Rapid Virus Production and Removal as Measured with Fluorescently Labeled Viruses as Tracers

Pelagic marine viruses have been shown to cause significant mortality of heterotrophic bacteria, cyanobacteria, and phytoplankton. It was previously demonstrated, in nearshore California waters, that viruses contributed to up to 50% of bacterial mortality, comparable to protists. However, in less productive waters, rates of virus production and removal and estimates of virus-mediated bacterial mortality have been difficult to determine. We have measured rates of virus production and removal, in nearshore and offshore California waters, by using fluorescently labeled viruses (FLV) as tracers. Our approach is mathematically similar to the isotope dilution technique, employed in the past to simultaneously measure the release and uptake of ammonia and amino acids. The results indicated overall virus removal rates in the dark ranging from 1.8 to 6.2% h⁻¹ and production rates in the dark ranging from 1.9 to 6.1% h⁻¹, corresponding to turnover times of virus populations of 1 to 2 days, even in oligotrophic offshore waters. Virus removal rates determined by the FLV tracer method were compared to rates of virus degradation, determined at the same locations by radiolabeling methods, and were similar even though the current FLV method is suitable for only dark incubations. Our results support previous findings that virus impacts on bacterial populations may be more important in some environments and less so in others. This new method can be used to determine rates of virus degradation, production, and turnover in eutrophic, mesotrophic, and oligotrophic waters and will provide important inputs for future investigations of microbial food webs.     

Viral production, decay rates, and life strategies along a trophic gradient in the North Adriatic Sea

Although the relationships between trophic conditions and viral dynamics have been widely explored in different pelagic environments, there have been few attempts at independent estimates of both viral production and decay. In this study, we investigated factors controlling the balance between viral production and decay along a trophic gradient in the north Adriatic basin, providing independent estimates of these variables and determining the relative importance of nanoflagellate grazing and viral life strategies. Increasing trophic conditions induced an increase of bacterioplankton growth rates and of the burst sizes. As a result, eutrophic waters displayed highest rates of viral production, which considerably exceeded observed rates of viral decay (up to 2.9 x 10(9) VLP liter(-1) h(-1)). Viral decay was also higher in eutrophic waters, where it accounted for ca. 40% of viral production, and dropped significantly to 1.3 to 10.7% in oligotrophic waters. These results suggest that viral production and decay rates may not necessarily be balanced in the short term, resulting in a net increase of viruses in the system. In eutrophic waters nanoflagellate grazing, dissolved-colloidal substances, and lysogenic infection were responsible together for the removal of ca. 66% of viral production versus 17% in oligotrophic waters. Our results suggest that different causative agents are primarily responsible for the removal of viruses from the water column in different trophic conditions. Factors other than those considered in the past might shed light on processes responsible for the removal and/or decay of viral particles from the water column.     

Viral Production, Decay Rates, and Life Strategies along a Trophic Gradient in the North Adriatic Sea

Although the relationships between trophic conditions and viral dynamics have been widely explored in different pelagic environments, there have been few attempts at independent estimates of both viral production and decay. In this study, we investigated factors controlling the balance between viral production and decay along a trophic gradient in the north Adriatic basin, providing independent estimates of these variables and determining the relative importance of nanoflagellate grazing and viral life strategies. Increasing trophic conditions induced an increase of bacterioplankton growth rates and of the burst sizes. As a result, eutrophic waters displayed highest rates of viral production, which considerably exceeded observed rates of viral decay (up to 2.9 × 10⁹ VLP liter⁻¹ h⁻¹). Viral decay was also higher in eutrophic waters, where it accounted for ca. 40% of viral production, and dropped significantly to 1.3 to 10.7% in oligotrophic waters. These results suggest that viral production and decay rates may not necessarily be balanced in the short term, resulting in a net increase of viruses in the system. In eutrophic waters nanoflagellate grazing, dissolved-colloidal substances, and lysogenic infection were responsible together for the removal of ca. 66% of viral production versus 17% in oligotrophic waters. Our results suggest that different causative agents are primarily responsible for the removal of viruses from the water column in different trophic conditions. Factors other than those considered in the past might shed light on processes responsible for the removal and/or decay of viral particles from the water column.     

Potential Significance of Lysogeny to Bacteriophage Production and Bacterial Mortality in Coastal Waters of the Gulf of Mexico

The potential effect that induction of lysogenic bacteria has on bacteriophage production and bacterial mortality in coastal waters was investigated, and we present estimates for the percentage of lysogenic cells in a natural aquatic bacterial community. Various concentrations of mitomycin C and exposure times to UV C radiation (UV-C) (wavelength of 254 nm) were used to induce the lytic cycle in lysogenic cells of natural communities of marine bacteria. UV-C treatment occasionally resulted in phage production, but phage production induced by UV-C was always less than that caused by the addition of mitomycin C. There was no evidence that high growth rates of bacteria resulted in lysogenic phage production. The burst size of cells induced by mitomycin C was determined by transmission electron microscopy and ranged from 11 to 45. Dividing the induced phage production by the burst size provided an estimate of the number of lysogenic bacterial cells, which ranged from 0.07 to 4.4% (average, 1.5%) of the total bacterial population. The percentages of lysogenic bacteria that were induced by mitomycin C were similar for samples collected nearshore from the pier of the Marine Science Institute (chlorophyll a, 1.6 to 2.9 (mu)g liter(sup-1)) and in relatively oligotrophic water (chlorophyll a, 0.2 to 0.9 (mu)g liter(sup-1)) collected 25 to 100 km offshore. By using a steady-state model, if all lysogenic bacteria were induced simultaneously, 0.14 to 8.8% (average, 3.0%) of the total bacterial mortality would result from induction of lysogenic cells. If mitomycin C induces all or the majority of lysogenized cells, our results imply that lysogenic phage production is generally not an important source of phage production or bacterial mortality in the coastal waters of the western Gulf of Mexico.     

Microbial controls on DMSP degradation and DMS formation in the Sargasso Sea

Bacterial degradation of dimethylsulfoniopropionate (DMSP) represents one of the main sources of the climatically–active trace gas dimethylsulfide (DMS) in the upper ocean. Short-term enrichment studies to stimulate specific pathways of DMSP degradation in oligotrophic waters from the Sargasso Sea were used to explore regulatory connections between the different bacterial DMSP degradation steps and determine potential biological controls on DMS formation in the open ocean. Experiments were conducted with surface water at the BATS station in the western North Atlantic Ocean. We added selected organic substrates (25 nmol L^?1 final concentration) to induce different steps of DMSP degradation in the microbial community, and then measured DMSP dynamics (assimilation and turnover rates), DMS yields (using ³⁵sulfur-DMSP tracer), and bacterial production rates. In most treatments, the main fate of consumed S-DMSP was excretion as a non-volatile S product. ³⁵S-DMSP tracer turnover rates (accumulation + assimilation + excretion of transformed products as DMS or others) increased upon addition of DMSP and glucose, but not acrylate, methymercaptopropionate (MMPA), methanethiol, DMS or glycine betaine. DMS yields from ³⁵S-DMSP never exceeded 16 % except in a short term DMSP enrichment, for which the yield reached 45 % (±17 %). Results show that availability of non-sulfur containing labile C sources (glucose, acrylate) decreased bacterial DMS production while stimulating bacterial heterotrophic production, and suggest an influence of bacterial sulfur demand in controlling DMS-yielding pathways. However, regulatory effects on ³⁵S-DMSP fate were not consistent across all reduced sulfur compounds (i.e., methanethiol or MMPA), and may reflect alternate roles of DMSP as a bacterial energy source and osmolyte.     

A Dilution Technique For The Direct Measurement Of Viral Production: A Comparison In Stratified And Tidally Mixed Coastal Waters

The abundance of heterotrophic bacteria and viruses, as well as rates of viral production and virus-mediated mortality, were measured in Discovery Passage and the Strait of Georgia (British Columbia, Canada) along a gradient of tidal mixing ranging from well mixed to stratified. The abundances of bacteria and viruses were approximately 10(6) and 10(7) mL(-1), respectively, independent of mixing regime. Viral production estimates, monitored by a dilution technique, demonstrated that new viruses were produced at rates of 10(6) and 10(7) mL(-1)h(-1) across the different mixing regimes. Using an estimated burst size of 50 viruses per lytic event, ca. 19 to 27% of the standing stock of bacteria at the stratified stations and 46 to 137% at the deep-mixed stations were removed by viruses. The results suggest that mixing of stratified waters during tidal exchange enhances virus-mediated bacterial lysis. Consequently, viral lysis recycled a greater proportion of the organic carbon required for bacterial growth under non-steady-state compared to steady-state conditions.     

Temporal and spatial variability in nearshore bacterioplankton communities of Lake Michigan

The spatial and temporal variability of bacterial communities were determined for the nearshore waters of Lake Michigan, an oligotrophic freshwater inland sea. A freshwater estuary and nearshore sites were compared six times during 2006 using denaturing gradient gel electrophoresis (DGGE). Bacterial composition clustered by individual site and date rather than by depth. Seven 16S rRNA gene clone libraries were constructed, yielding 2717 bacterial sequences. Spatial variability was detected among the DGGE banding patterns and supported by clone library composition. The clone libraries from deep waters and the estuary environment revealed highest overall bacterial diversity. Betaproteobacteria sequence types were the most dominant taxa, comprising 40.2–67.7% of the clone libraries. BAL 47 was the most abundant freshwater cluster of Betaproteobacteria , indicating widespread distribution of this cluster in the nearshore waters of Lake Michigan. Incertae sedis 5 and Oxalobacteraceae sequence types were prevalent in each clone library, displaying more diversity than previously described in other freshwater environments. Among the Oxalobacteraceae sequences, a globally distributed freshwater cluster was determined. The nearshore waters of Lake Michigan are a dynamic environment that experience forces similar to the coastal ocean environment and share common bacterial diversity with other freshwater habitats.     

Dual-Label Radioisotope Method for Simultaneously Measuring Bacterial Production and Metabolism in Natural Waters

Bacterial production and amino acid metabolism in aquatic systems can be estimated by simultaneous incubation of water samples with both tritiated methyl-thymidine and ¹⁴C-labeled amino acids. This dual-label method not only saves time, labor, and materials, but also allows determination of these two parameters in the same microbial subcommunity. Both organic carbon incorporation and respiration can be estimated. The results obtained with the dual-label technique are not significantly different from single-radiolabel methods over a wide range of bacterial activity. The method is particularly suitable for large-scale field programs and has been used successfully with eutrophic estuarine samples as well as with oligotrophic oceanic water. In the mesohaline portion of Chesapeake Bay, thymidine incorporation ranged seasonally from 2 to 635 pmol liter⁻¹ h⁻¹ and amino acid turnover rates ranged from 0.01 to 28.4% h⁻¹. Comparison of thymidine incorporation with amino acid turnover measurements made at a deep, midbay station in 1985 suggested a close coupling between bacterial production and amino acid metabolism during most of the year. However, production-specific amino acid turnover rates increased dramatically in deep bay waters during the spring phytoplankton bloom, indicating transient decoupling of bacterial production from metabolism. Ecological features such as this are readily detectable with the dual-label method.     

Virus Production and Lysate Recycling in Different Sub-basins of the Northern Baltic Sea

In the Gulf of Bothnia, northern Baltic Sea, a large freshwater inflow creates north-southerly gradients in physico-chemical and biological factors across the two sub-basins, the Bothnian Bay (BB) and the Bothnian Sea. In particular, the sub-basins differ in nutrient limitation (nitrogen vs. phosphorus; P). Since viruses are rich in P, and virus production is commonly connected with bacterial abundance and growth, we hypothesized that the role of viral lysis differs between the sub-basins. Thus, we examined virus production and the potential importance of lysate recycling in surface waters along a transect in the Gulf of Bothnia. Surprisingly, virus production and total P were negatively correlated. In the BB, virus production rates were double those elsewhere in the system, although bacterial abundance and production were the lowest. In the BB, virus-mediated cell lysates could account for 70-180% and 100-250% of the bacterial carbon and P demand, respectively, while only 4-15% and 8-21% at the other stations. Low concentrations of dissolved DNA (D-DNA) with a high proportion of encapsulated DNA (viruses) in the BB suggested rapid turnover and high uptake of free DNA. The correlation of D-DNA and total P indicates that D-DNA is a particularly important nutrient source in the P-limited BB. Our study demonstrates large and counterintuitive differences in virus-mediated recycling of carbon and nutrients in two basins of the Gulf of Bothnia, which differ in microbial community composition and nutrient limitation.     

Effects of Photochemical Transformations of Dissolved Organic Matter on Bacterial Metabolism and Diversity in Three Contrasting Coastal Sites in the Northwestern Mediterranean Sea during Summer

The effects of phototransformation of dissolved organic matter (DOM) on bacterial growth, production, respiration, growth efficiency, and diversity were investigated during summer in two lagoons and one oligotrophic coastal water samples from the Northwestern Mediterranean Sea, differing widely in DOM and chromophoric DOM concentrations. Exposure of 0.2-μm filtered waters to full sun radiation for 1 d resulted in small changes in optical properties and concentrations of DOM, and no changes in nitrate, nitrite, and phosphate concentrations. After exposure to sunlight or dark (control) treatments, the water samples were inoculated with the original bacterial community. Phototransformation of DOM had contrasting effects on bacterial production and respiration, depending on the water’s origin, resulting in an increase of bacterial growth efficiency for the oligotrophic coastal water sample (120%) and a decrease for the lagoon waters (20 to 40%) relative to that observed in dark treatments. We also observed that bacterial growth on DOM irradiated by full sun resulted in changes in community structure of total and metabolically active bacterial cells for the three locations studied when compared to the bacteria growing on un-irradiated DOM, and that changes were mainly caused by phototransformation of DOM by UV radiation for the eutrophic lagoon and the oligotrophic coastal water and by photosynthetically active radiation (PAR) for the mesoeutrophic lagoon. These initial results indicate that phototransformation of DOM significantly alters both bacterial metabolism and community structure in surface water for a variety of coastal ecosystems in the Mediterranean Sea. Further studies will be necessary to elucidate a more detailed appreciation of potential temporal and spatial variations of the effects measured.     

Dynamics of bacterioplankton in oligotrophic and eutrophic aquatic environments: bottom-up or top-down control?

Measurements of bacterial biomass, production and mortality have been carried out in a large range of aquatic environments, including eutrophic and oligotrophic ones. The general trends of variations of bacterial biomass, size, specific growth rate and mortality rate in all these environments are examined. The overall flux of bacterial production is taken as an index of the flux of organic matter available to bacteria, thus characterizing the richness of the environment. Bacterial biomass is roughly proportional to richness, while mean cell size increases with it. The turnover rate of biomass, as revealed either by growth or by mortality rates, appears to be fairly independent of richness.These observations are compatible with a simple resource-limited (bottom-up controlled) model of the dynamics of bacterioplankton. On the other hand, they are in contradiction with the predictions of a predator-controlled (top-down controlled) model.     

Latitudinal variation in virus-induced mortality of phytoplankton across the North Atlantic Ocean

Viral lysis of phytoplankton constrains marine primary production, food web dynamics and biogeochemical cycles in the ocean. Yet, little is known about the biogeographical distribution of viral lysis rates across the global ocean. To address this, we investigated phytoplankton group-specific viral lysis rates along a latitudinal gradient within the North Atlantic Ocean. The data show large-scale distribution patterns of different virus groups across the North Atlantic that are associated with the biogeographical distributions of their potential microbial hosts. Average virus-mediated lysis rates of the picocyanobacteria Prochlorococcus and Synechococcus were lower than those of the picoeukaryotic and nanoeukaryotic phytoplankton (that is, 0.14 per day compared with 0.19 and 0.23 per day, respectively). Total phytoplankton mortality (virus plus grazer-mediated) was comparable to the gross growth rate, demonstrating high turnover rates of phytoplankton populations. Virus-induced mortality was an important loss process at low and mid latitudes, whereas phytoplankton mortality was dominated by microzooplankton grazing at higher latitudes (>56°N). This shift from a viral-lysis-dominated to a grazing-dominated phytoplankton community was associated with a decrease in temperature and salinity, and the decrease in viral lysis rates was also associated with increased vertical mixing at higher latitudes. Ocean-climate models predict that surface warming will lead to an expansion of the stratified and oligotrophic regions of the world''s oceans. Our findings suggest that these future shifts in the regional climate of the ocean surface layer are likely to increase the contribution of viral lysis to phytoplankton mortality in the higher-latitude waters of the North Atlantic, which may potentially reduce transfer of matter and energy up the food chain and thus affect the capacity of the northern North Atlantic to act as a long-term sink for CO₂.     

Higher abundance of bacteria than of viruses in deep Mediterranean sediments

The interactions between viral abundance and bacterial density, biomass, and production were investigated along a longitudinal transect consisting of nine deep-sea stations encompassing the entire Mediterranean basin. The numbers of viruses were very low (range, 3.6 x 10(7) to 12.0 x 10(7) viruses g(-1)) and decreased eastward. The virus-to-bacterium ratio was always < 1.0, indicating that the deep-sea sediments of the Mediterranean Sea are the first example of a marine ecosystem not numerically dominated by viruses. The lowest virus numbers were found where the lowest bacterial metabolism and turnover rates and the largest cell size were observed, suggesting that bacterial doubling time might play an important role in benthic virus development.     

Evaluation of Tangential Flow Filtration for the Concentration and Separation of Bacteria and Viruses in Contrasting Marine Environments

Tangential flow filtration (TFF), which has been widely adopted to concentrate a diverse array of microbes from water, is a promising method of microbial separation or removal. However, it is essential to select an optimal membrane suitable for the specific filtration application. This study evaluated two different scales of TFF systems for concentrating and separating microbes (including bacteria and viruses) from contrasting marine waters. Among bacteria-size membranes, polyvinylidene difluoride (PVDF) membranes showed higher bacterial recovery, but lower viral permeation efficiencies than polyethersulfone (PES) membranes, regardless of environments and scales of TFF. Estuary samples showed significantly higher percentages of bacterial retention than nearshore and ocean samples. For virus-size membranes, a higher viral recovery and lower sorption was observed for regenerated cellulose membrane than PES membranes in the small-scale TFF. Similar viral recoveries were observed between PES membranes in the large-scale TFF, with higher viral concentrations being observed in estuary samples than in nearshore samples. Deep ocean samples showed the lowest recovery of viruses, which was consistent with observations of bacterial recovery. Synthetically, PVDF may be more suitable for the concentration of bacterial cells, while PES would be a better choice for the collection of viruses. When compared with the PES membrane, regenerated cellulose is better for viral concentration, while PES is recommended to obtain bacteria- and virus-free seawater.     

Light and dark uptake and loss of 14C: methodological problems with productivity measurements in oceanic waters

Measurements of the uptake and loss of ⁴C in the light and in the dark in the Tasman and Coral Seas have revealed methodological problems with the estimation of productivity in these waters. Rates of productivity estimated without replication, time series incubations and dark controls frequently overestimated the true rates of autotrophic production. The data showed unexpectedly high rates of both uptake and loss in the dark in oligotrophic waters. In oligotrophic oceanic waters, dark incorporation of ¹⁴C sometimes equalled the uptake of ¹⁴C in the light bottle. Rapid uptake of isotope in the dark controls appeared to be the result of rapid bacterial growth and metabolism. This problem was exacerbated by agitation of the sample before or during the incubation. Tropical samples were particularly susceptible to problems arising from the agitation of the samples. Latitudinal gradients of dark uptake and loss were revealed in these incubations. The loss of label during 8–12 hours in the dark (after 12 hr in the light) was as high as 50% in subtropical waters. The loss was frequently unmeasurable (< 10%) in temperate waters. The time course of ¹⁴C uptake indicated active grazing in the bottles and suggested that most of the nighttime losses of label were due to grazing by microheterotrophs. Respiratory losses appeared to be small. Calculated values of the assimilation number (or photosynthetic capacity) which did not correct for dark ¹⁴C uptake were too high to be biochemically realistic. The errors were due to the heterotrophic uptake of label and the lack of dark controls. Rapid release of ¹⁴C in the dark after incubation in the light meant that the estimate of productivity was dependant on the trophic state of the sample and on the period of incubation.     

Viral dynamics in two trophically different areas in the Central Adriatic Sea

To understand the activity of marine viruses, experiments on viral production, viral decay and the percentage of lytic and lysogenic bacterial cells among the total number of bacterial cells were carried out seasonally at two stations in the Adriatic Sea with different trophic conditions. Additionally, we are providing an insight on the enrichment with dissolved and particulate organic matter by viral lysis in the studied area. Viral production was higher at the coastal station than at the open-sea station. Viral decay rates were also higher at the coastal sea station than at the open-sea station, and accounted for approximately 40% of viral production at both investigated stations. The percentage of lysogenic infection was lower than that of lytical infection, which indicates the prevalence of the lytic cycle at both stations. Viruses had a significant influence on bacterial mortality through high daily removal of the bacterial standing stock at the coastal and open-sea station. The viruses contributed to the restoration of dissolved organic carbon, nitrogen and phosphorus in the microbial loop by lysing the bacterial cells at the studied stations. All the above suggest that viruses are important in the microbial food web and an important factor in the control of bacterial populations within the study area.     

Pyrosequencing Revealed SAR116 Clade as Dominant dddP-Containing Bacteria in Oligotrophic NW Pacific Ocean

Dimethyl sulfide (DMS) is a climatically active gas released into the atmosphere from oceans. It is produced mainly by bacterial enzymatic cleavage of dimethylsulfoniopropionate (DMSP), and six DMSP lyases have been identified to date. To determine the biogeographical distribution of bacteria relevant to DMS production, we investigated the diversity of dddP—the most abundant DMS-producing gene—in the northwestern Pacific Ocean using newly developed primers and the pyrosequencing method. Consistent with previous studies, the major dddP-containing bacteria in coastal areas were those belonging to the Roseobacter clade. However, genotypes closely related to the SAR116 group were found to represent a large portion of dddP-containing bacteria in the surface waters of the oligotrophic ocean. The addition of DMSP to a culture of the SAR116 strain Candidatus Puniceispirillum marinum IMCC1322 resulted in the production of DMS and upregulated expression of the dddP gene. Considering the large area of oligotrophic water and the wide distribution of the SAR116 group in oceans worldwide, we propose that these bacteria may play an important role in oceanic DMS production and biogeochemical sulfur cycles, especially via bacteria-mediated DMSP degradation.     

Viruses and flagellates sustain apparent richness and reduce biomass accumulation of bacterioplankton in coastal marine waters

To gain a better understanding of the interactions among bacteria, viruses and flagellates in coastal marine ecosystems, we investigated the effect of viral lysis and protistan bacterivory on bacterial abundance, production and diversity [determined by 16S rRNA gene polymerase chain reaction (PCR) and denaturing gradient gel electrophoresis (DGGE)] in three coastal marine sites with different nutrient supplies in Hong Kong. Six experiments were set up using filtration and dilution methods to develop virus, flagellate and virus+flagellate treatments for natural bacterial populations. All three predation treatments had significant repressing effects on bacterial abundance. Bacterial production was significantly repressed by flagellates and both predators (flagellates and viruses). Bacterial apparent species richness (indicated as the number of DGGE bands) was always significantly higher in the presence of viruses, flagellates and both predators than in the predator-free control. Cluster analysis of the DGGE patterns showed that the effects of viruses and flagellates on bacterial community structure were relatively stochastic while the co-effects of predators caused consistent trends (DGGE always showed the most similar patterns when compared with those of in situ environments) and substantially increased the apparent richness. Overall, we found strong evidence that viral lysis and protist bacterivory act additively to reduce bacterial production and to sustain diversity. This first systematic attempt to study the interactive effects of viruses and flagellates on the diversity and production of bacterial communities in coastal waters suggests that a tight control of bacterioplankton dominants results in relatively stable bacterioplankton communities.     

Viriobenthos Production and Virioplankton Sorptive Scavenging by Suspended Sediment Particles in Coastal and Pelagic Waters

Virus production in oxic surface sediments and virioplankton sorption to suspended particles was estimated across three stations in the Southern California region (33.4°N, 118.6°W). Viriobenthos production was estimated using a sterile sediment and filtered porewater dilution technique that targeted production from both attached bacteria and bacteria living free in the porewater, and attached bacteria alone. Potential virus production rates by bacteria free in the porewater ranged from 1.7 to 4.6 × 10⁸ VLP cm^–3 h^–1, while attached bacteria had slower potential production rates of between 0.4 and 1.1 × 10⁸ VLP cm^–3 h^–1, suggesting turnover rates of viruses in sediments (1–5 h) which are significantly higher than those of virioplankton (~24–48 h). Virioplankton adsorbed to small (<150 µm) suspended sediments at stations with high ambient suspended solid concentrations. Virioplankton scavenging rates combined with published sedimentation rates demonstrate that this mechanism of virus arrival could only account for 0.01% of daily benthic virus production. Calculated mortality rates of benthic bacteria (4–14% h^–1) suggest viruses may play an important role in sediment carbon cycling.