Seasonal variation in viral-induced mortality of bacterioplankton in the water column of a large mesotrophic lake (Lake Biwa, Japan)

Ram, Anirudh; Nishimura, Yusaku; Tomaru, Yuji; Nagasaki, Keisuke; Nagata, Toshi

doi:10.3354/ame01381

Cited by 26 publications

(19 citation statements)

References 56 publications

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“…This pattern might be attributable to the lower production of bacterioplankton in the hypolimnion, resulting in a prolonged viral lytic cycle. To support this, a previous study in Lake Biwa estimated that bacterial production was 10‐fold lower in the hypolimnion (0.4 ± 0.1 μg C l −1 d −1 ) than in the epilimnion (4.2 ± 3.2 μg C l −1 d −1 ), and the percentage of daily bacterial production lost to viruses was fourfold lower in the hypolimnion (13.6 ± 5.2%) than in the epilimnion (52.7 ± 16.2%) (Pradeep Ram et al ., ).…”

Section: Resultsmentioning

confidence: 97%

“…The epilimnion (5 m) was sampled over 3 months and the hypolimnion (65 m) was sampled over 9 months. Water temperature, dissolved oxygen concentration, and the abundances of bacteria and virus‐like particles in the study site (Supporting Information Table S1) were within the range reported from previous studies in the lake (Pradeep Ram et al ., ; Okazaki et al ., ). Notably, thermal stratification was observed from June to December and the hypolimnion was always oxygenated, with dissolved oxygen concentrations of >6.0 mg L −1 .…”

Section: Resultsmentioning

confidence: 98%

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Genome‐resolved viral and cellular metagenomes revealed potential key virus‐host interactions in a deep freshwater lake

Okazaki

Nishimura

Yoshida

et al. 2019

Environmental Microbiology

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Summary Metagenomics has dramatically expanded the known virosphere, but freshwater viral diversity and their ecological interaction with hosts remain poorly understood. Here, we conducted a metagenomic exploration of planktonic dsDNA prokaryotic viruses by sequencing both virion (<0.22 μm) and cellular (0.22–5.0 μm) fractions collected spatiotemporally from a deep freshwater lake (Lake Biwa, Japan). This simultaneously reconstructed 183 complete (i.e., circular) viral genomes and 57 bacterioplankton metagenome‐assembled genomes. Analysis of metagenomic read coverage revealed vertical partitioning of the viral community analogous to the vertically stratified bacterioplankton community. The hypolimnetic community was generally stable during stratification, but occasionally shifted abruptly, presumably due to lysogenic induction. Genes involved in assimilatory sulfate reduction were encoded in 20 (10.9%) viral genomes, including those of dominant viruses, and may aid viral propagation in sulfur‐limited freshwater systems. Hosts were predicted for 40 (21.9%) viral genomes, encompassing 10 phyla (or classes of Proteobacteria) including ubiquitous freshwater bacterioplankton lineages (e.g., Ca. Fonsibacter and Ca. Nitrosoarchaeum). Comparison with viral genomes derived from published metagenomes revealed viral phylogeographic connectivity in geographically isolated habitats. Notably, analogous to their hosts, actinobacterial viruses were among the most diverse, ubiquitous and abundant viral groups in freshwater systems, with potential high lytic activity in surface waters.

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Section: Resultsmentioning

confidence: 97%

Section: Resultsmentioning

confidence: 98%

Genome‐resolved viral and cellular metagenomes revealed potential key virus‐host interactions in a deep freshwater lake

Okazaki

Nishimura

Yoshida

et al. 2019

Environmental Microbiology

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“…A prominent feature was the significant correlation between PA and VLP, which so far has not been established in humic lakes (25,47). PA alone explained 78% of the variance in VLP, which suggested that PA is a good predictor of VLP in Lake Vassivière, as prokaryotes are known to be the main hosts for pelagic viruses (32,38). With the exception of temperature, none of the measured abiotic variables was able to explain the variations in viral parameters in Lake Vassivière (Table 3).…”

Section: Discussionmentioning

confidence: 97%

“…Recent studies have suggested that viral lytic infection contributes significantly to the bulk of prokaryotic mortality in aquatic ecosystems, and the VIC (expressed as the percentage of total prokaryotic cells) is a measure of the magnitude of this process (16,38). We used the transmission electron microscopy (TEM) method (i.e., whole-cell approach) for the determination of the VIC, which provided direct evidence of phage infection.…”

Section: Discussionmentioning

confidence: 99%

High Lytic Infection Rates but Low Abundances of Prokaryote Viruses in a Humic Lake (Vassivière, Massif Central, France)

Ram

Rasconi

Jobard

et al. 2011

Appl Environ Microbiol

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We explored the abundance and infection rates of viruses on a time series scale in the euphotic zone of the humic mesotrophic Lake Vassivière (Massif Central, France) and compared them to nonhumic lakes of contrasting trophy (i.e., the oligomesotrophic Lake Pavin and the eutrophic Lake Aydat) located in the same geographical region and sampled during the same period. In Lake Vassivière, the abundances of virus-like particles (range, 1.7 ؋ 10 10 to 2.6 ؋ 10 10 liter ؊1 ) were significantly (P < 0.001) lower than in Lakes Pavin and Aydat. The percentage of virus-infected prokaryotic cells (mean, 18.0%) was significantly higher (P < 0.001) in Vassivière than in Pavin (mean, 11.5%) and Aydat (mean, 9.7%). In Vassivière, the abundance of prokaryotes was a good predictor (r ‫؍‬ 0.78, P < 0.001) of the number of virus-like particles, while the potential grazing rate from heterotrophic nanoflagellates was positively correlated to the viral infection rate (r ‫؍‬ 0.75, P < 0.001; n ‫؍‬ 20), indicating the prevalence of cycling interactions among viruses, prokaryotes, and grazers, which is in agreement with past experiments. The absence of correlation between chlorophyll a concentrations (Chl) and viral parameters suggested that the resources for the lytic activity of viruses in Vassivière were mainly under allochthonous control, through host activity. Indeed, compilation of data obtained from several nonhumic lakes in the French Massif Central revealed that Chl was positively correlated to the abundance of virus-like particles at concentrations above 0.5 g Chl liter ؊1 and negatively at concentrations below 0.5 g Chl liter ؊1 , suggesting that phytoplankton-derived resources could force prokaryotic growth to attain a certain threshold level when the host availability is sufficient to boost the proliferation of viruses. Therefore, based on the high level of lytic infection rates in Lake Vassivière, we conclude that viruses are key agents for prokaryotic mortality and could influence the food web dynamics in humic lakes, which may ultimately depend on the internal cycling of resources and, perhaps, mainly on the allochthonous inputs and the associated humic substances.

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“…Pradeep Ram et al (2010) showed that the viral lysis was responsible, in Lake Biwa, for a loss of about 30% of the bacterial production. This value was set as 25% in our model, as 30% would not be compatible with the other constraints applied and resulted in no possible solution.…”

Section: Initial Modelmentioning

confidence: 99%

Potential role of fungi in plankton food web functioning and stability: a simulation analysis based on Lake Biwa inverse model

Niquil¹,

Kagami²,

Urabe³

et al. 2010

Hydrobiologia

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International audienceRecent investigations of molecular diversity in the plankton of lakes and coastal lagoons have detected an unexpected diversity of fungi including chytrids. Microscopic observations have provided evidence for the presence of two main forms. The sporangia are implied in algal parasitism. The propagules, i.e. uniflagellated zoospores, may constitute an alternate resource for consumers. These results suggest a need to reconsider the concept of plankton food web functioning. In order to describe the potential role of fungi in food web functioning, we revisit the model of carbon flows in the photic zone of the North basin of Lake Biwa in summer, established using the inverse analysis method for estimating missing flow values. In the absence of quantification of the flows induced by fungal activity, simulations are realised of their potential role in the plankton food web. Different rates of parasitism of micro-phytoplankton are tested, with a return of this carbon to the consumer via the consumption of zoospores by mesozooplankton and, at a lower rate, microzooplankton. The presence of this indirect pathway channelling micro-phytoplankton production to the consumers via the fungi, leads to the following trends: (i) an enhancement of the trophic efficiency index, (ii) a decrease of the ratio detritivory/herbivory, (iii) a decrease of the percentage of carbon flowing in cyclic pathways, and (iv) an increase in the relative ascendency of the system. Relative ascendency, which indicates pathways more specialised and less redundant, is related to theories linking food web patterns and stability. A high ascendency in the plankton food web (low trophic level), if connected to a food web of high redundancy at higher trophic levels (e.g. nekton food web) would fit well to the stabilising pattern called structural asymmetry, considered a stability criterion. More precise models, taking into account the species diversity of fungi and the high specificity of their parasitism on the micro-phytoplankton, would further accentuate this observation

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Seasonal variation in viral-induced mortality of bacterioplankton in the water column of a large mesotrophic lake (Lake Biwa, Japan)

Cited by 26 publications

References 56 publications

Genome‐resolved viral and cellular metagenomes revealed potential key virus‐host interactions in a deep freshwater lake

Genome‐resolved viral and cellular metagenomes revealed potential key virus‐host interactions in a deep freshwater lake

High Lytic Infection Rates but Low Abundances of Prokaryote Viruses in a Humic Lake (Vassivière, Massif Central, France)

Potential role of fungi in plankton food web functioning and stability: a simulation analysis based on Lake Biwa inverse model

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