteriodetes are known to participate in recycling algal blooms. Studies of phage–host interactions involving this phylum are hence important to understand the processes shaping bacterial and viral communities in the ocean as well as nutrient cycling. In this study, we isolated and sequenced three strains of flavobacteria—LMO6, LMO9, LMO8—and 38 virulent phages infecting them. These phages represent 15 species, occupying three novel genera. Additionally, one temperate phage was induced from LMO6 and was found to be competent at infecting LMO9. Functions could be predicted for a limited number of phage genes, mainly representing roles in DNA replication and virus particle formation. No metabolic genes were detected. While the phages isolated on LMO8 could infect all three bacterial strains, the LMO6 and LMO9 phages could not infect LMO8. Of the phages isolated on LMO9, several showed a host-derived reduced efficiency of plating on LMO6, potentially due to differences in DNA methyltransferase genes. Overall, these phage–host systems contribute novel genetic information to our sequence databases and present valuable tools for the study of both virulent and temperate phages. Full article
(This article belongs to the Special Issue Viruses of Aquatic Ecosystems)
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Review

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31 pages, 8141 KiB  
Review
Femtoplankton: What’s New?
by Jonathan Colombet, Maxime Fuster, Hermine Billard and Télesphore Sime-Ngando
Viruses 2020, 12(8), 881; https://doi.org/10.3390/v12080881 - 12 Aug 2020
Cited by 4 | Viewed by 8191
Abstract
Since the discovery of high abundances of virus-like particles in aquatic environment, emergence of new analytical methods in microscopy and molecular biology has allowed significant advances in the characterization of the femtoplankton, i.e., floating entities filterable on a 0.2 µm pore size filter. [...] Read more.
Since the discovery of high abundances of virus-like particles in aquatic environment, emergence of new analytical methods in microscopy and molecular biology has allowed significant advances in the characterization of the femtoplankton, i.e., floating entities filterable on a 0.2 µm pore size filter. The successive evidences in the last decade (2010–2020) of high abundances of biomimetic mineral–organic particles, extracellular vesicles, CPR/DPANN (Candidate phyla radiation/Diapherotrites, Parvarchaeota, Aenigmarchaeota, Nanoarchaeota and Nanohaloarchaeota), and very recently of aster-like nanoparticles (ALNs), show that aquatic ecosystems form a huge reservoir of unidentified and overlooked femtoplankton entities. The purpose of this review is to highlight this unsuspected diversity. Herein, we focus on the origin, composition and the ecological potentials of organic femtoplankton entities. Particular emphasis is given to the most recently discovered ALNs. All the entities described are displayed in an evolutionary context along a continuum of complexity, from minerals to cell-like living entities. Full article
(This article belongs to the Special Issue Viruses of Aquatic Ecosystems)
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