Effects of Viruses on Nutrient Turnover and Growth Efficiency of Noninfected Marine Bacterioplankton (original) (raw)

Middelboe M, Jorgensen NOG, Kroer N.. Effects of viruses on nutrient turnover and growth efficiency of noninfected marine bacterioplankton. Appl Environ Microbiol 62: 1991-1997

Applied and Environmental Microbiology

The effects of virus infection and lysis of a marine Vibrio sp. on C, N, and P turnover and the growth efficiency of noninfected bacterioplankton were studied in a series of dilution cultures. The cultures were enriched with various sources of organic matter and N and P. The growth of the Vibrio host and the growth of the natural bacterioplankton were measured by immunofluorescence and 4,6-diamidino-2-phenylindole staining methods, respectively. Lysis products resulting from infection of the Vibrio sp. caused an increase in metabolic activity and cell production by the noninfected bacterioplankton. In P-limited cultures, the addition of viruses increased the uptake of dissolved organic carbon by 72% and the potential alkaline phosphatase activity by 89% compared with control cultures without viruses. Our data suggest that input of available phosphorus through virus-induced Vibrio lysates occurred, which caused an increase in the bacterial nutrient uptake. The growth efficiency of noninfected bacteria was reduced in the presence of viruses compared with the control without viruses (growth efficiencies, 0.08 ؎ 0.03 and 0.24 ؎ 0.02, respectively). We suggest that the decrease in growth efficiency may be explained by an increase in bacterial energy demand associated with extracellular degradation of polymeric organic nitrogen and phosphorus in cell lysates.

Effects of viral enrichment on the mortality and growth of heterotrophic bacterioplankton

Aquatic Microbial Ecology, 1999

The direct effects of viral enrichments upon natural populations of marine viruses and bacteria were studied in seawater from Santa Monica Bay, CA. USA. Active virus concentrates, or control additions (ultrafiltered seawater or autoclaved virus concentrate) were added to 2 1 incubations of protist-free seawater, and the effects were monitored for about 3 d. At the beginning of the experiments, the virus numbers reflected the expected addition of intact virus particles as determined by transmission electron microscopy (TEM). Subsequently, the mean frequency of visibly infected bacteria [FVIB; % bacteria which were visibly infected with 5 or more virus-like particles) was greater in the enriched incubations than in the controls. In controls, the estimated percent of bacteria that were infected remained constant at about S to 10% of the total bacterial population, but with active enrichment, 10 to 35% of the total bacterial population was infected at a given time. Therefore, by increasing the concentration of active viruses in seawater incubations we were able to increase the amount of bacterial mortality attributed to virus infection. Even with the presumed increase in bacterial mortality, the net increases in bacterial abundance in the samples that were enriched with active virus concentrate were higher than those seen in the controls. The viral abundance in bottles that were enriched with the active virus concentrate was significantly higher than that in the controls in Expts 2 and 3 (p < 0.05), but by the end of the experiments, viral abundances in the enriched incubations approached control levels. In Expts 1 and 2, rates of DOP hydrolysis were higher in the samples enriched with the active virus concentrate, and may have been due to an increase in the incidence of viral lysis. However, overall analysis of DCAA, DFAA, and DOP hydrolysis were quite variable and difficult to interpret. Results indicate that viral enrichment increased the incidence of bacterial infection and consequently stimulated the growth of subpopulations of non-infected heterotrophic bacterioplankton.

Effects of virus infection on respiration rates of marine phytoplankton and microplankton communities

Marine Ecology Progress Series, 2003

The possible influence of viral infection on respiration rates in marine microbial pelagic communities was assessed by means of 3 experiments on respiration rate with viral concentrate addition on single-species cultures of Mantoniella sp. and Micromonas pusilla and another 3 on natural microplankton communities (organisms < 200 µm) from the Kattegat Sea (Åstol) and the Baltic Sea. Coastal surface seawater samples were taken during cruises of the RVs 'Ancylus' and 'Argos' during winter and spring 2000. Approximately 50 to 70 l of seawater were concentrated by ultrafiltration. The experiments were started by adding a viral particle concentrate to a container with algae or a natural microplankton community; a control container was kept free of the viral concentrate addition. Oxygen concentration determinations were carried out on each treatment and control to measure respiration rates throughout the incubation period. The in vivo chlorophyll a fluorescence was also monitored as an indication of algal infection. The rates of respiration indicated that the addition of the viral particle concentrate affected the respective metabolisms of the Mantoniella sp. and Micromonas pusilla cultures as well as natural microplankton communities. Viral infection decreased the Mantoniella sp. respiration rate (by 96%) and increased the Micromonas pusilla respiration rate (by 235%). Hence, if our results can be extrapolated to nature, then, at least in a bloom situation, the fate of primary production and carbon fluxes could be strongly modulated by viral infection. The addition of a viral particle concentrate to the microplankton community generated complex responses in terms of respiration rates, which increased (by 84%) or remained similar to the controls. Our results suggest that viral infection of microplanktonic organisms could be one of the factors significantly modifying pelagic carbon fluxes.

Virus impact on heterotrophic bacterioplankton of water reservoirs

2011

The quantitative distribution of viruses and their impact on heterotrophic bacterioplankton were studied in mesotrophic and eutrophic reservoirs of the Volga and Volga-Baltic waterway. The abundance of planktonic virus particles ranged from 9.4 × 10 6 to 120 × 10 6 ml-1 and was from 2.5 to 9 times greater than the bacterial numbers. Production of virioplankton varied from 2.1 × 10 6 to 132 × 10 6 particles (ml day)-1 and the population turnover time values were between 0.3 and 11.6 days. The maximum values of numbers and pro duction of virio and bacterioplankton were observed in the eutrophic Ivan'kovo reservoir. Distribution of the viruses in the Volga reservoirs depended to a significant degree on the number and activity of heterotrophic bacterioplankton. The infected bacteria accounted for 5.5-33.5% of the total bacterial abundance. Phages were an important factor of bacterial mortality. During July to September virus induced bacterial mortality varied between 6.1 and 40.6% (20.2% on average) of daily bacterioplankton production.

Distribution of viruses and their impact on bacterioplankton in mesotrophic and eutrophic reservoirs

2008

Spatial distribution of planktonic viral particles (virioplankton) and mortality of heterotrophic bacteria caused by viral lysis were studied in the eutrophic Ivan'kovskoe and mesotrophic Uglichskoe reservoirs (the Upper Volga). During the summer peak of phytoplankton, the number of viral particles was higher in the Ivan'kovskoe Reservoir ((55.1 ± 9.5) × 10 6 ml-1 on average) than in the Uglichskoe Reservoir ((42.9 ± 5.1) × 10 6 ml-1 on average). The ratio of viral to bacterial abundances ranged from 2.5 to 7.0. The average number of mature phages in infected heterotrophic bacteria varied from 17 to 109 particles/cell. Most of the infected bacterial cells in the Ivan'kovskoe Reservoir were rod-shaped, and, in the Uglichskoe Reservoir, they were mainly vibrio-shaped. In the Ivan'kovskoe Reservoir, from 8.3 to 22.4% of planktonic bacteria were infected by phages, suggesting phage-induced mortality of bacterioplankton equal to 10.5-34.8% (19.1% on average) of the daily bacterial production. In the Uglichskoe Reservoir, from 9.4 to 33.5% of bacteria were phage-infected, suggesting phage-induced bacterial mortality of 13.7-40.2% (23.5% on average) of the daily bacterial production. The obtained results testify to an important role of autochthonous viruses in the regulation of bacterioplankton abundance and production in the reservoirs.

Viruses as regulators of nutrient cycles in aquatic environments

2000

ABSTRACT Viruses are abundant and dynamic members of marine environments. The persistence of viral communities in aquatic systems requires the daily destruction of a significant proportion of the bacterial and phytoplankton populations. While the destruction of host cells by viruses has several implications, one of the most important effects may be the role viruses play as regulators of nutrient cycles.

Viruses in Marine Planktonic Systems

Oceanography, 1993

The last 10-15 years have seen major changes in our views of marine planktonic food webs, primarily from the realization that prokaryotic microorganisms and small eukaryotes are responsible for a significant fraction, often 50% or more, of the primary production and heterotrophic consumption of organic matter in these systems (Williams, 1981: Azam et al., 1983: Stockner and Antia, 1986: Fuhrman, 1992).

Cell Cycle Dependent Virus Production in Marine PHYTOPLANKTON1

Journal of Phycology, 2002

In this study we investigated virus production in two marine phytoplankton species and how it relates to the host's cell cycle. Phaeocystis pouchetii (Hariot) Lagerheim and Pyramimonas orientalis McFadden, Hill & Wetherby, growing synchronously in batch cultures, were infected with their respective viruses (PpV and PoV) at four different stages in the cell cycle and the production of free virus was then measured for 30 h. The virus production in P. orientalis infected with PoV depended on the time of infection, whereas no such relation was found for P. pouchetii infected with PpV. The P. orientalis cultures infected at the end of the dark period and at the beginning of the light period produced three times more virus than those infected in the middle of the light period and eight times more virus than those infected at the beginning of the dark period. The latent periods for PpV and PoV were 12-14 h and 18-20 h, respectively, and in both cases were independent of the host cell cycle. The differences in virus production may be attributed to light or cell cycle dependent regulation of host infection, metabolism, or burst size. Regardless of the mechanism, these differences may be related to differences in the ecological strategies of the hosts and their ability to form blooms.

Size-specific mortality of lake bacterioplankton by natural virus communities

Aquatic Microbial Ecology, 1998

The potential effect that viral lysis has on the cell size distribution of bacterioplankton was investigated during late summer stratification In Lake Pluhsee, Germany Size-specific bactenal mortality due to viral lysis was estimated from in s~t u s a n~p l e s by a transmission electron mici-oscopy based examination of vislbly infected cells [VIC) and In an experiment with varying concentrations of the natural virus community. In all depth layers the highest percentage of cells was found in a cell length class that was smaller for the entire bacterial comn~unity (0.3-0 6 pm) than for VIC (0.6-0.9 pm). For cells < 2 4 pm the highest frequency of VIC (FVIC) was detected in the size classes 0 6-0 9 and 0.9-1.2 pm, and the FVIC was high in the size classes 1 2-1.5 (all depth layers) and 1 5-1 8 pm (meta-and hypolimnion). The estimated mortality d u e to viral lysis In these size classes was significant with maxima of 29 to 55"o In the epilimnion, 30 to 59% in the metalimnion and 56 to 107'% in the hypolimnion In all depth layers the FVlC of bacteria < O 3 pm in length was ca 3 0 % of that averaged for the entire bacte-I-ial community, and in the expel-iment the percentage of cells <O 3 pm was highest in enclosurci w~t h high vli-a1 activity In the expenment the average cell size was smaller in enclosures with high than In that 1~1th low vil-a1 activity. The data demonstrate that being small could be a strategy of cells to reduce mortality d u e to viral lysis probably by reducing the contact rates wlth viruses. Thus, vlral l y s~s could be one of the mechanlsms keeping the cell size small in aquatic ecosystems In oxic water cells in the largest slze class (>2.4 pm) were not infected with viruses, and in enclosures with epilimnetic lake water the percentage of cells >2.4 pm was highest in enclosures w~t h highest viral abundance, suggestlng that resistance against infection favored large cells. However, In the meta-and hypolimnion the FVIC was high for cells > 2 4 pm and, since the burst size Increased with bacterial cell size, lysis of large ceUs could contribute sigi~ificantly to viral production. Also, a major portion of bioinass was found in sells > 2 4 pm. The finding that v~r a l lysis is size-specific and can affect the cell size distribution of bacteria in lake watel-has important implications for our understanding of the mechanlsms ivhich regulate bacterial production a n d nutrient cycliilg in pelagic environments