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Viral-Induced Mortality of Prokaryotes in a Tropical Monsoonal Estuary.

ABSTRACT: Viruses are recognized as the most abundant and dynamic biological entities in the marine and estuarine environment. However, studies on the dynamics and activity of viruses in transient estuarine systems are limited. This study examines temporal and spatial variations in viral abundance (VA) and viral activity across the salinity gradient in a monsoon-driven tropical estuarine system (Cochin estuary, CE) along the southwest coast of India. Water samples were collected from five stations (with different hydrological settings) every 3 h for 24 h period during two distinct seasons, namely pre-monsoon (PRM, dry season) and monsoon (MON, wet season). Time series measurements were made for a spring and neap tidal cycle for each season at all the stations. The results showed marked spatial and seasonal variability with relatively low diel and tidal variations in VA and lytic activity. Viral activity was found to be distinct in five stations studied with the maximum activity in the mesohaline regions (salinity <20) of the estuary. This region was characterized by high VA, lytic infection and viral production, accompanied by low (BGE) and high bacterial respiration. Based on viral lytic production, lytic viruses were found to be responsible for the release of ca. 72.9 ± 58.5 ?g C L^-1d^-1 of bacterial carbon. The contribution of the viral shunt to the dissolved organic carbon (DOC) pool was higher during the dry season (PRM) than MON. Statistical analysis confirmed a significant association of viruses with the host availability and salinity. This work demonstrates the spatiotemporal distribution of viruses in a tropical estuarine ecosystem and highlights their role in microbial mortality across different salinity gradients. This study forms the first report on viral processes from a monsoon-driven tropical estuarine ecosystem.

SUBMITTER: Jasna V

PROVIDER: S-EPMC5440509 | biostudies-literature | 2017

REPOSITORIES: biostudies-literature

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Viral-Induced Mortality of Prokaryotes in a Tropical Monsoonal Estuary.

Jasna Vijayan V Parvathi Ammini A Pradeep Ram Angia Sriram AS Balachandran Kizhekkapat K KK Madhu Nikathil V NV Nair Maheswari M Jyothibabu Retnamma R Jayalakshmy K Veeraraghava KV Revichandran Chenicherry C Sime-Ngando Télesphore T

Frontiers in microbiology 20170523

Viruses are recognized as the most abundant and dynamic biological entities in the marine and estuarine environment. However, studies on the dynamics and activity of viruses in transient estuarine systems are limited. This study examines temporal and spatial variations in viral abundance (VA) and viral activity across the salinity gradient in a monsoon-driven tropical estuarine system (Cochin estuary, CE) along the southwest coast of India. Water samples were collected from five stations (with d ...[more]

PMID: 28588564

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Project description:Prokaryotes represent the largest living biomass reservoir in aquatic environments and play a crucial role in the global ocean. However, the factors that shape the abundance and potential growth rate of the ecologically distinct prokaryotic subgroups [i.e., high nucleic acid (HNA) and low nucleic acid (LNA) cells] along varying trophic conditions in the ocean remain poorly understood. This study conducted a series of modified dilution experiments to investigate how the abundance and potential growth rate of HNA and LNA prokaryotes and their regulating factors (i.e., protozoan grazing and viral lysis) change along a cross-shore nutrient gradient in the northern South China Sea. The results showed that the abundance of both HNA and LNA cells was significantly positively correlated with the abundance of heterotrophic nanoflagellates and viruses, whereas only HNA abundance exhibited a significant positive correlation with nutrient level. With a decreasing nutrient concentration, the potential growth rate of the HNA subgroup declined significantly, while that of the LNA subgroup was significantly enhanced, leading to an elevated relative potential growth rate of the LNA to HNA subgroup under decreasing nutrient levels. Furthermore, our data revealed different regulatory roles of protozoan grazing and viral lysis on the HNA and LNA subgroups, with HNA suffering higher mortality pressure from grazing than from lysis in contrast to LNA, which experienced equivalent pressures. As the nutrient levels declined, the relative contribution of lysis to the mortality of the HNA subgroup increased significantly, in contrast to the insignificant change in that of the LNA subgroup. Our results indicated the elevated role of LNA cells in the prokaryotic community and the enhanced viral lysis pressure on the total prokaryotes under oligotrophic conditions. This implies a weakened efficiency of carbon cycling within the microbial loop and enhanced viral lysis to shunt more carbon and energy flow in the future ocean, in which oligotrophication will be strengthened due to global warming.

Project description:Bacteria and archaea face continual onslaughts of rapidly diversifying viruses and plasmids. Many prokaryotes maintain adaptive immune systems known as clustered regularly interspaced short palindromic repeats (CRISPR) and CRISPR-associated genes (Cas). CRISPR-Cas systems are genomic sensors that serially acquire viral and plasmid DNA fragments (spacers) that are utilized to target and cleave matching viral and plasmid DNA in subsequent genomic invasions, offering critical immunological memory. Only 50% of sequenced bacteria possess CRISPR-Cas immunity, in contrast to over 90% of sequenced archaea. To probe why half of bacteria lack CRISPR-Cas immunity, we combined comparative genomics and mathematical modeling. Analysis of hundreds of diverse prokaryotic genomes shows that CRISPR-Cas systems are substantially more prevalent in thermophiles than in mesophiles. With sequenced bacteria disproportionately mesophilic and sequenced archaea mostly thermophilic, the presence of CRISPR-Cas appears to depend more on environmental temperature than on bacterial-archaeal taxonomy. Mutation rates are typically severalfold higher in mesophilic prokaryotes than in thermophilic prokaryotes. To quantitatively test whether accelerated viral mutation leads microbes to lose CRISPR-Cas systems, we developed a stochastic model of virus-CRISPR coevolution. The model competes CRISPR-Cas-positive (CRISPR-Cas+) prokaryotes against CRISPR-Cas-negative (CRISPR-Cas-) prokaryotes, continually weighing the antiviral benefits conferred by CRISPR-Cas immunity against its fitness costs. Tracking this cost-benefit analysis across parameter space reveals viral mutation rate thresholds beyond which CRISPR-Cas cannot provide sufficient immunity and is purged from host populations. These results offer a simple, testable viral diversity hypothesis to explain why mesophilic bacteria disproportionately lack CRISPR-Cas immunity. More generally, fundamental limits on the adaptability of biological sensors (Lamarckian evolution) are predicted.A remarkable recent discovery in microbiology is that bacteria and archaea possess systems conferring immunological memory and adaptive immunity. Clustered regularly interspaced short palindromic repeats (CRISPR) and CRISPR-associated genes (CRISPR-Cas) are genomic sensors that allow prokaryotes to acquire DNA fragments from invading viruses and plasmids. Providing immunological memory, these stored fragments destroy matching DNA in future viral and plasmid invasions. CRISPR-Cas systems also provide adaptive immunity, keeping up with mutating viruses and plasmids by continually acquiring new DNA fragments. Surprisingly, less than 50% of mesophilic bacteria, in contrast to almost 90% of thermophilic bacteria and Archaea, maintain CRISPR-Cas immunity. Using mathematical modeling, we probe this dichotomy, showing how increased viral mutation rates can explain the reduced prevalence of CRISPR-Cas systems in mesophiles. Rapidly mutating viruses outrun CRISPR-Cas immune systems, likely decreasing their prevalence in bacterial populations. Thus, viral adaptability may select against, rather than for, immune adaptability in prokaryotes.

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Dataset Information

Viral-Induced Mortality of Prokaryotes in a Tropical Monsoonal Estuary.

Publications

Viral-Induced Mortality of Prokaryotes in a Tropical Monsoonal Estuary.

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