Prevalence of Viral Frequency-Dependent Infection in Coastal Marine Prokaryotes Revealed Using Monthly Time Series Virome Analysis

Tominaga, Keiko; Ogawa-Haruki, Nana; Nishimura, Yosuke; Watai, Hiroyasu; Yamamoto, Kazuo; Ogata, Hiroyuki; Yoshida, Takashi

doi:10.1128/msystems.00931-22

Cited by 8 publications

(19 citation statements)

References 101 publications

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“…In addition, 3 of the 13 viruses encoded glycoside hydrolase GH16, a CAZyme that mainly hydrolyzes β-1,3-glucosyl linkages of β-glucan, such as laminarinase ( 47 ) (Table S7). This AMG is not present in any genomes of the isolated Polaribacter viruses ( 29 , 48 ) and previously published group 2 Bacteroidetes viruses ( 25 , 45 ).…”

Section: Resultsmentioning

confidence: 53%

“…Given our finding that CIF and HIF have different effects on the prokaryotic community structures and growth of particular prokaryotic taxa, we investigated the viruses present in the microcosm cultures. To detect viruses that explicitly increased during the experiment in each treatment, we first prepared a virome data set consisting of 9,313 non-redundant viral operational taxonomic units (vOTUs) (>10 kb), of which 465 were newly assembled in this study (Tables S3 and S4), while 8,848 were collected from the previous studies ( 25 , 45 ). We calculated the approximate particle numbers of these viruses in our microcosm samples.…”

Section: Resultsmentioning

confidence: 99%

“…To determine whether the above co-occurrence dynamics of these vOTUs and prokaryotic ASVs could be observed in the environment, we performed a correlation network analysis between them using the 17 data sets from Osaka Bay, collected monthly between 2015 and 2016 ( 25 ) (Table S9). We found a significant positive correlation in 13 cases ( r > 0.6, P < 0.01, and q < 0.05) (Table S10).…”

Section: Resultsmentioning

confidence: 99%

“…These differences would facilitate testing our hypothesis. Furthermore, we analyzed the environmental metagenomic data obtained from Osaka Bay, Japan ( 25 ), to confirm whether the prokaryotic and viral dynamics observed in our experiment occurred in the natural environment. We propose that different phytoplankton blooms lead to distinct dynamics of prokaryotic viruses and can differentially affect biogeochemical cycling.…”

Section: Introductionmentioning

confidence: 92%

“…In particular, viruses are the most abundant biological entities, and many infect marine prokaryotes ( 21 – 23 ). A theoretical study estimated that viral infection of prokaryotes contributes to 10%–20% of prokaryotic cell mortality per day ( 24 ), and a most recent study analyzing prokaryotic and viral dynamics in a coastal seawater reported that most abundant prokaryotic taxa are frequently infected in the natural environment ( 25 ). Those viral infections enable the release of their cellular compounds and metabolites into DOM pools, which can be readily taken up by other microorganisms ( 21 – 23 ).…”

Section: Introductionmentioning

confidence: 99%

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Taxonomic difference in marine bloom-forming phytoplanktonic species affects the dynamics of both bloom-responding prokaryotes and prokaryotic viruses

Takebe,

Tominaga,

Isozaki

et al. 2024

mSystems

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The production of dissolved organic matter during phytoplankton blooms and consumption by heterotrophic prokaryotes promote marine carbon biogeochemical cycling. Although prokaryotic viruses presumably affect this process, their dynamics during blooms are not fully understood. Here, we investigated the effects of taxonomic difference in bloom-forming phytoplankton on prokaryotes and their viruses. We analyzed the dynamics of coastal prokaryotic communities and viruses under the addition of dissolved intracellular fractions from taxonomically distinct phytoplankton, the diatom Chaetoceros sp. (CIF) and the raphidophycean alga Heterosigma akashiwo (HIF), using microcosm experiments. Ribosomal RNA gene amplicon and viral metagenomic analyses revealed that particular prokaryotes and prokaryotic viruses specifically increased in either CIF or HIF, indicating that taxonomic difference in bloom-forming phytoplankton promotes distinct dynamics of not only the prokaryotic community but also prokaryotic viruses. Furthermore, combining our microcosm experiments with publicly available environmental data mining, we identified both known and novel possible host-virus pairs. In particular, the growth of prokaryotes associating with phytoplanktonic organic matter, such as Bacteroidetes ( Polaribacter and NS9 marine group), Vibrio spp., and Rhodobacteriales ( Nereida and Planktomarina ), was accompanied by an increase in viruses predicted to infect Bacteroidetes, Vibrio , and Rhodobacteriales, respectively. Collectively, our findings suggest that changes in bloom-forming species can be followed by an increase in a specific group of prokaryotes and their viruses and that elucidating these tripartite relationships among specific phytoplankton, prokaryotes, and prokaryotic viruses improves our understanding of coastal biogeochemical cycling in blooms. IMPORTANCE The primary production during marine phytoplankton bloom and the consumption of the produced organic matter by heterotrophic prokaryotes significantly contribute to coastal biogeochemical cycles. While the activities of those heterotrophic prokaryotes are presumably affected by viral infection, the dynamics of their viruses during blooms are not fully understood. In this study, we experimentally demonstrated that intracellular fractions of taxonomically distinct bloom-forming phytoplankton species, the diatom Chaetoceros sp. and the raphidophycean alga Heterosigma akashiwo, promoted the growth of taxonomically different prokaryotes and prokaryotic viruses. Based on their dynamics and predicted hosts of those viruses, we succeeded in detecting already-known and novel possible host-virus pairs associating with either phytoplankton species. Altogether, we propose that the succession of bloom-forming phytoplankton would change the composition of the abundant prokaryotes, resulting in an increase in their viruses. These changes in viral composition, depending on bloom-forming species, would alter the dynamics and metabolism of prokaryotes, affecting biogeochemical cycling in blooms.

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Section: Resultsmentioning

confidence: 53%

Section: Resultsmentioning

confidence: 99%

Section: Resultsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 92%

Section: Introductionmentioning

confidence: 99%

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Taxonomic difference in marine bloom-forming phytoplanktonic species affects the dynamics of both bloom-responding prokaryotes and prokaryotic viruses

Takebe,

Tominaga,

Isozaki

et al. 2024

mSystems

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Dissecting the main factors affecting the viral abundance in a shrimp aquaculture ecosystem

Encinas-García,

Mendoza-Cano,

De la Re-Vega

et al. 2024

Regional Studies in Marine Science

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Metagenomic time series reveals a Western English Channel viral community dominated by members with strong seasonal signals

Bolaños,

Michelsen,

Temperton

2024

The ISME Journal

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Marine viruses are key players of ocean biogeochemistry, profoundly influencing microbial community ecology and evolution. Despite their importance, few studies have explored continuous inter-seasonal viral metagenomic time-series in marine environments. Viral dynamics are complex, influenced by multiple factors such as host population dynamics and environmental conditions. To disentangle the complexity of viral communities, we developed an unsupervised machine learning framework to classify viral contigs into "chronotypes" based on temporal abundance patterns. Analysing an inter-seasonal monthly time-series of surface viral metagenomes from the Western English Channel, we identified chronotypes and compared their functional and evolutionary profiles. Results revealed a consistent annual cycle with steep compositional changes from winter to summer and steadier transitions from summer to winter. Seasonal chronotypes were enriched in potential auxiliary metabolic genes of the ferrochelatases and 2OG-Fe(II) oxygenase orthologous groups compared to non-seasonal types. Chronotypes clustered into four groups based on their correlation profiles with environmental parameters, primarily driven by temperature and nutrients. Viral contigs exhibited a rapid turnover of polymorphisms, akin to Red Queen dynamics. However, within seasonal chronotypes, some sequences exhibited annual polymorphism recurrence, suggesting that a fraction of the seasonal viral populations evolve more slowly. Classification into chronotypes revealed viral genomic signatures linked to temporal patterns, likely reflecting metabolic adaptations to environmental fluctuations and host dynamics. This novel framework enables the identification of long-term trends in viral composition, environmental influences on genomic structure, and potential viral interactions.

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Prevalence of Viral Frequency-Dependent Infection in Coastal Marine Prokaryotes Revealed Using Monthly Time Series Virome Analysis

Abstract: There is little room for doubt that viral infection is prevalent among abundant marine prokaryotes regardless of their taxa or growth strategy. However, comprehensive evaluations of viral infections in natural prokaryotic communities are still technically difficult.

Cited by 8 publications

References 101 publications

Taxonomic difference in marine bloom-forming phytoplanktonic species affects the dynamics of both bloom-responding prokaryotes and prokaryotic viruses

Taxonomic difference in marine bloom-forming phytoplanktonic species affects the dynamics of both bloom-responding prokaryotes and prokaryotic viruses

Dissecting the main factors affecting the viral abundance in a shrimp aquaculture ecosystem

Metagenomic time series reveals a Western English Channel viral community dominated by members with strong seasonal signals

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