Virus-bacterium interactions in water and sediment of West African inland aquatic systems

The ecology of virioplankton in tropical aquatic ecosystems is poorly documented, and in particular, there are no references concerning African continental waters in the literature. In this study, we examined virus-bacterium interactions in the pelagic and benthic zones of seven contrasting shallow inland waters in Senegal, including one hypersaline lake. SYBR Gold-stained samples revealed that in the surface layers of the sites, the numbers of viruses were in the same range as the numbers of viruses reported previously for productive temperate systems. Despite high bacterial production rates, the percentages of visibly infected cells (as determined by transmission electron microscopy) were similar to the lowest percentages (range, 0.3 to 1.1%; mean, 0.5%) found previously at pelagic freshwater or marine sites, presumably because of the local environmental and climatic conditions. Since the percentages of lysogenic bacteria were consistently less than 8% for pelagic and benthic samples, lysogeny did not appear to be a dominant strategy for virus propagation at these sites. In the benthic samples, viruses were highly concentrated, but paradoxically, no bacteria were visibly infected. This suggests that sediment provides good conditions for virus preservation but ironically is an unfavorable environment for proliferation. In addition, given the comparable size distributions of viruses in the water and sediment samples, our results support the paradigm that aquatic viruses are ubiquitous and may have moved between the two compartments of the shallow systems examined. Overall, this study provides additional information about the relevance of viruses in tropical areas and indicates that the intensity of virus-bacterium interactions in benthic habitats may lower than the intensity in the adjacent bodies of water.     

Bacteria and viruses in the water column of tropical freshwater reservoirs

In tropical freshwater reservoirs of Sri Lanka, which are linked in an aquatic network, bacterial abundance and production as well as virus abundance, frequency of viral infection and virus production were investigated together with a set of nutrient species (Kjeldahl-N, NO3-N, total P, soluble P, PO4-P). At two characteristic seasons (wet season, dry season), samples were taken from two types of reservoirs (new upland impoundment and ancient, shallow lowland reservoir), each during 4 days at various depths of the entire water columns. Kjeldahl-N and total P were greatly elevated in the wind-mixed water body of the shallow impoundment during the dry season, whereas the deeper reservoir type exhibited no obvious seasonality. In SYBR green trade mark -stained samples, bacterial abundance showed no seasonal pattern in either reservoir type. Bacterial secondary production, however, was significantly elevated in the entire water column of the shallow impoundment under wind-mixed conditions in the dry season. Highest abundance of virus particles and elevated frequency of bacteria containing mature phages were also observed in the shallow reservoir during the dry season indicating favourable conditions for virus propagation. Data from this aquatic network show that most virus parameters, such as abundance or frequency of visibly infected cells, were positively linked to bacterial abundance and production, but also to organic nitrogen or some phosphorus species. We calculated that between 13.2% and 46.1% of the bacterial standing stocks would be subjected to virus-mediated mortality. Estimates of bacteriophage production revealed that from 10 x 10(9) up to 98 x 10(9) phages were produced per litre and day. Bacteria and viruses in the studied tropical freshwater system appear to be linked to various environmental conditions and may affect processes at the ecosystem scale.     

Infection Paradox: High Abundance but Low Impact of Freshwater Benthic Viruses

The discovery of an abundant and diverse virus community in oceans and lakes has profoundly reshaped ideas about global carbon and nutrient fluxes, food web dynamics, and maintenance of microbial biodiversity. These roles are exerted through massive viral impact on the population dynamics of heterotrophic bacterioplankton and primary producers. We took advantage of a shallow wetland system with contrasting microhabitats in close proximity to demonstrate that in marked contrast to pelagic systems, viral infection, determined directly by transmission electron microscopy, and consequently mortality of prokaryotes were surprisingly low in benthic habitats in all seasons. This was true even though free viruses were abundant throughout the year and bacterial infection and mortality rates were high in surrounding water. The habitats in which we found this pattern include sediment, decomposing plant litter, and biofilms on aquatic vegetation. Overall, we detected viruses in only 4 of a total of ~15,000 bacterial cells inspected in these three habitats; for comparison, nearly 300 of ~5,000 cells suspended in the water column were infected. The strikingly low incidence of impact of phages in the benthos may have important implications, since a major portion of microbial biodiversity and global carbon and nutrient turnover are associated with surfaces. Therefore, if failure to infect benthic bacteria is a widespread phenomenon, then the global role of viruses in controlling microbial diversity, food web dynamics, and biogeochemical cycles would be greatly diminished compared to predictions based on data from planktonic environments.     

Infection paradox: high abundance but low impact of freshwater benthic viruses

The discovery of an abundant and diverse virus community in oceans and lakes has profoundly reshaped ideas about global carbon and nutrient fluxes, food web dynamics, and maintenance of microbial biodiversity. These roles are exerted through massive viral impact on the population dynamics of heterotrophic bacterioplankton and primary producers. We took advantage of a shallow wetland system with contrasting microhabitats in close proximity to demonstrate that in marked contrast to pelagic systems, viral infection, determined directly by transmission electron microscopy, and consequently mortality of prokaryotes were surprisingly low in benthic habitats in all seasons. This was true even though free viruses were abundant throughout the year and bacterial infection and mortality rates were high in surrounding water. The habitats in which we found this pattern include sediment, decomposing plant litter, and biofilms on aquatic vegetation. Overall, we detected viruses in only 4 of a total of approximately 15,000 bacterial cells inspected in these three habitats; for comparison, nearly 300 of approximately 5,000 cells suspended in the water column were infected. The strikingly low incidence of impact of phages in the benthos may have important implications, since a major portion of microbial biodiversity and global carbon and nutrient turnover are associated with surfaces. Therefore, if failure to infect benthic bacteria is a widespread phenomenon, then the global role of viruses in controlling microbial diversity, food web dynamics, and biogeochemical cycles would be greatly diminished compared to predictions based on data from planktonic environments.     

Relationships Between Environmental Factors, Bacterial Indicators, and the Occurrence of Enteric Viruses in Estuarine Sediments

Current standards for evaluation of the public health safety of recreational and shellfish-harvesting waters are based upon bacteriological analysis, but do not include an evaluation of the number of viruses. The objective of this study was to determine the occurrence of enteric viruses in estuarine sediments and to find a relationship, if any, between the presence of viruses in seawater or sediment or both and various biological and physicochemical characteristics of the environment. Viruses were found in greater numbers in sediment than in overlying seawater on a volume basis. Several types of enteroviruses were isolated: coxsackievirus types A16, B1, and B5, echovirus type 1, and poliovirus type 2. On several occasions, viruses were isolated from sediments when overlying seawaters met bacteriological water quality standards for recreational use. Statistical analysis of the relationship between viruses in seawater or in sediment and other variables measured yielded only one significant association: the number of viruses in sediment was found to be positively correlated with the number of fecal coliforms in sediment. No other physical, chemical, or biological characteristic of seawater or sediment that was measured showed statistically significant association with viral numbers. No correlation was found between bacterial indicators and virus in the overlying waters. The data indicated that evaluation of the presence of bacteria and viruses in sediment may provide additional insight into long-term water quality conditions and that indicator bacteria in water are not reflective of the concentration of enteric viruses in marine waters.     

Relationships between environmental factors, bacterial indicators, and the occurrence of enteric viruses in estuarine sediments

Current standards for evaluation of the public health safety of recreational and shellfish-harvesting waters are based upon bacteriological analysis, but do not include an evaluation of the number of viruses. The objective of this study was to determine the occurrence of enteric viruses in estuarine sediments and to find a relationship, if any, between the presence of viruses in seawater or sediment or both and various biological and physicochemical characteristics of the environment. Viruses were found in greater numbers in sediment than in overlying seawater on a volume basis. Several types of enteroviruses were isolated: coxsackievirus types A16, B1, and B5, echovirus type 1, and poliovirus type 2. On several occasions, viruses were isolated from sediments when overlying seawaters met bacteriological water quality standards for recreational use. Statistical analysis of the relationship between viruses in seawater or in sediment and other variables measured yielded only one significant association: the number of viruses in sediment was found to be positively correlated with the number of fecal coliforms in sediment. No other physical, chemical, or biological characteristic of seawater or sediment that was measured showed statistically significant association with viral numbers. No correlation was found between bacterial indicators and virus in the overlying waters. The data indicated that evaluation of the presence of bacteria and viruses in sediment may provide additional insight into long-term water quality conditions and that indicator bacteria in water are not reflective of the concentration of enteric viruses in marine waters.     

Benthic carbon is inefficiently transferred in the food webs of two eutrophic shallow lakes

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Effects of Terrestrial Organic Matter on Aquatic Primary Production as Mediated by Pelagic–Benthic Resource Fluxes

Flows of energy and matter across habitat boundaries can be major determinants of the functioning of recipient ecosystems. It is currently debated whether terrestrial dissolved organic matter (tDOM) is a resource subsidy or a resource subtraction in recipient lakes. We present data from a long-term field experiment in which pelagic phosphorus concentration and whole-ecosystem primary production increased with increasing tDOM input, suggesting that tDOM acted primarily as a direct nutrient subsidy. Piecewise structural equation modeling supports, however, a substantial contribution of a second mechanism: colored tDOM acted also as a resource subtraction by shading benthic algae, preventing them from intercepting nutrients released across the sediment–water interface. Inhibition of benthic algae by colored tDOM thus indirectly promoted pelagic algae and whole-ecosystem primary production. We conclude that cross-ecosystem terrestrial DOM inputs can modify light and nutrient flows between aquatic habitats and alter the relative contributions of benthic and pelagic habitats to total primary production. These results are particularly relevant for shallow northern lakes, which are projected to receive increased tDOM runoff.     

Bacteriophage in polar inland waters

Bacteriophages are found wherever microbial life is present and play a significant role in aquatic ecosystems. They mediate microbial abundance, production, respiration, diversity, genetic transfer, nutrient cycling and particle size distribution. Most studies of bacteriophage ecology have been undertaken at temperate latitudes. Data on bacteriophages in polar inland waters are scant but the indications are that they play an active and dynamic role in these microbially dominated polar ecosystems. This review summarises what is presently known about polar inland bacteriophages, ranging from subglacial Antarctic lakes to glacial ecosystems in the Arctic. The review examines interactions between bacteriophages and their hosts and the abiotic and biotic variables that influence these interactions in polar inland waters. In addition, we consider the proportion of the bacteria in Arctic and Antarctic lake and glacial waters that are lysogenic and visibly infected with viruses. We assess the relevance of bacteriophages in the microbial loop in the extreme environments of Antarctic and Arctic inland waters with an emphasis on carbon cycling.     

Viruses in bottom sediments of a Mesotrophic Reservoir (Rybinsk Reservoir,Upper Volga)

The total number and morphological and size composition of viriobenthos, number of bacteria infected by viruses, and burst size, as well as virus-induced mortality, abundance, and production of bacteriobenthos, have been estimated in bottom sediments of the Rybinsk Reservoir. The total number of viriobenthos in the reservoir varies within (1.1–10.9) × 10⁹ (on average, (5.9 ± 0.6) × 10⁹) particles/cm³; the total number of virus-to-bacteria ratio ranges within 0.2–2.1 (on average 0.9 ± 0.3). A weak positive correlation is found between the abundance of benthic viruses and the abundance and production of benthic bacteria. In most surveyed parts of the reservoir, infected benthic bacteria were not found or the portion of visibly infected bacterial cells (FVIC) did not exceed 0.5% of the total abundance of bacteriobenthos (N _B). A comparatively high infection of bacteria by viruses was recorded in bottom sediments only at one deep-water station, where FVIC was 2.5 of N _B.     

Viruses in subarctic lakes and their impact on benthic and pelagic bacteria

Virus–bacterium interactions were investigated in the pelagic and benthic habitats in a set of lakes along an altitudinal gradient in the subarctic northern Sweden. Viral and bacterial abundances showed a significant variation between the lakes, with the highest benthic microbial abundances recorded in a high-altitude lake [993 m above sea level (a.s.l.)], whereas the highest pelagic microbial abundances were found in a low-altitude lake (270 m a.s.l.). In the pelagic habitat, there was also a distinct difference in microbial abundances between the summer–autumn and the winter sampling occasion. A positive relationship was noted between viruses and bacteria in both the pelagic and the benthic habitats. Visibly virus-infected bacterial cells were uncommon in the pelagic habitat and undetectable in the benthos. Both lytic and lysogenic pelagic viral production rates were undetectable or low; thus, a possible explanation for the relative high viral abundances found in the water column could be an allochthonous input of viruses or release of sediment-derived viruses. Overall, our results provide novel information about the relevance of viruses in the subarctic region and indicate that viruses play only a minor role in the nutrient and carbon cycling in the microbial communities of subarctic lakes.     

Planktonic viruses,heterotrophic bacteria,and nanoflagellates in fresh and coastal marine waters of the Kara Sea Basin (the Arctic)

In August–September 2009, the concentration of dissolved organic matter and quantitative distribution of virioplankton, bacterioplankton, and heterotrophic nanoflagellates were studied in the coastal waters of the Kara Sea, the fresh waters of the islands and the coasts of the sea, and the estuaries of the Ob’ and Yenisei rivers. A high positive correlation was observed between the abundances of viruses and bacteria. The frequency of visibly infected bacteria in marine waters ranged from 0.6 to 4.3% (an average of 1.6%); in the fresh waters of islands and coastline and in estuaries, it ranged from 0.3 to 3.9% (an average of 1.5%) and from 0.5 to 1.6% (an average of 1.1%) respectively. In most surveyed water bodies, the role of viruses in bacterioplankton mortality was considerably higher than that of heterotrophic flagellates.     

Functional Groups and Activities of Bacteria in a Highly Acidic Volcanic Mountain Stream and Lake in Patagonia,Argentina

Acidic volcanic waters are naturally occurring extreme habitats that are subject of worldwide geochemical research but have been little investigated with respect to their biology. To fill this gap, the microbial ecology of a volcanic acidic river (pH approximately equal to 0-1.6), Rio Agrio, and the recipient lake Caviahue in Patagonia, Argentina, was studied. Water and sediment samples were investigated for Fe(II), Fe(III), methane, bacterial abundances, biomass, and activities (oxygen consumption, iron oxidation and reduction). The extremely acidic river showed a strong gradient of microbial life with increasing values downstream and few signs of life near the source. Only sulfide-oxidizing and fermentative bacteria could be cultured from the upper part of Rio Agrio. However, in the lower part of the system, microbial biomass and oxygen penetration and consumption in the sediment were comparable to non-extreme aquatic habitats. To characterize similarities and differences of chemically similar natural and man-made acidic waters, our findings were compared to those from acidic mining lakes in Germany. In the lower part of the river and the lake, numbers of iron and sulfur bacteria and total biomass in sediments were comparable to those known from acidic mining lakes. Bacterial abundance in water samples was also very similar for both types of acidic water (around 10(5) mL(-1)). In contrast, Fe(II) oxidation and Fe(III) reduction potentials appeared to be lower despite higher biogenic oxygen consumption and higher photosynthetic activity at the sediment-water interface. Surprisingly, methanogenesis was detected in the presence of high sulfate concentrations in the profundal sediment of Lake Caviahue. In addition to supplementing microbiological knowledge on acidic volcanic waters, our study provides a new view of these extreme sites in the general context of aquatic habitats.     

Does virus-induced lysis contribute significantly to bacterial mortality in the oxygenated sediment layer of shallow oxbow lakes?

Despite the recognition that viruses are ubiquitous components of aquatic ecosystems, the number of studies on viral abundance and the ecological role of viruses in sediments is scarce. In this investigation, the interactions between viruses and bacteria were studied in the oxygenated silty sediment layer of a mesotrophic oxbow lake. A long-term study (13 months) and a diel study revealed that viruses are a numerically important and dynamic component of the microbial community. The abundance and decay rates ranged from 4.3 x 10(9) to 7.2 x 10(9) particles ml of wet sediment(-1) and from undetectable to 22.2 x 10(7) particles ml(-1) h(-1), respectively, and on average the values were 2 orders of magnitude higher than the values for the overlying water. In contrast to our expectations, viruses did not contribute significantly to the bacterial mortality in the sediment, since on average only 6% (range, 0 to 25%) of the bacterial secondary production was controlled by viruses. The low impact of viruses on the bacterial community may be associated with the quantitatively low viral burden that benthic bacteria have to cope with compared to the viral burden with which bacterial assemblages in the water column are confronted. The virus-to-bacterium ratio of the sediment varied between 0.9 and 3.2, compared to a range of 5.0 to 12.4 obtained for the water column. We speculate that despite high numbers of potential hosts, the possibility of encountering a host cell is limited by the physical conditions in the sediment, which is therefore not a favorable environment for viral proliferation. Our data suggest that viruses do not play an important role in the processing and transfer of bacterial carbon in the oxygenated sediment layer of the environment investigated.     

Warming shifts top-down and bottom-up control of pond food web structure and function

The effects of global and local environmental changes are transmitted through networks of interacting organisms to shape the structure of communities and the dynamics of ecosystems. We tested the impact of elevated temperature on the top-down and bottom-up forces structuring experimental freshwater pond food webs in western Canada over 16 months. Experimental warming was crossed with treatments manipulating the presence of planktivorous fish and eutrophication through enhanced nutrient supply. We found that higher temperatures produced top-heavy food webs with lower biomass of benthic and pelagic producers, equivalent biomass of zooplankton, zoobenthos and pelagic bacteria, and more pelagic viruses. Eutrophication increased the biomass of all organisms studied, while fish had cascading positive effects on periphyton, phytoplankton and bacteria, and reduced biomass of invertebrates. Surprisingly, virus biomass was reduced in the presence of fish, suggesting the possibility for complex mechanisms of top-down control of the lytic cycle. Warming reduced the effects of eutrophication on periphyton, and magnified the already strong effects of fish on phytoplankton and bacteria. Warming, fish and nutrients all increased whole-system rates of net production despite their distinct impacts on the distribution of biomass between producers and consumers, plankton and benthos, and microbes and macrobes. Our results indicate that warming exerts a host of indirect effects on aquatic food webs mediated through shifts in the magnitudes of top-down and bottom-up forcing.     

Benthic–pelagic coupling in the population dynamics of the harmful cyanobacterium Microcystis

1. In eutrophic lakes, large amounts of the cyanobacterium Microcystis may overwinter in the sediment and re‐inoculate the water column in spring. 2. We monitored changes in pelagic and benthic populations of Microcystis in Lake Volkerak, The Netherlands. In addition, sedimentation rates and the rate of recruitment from the sediment were measured using traps. These data were used to model the coupling between the benthic and pelagic populations and to calculate the contribution of overwintering benthic and pelagic populations to the magnitude of the pelagic summer bloom. 3. Changes in the benthic Microcystis population showed a time lag of 3–14 weeks compared with the pelagic population. This time lag increased with lake depth. The largest amount of benthic Microcystis was found in the deepest parts of the lake. These observations suggest horizontal transport of sedimented Microcystis from shallow to deep parts of the lake. 4. Recruitment from and sedimentation to the sediment occurred throughout the year, with highest recruitment and sedimentation rates during summer. Model simulations indicate that the absence of benthic recruitment would reduce the summer bloom by 50%. 5. In spring, the total pelagic population was three to six times smaller than the total benthic population. Yet, model simulations predict that the absence of this small overwintering pelagic population would reduce the summer bloom by more than 64%. 6. Reduction of the overwintering pelagic populations, for instance by flushing, may be a useful management strategy to suppress or at least delay summer blooms of Microcystis.     

Benthic-pelagic interactions in shallow water columns: an experimentalist's perspective

Shallow water column benthic and pelagic communities are thought to be linked by trophic relationships, through life history or ontogenetic links, and by biologically or physically-mediated resuspension or sedimentation processes. It is often confusing and sometimes misleading to focus only on benthic or only on pelagic components of aquatic food webs, even though the literature on shallow water column experiments contains few experiments that give a balanced view of these components, or interactions between components in different habitats. The rarity of balanced experiments is especially troublesome because the most common types of manipulations in shallow water column experiments (fish and nutrients) often have rapid, direct effects on both kinds of habitats, or easily recognized indirect links between the two habitats that go unevaluated. Despite a large experimental literature on pelagic and benthic foodwebs (with less on both in the same systems), there appears to be continuing uncertainty about the importance to pelagic productivity of nutrients released from resuspended sediments, the role of macrobenthos in controlling plankton, and the efficacy and interaction of trophic cascades between pelagic and benthic communities.     

Benthic–pelagic coupling: a comparison of the community structure of benthic and planktonic heterotrophic protists in shallow inlets of the southern Baltic

1. The taxonomic composition, abundance and biomass of heterotrophic protists (ciliates, heterotrophic flagellates (HF), rhizopods and actinopods) in the sediment and water column of shallow inlets of the Southern Baltic was studied under a variety of environmental conditions during 1996–1997. A shallow, highly eutrophic station and a deeper, less eutrophic station were compared.
2. Community biomass ranged from 0.12 to 0.34 μg C cm?3 in the water column and from 1.5 to 105 μg C cm?3 in the sediment. Heterotrophic protists dominated zooplankton biomass at both stations (73% and 84% mean contribution), while they were of minor importance within the zoobenthos. Expressed per unit area, benthic biomass contributed a significant part (44% and 49%) to the total heterotrophic protistan community at both stations.
3. Although the methodology for counting ciliates and HF was focussed on a high taxonomic resolution, the results reveal some general trends in the distribution of heterotrophic protists: protozooplankton biomass was dominated by flagellates (80% mean biomass contribution) at the shallow station and by ciliates (73% mean biomass contribution) at the deep station. In the benthos at both stations, ciliates were the dominant protozoans, followed by the hitherto little‐studied rhizopods (25% and 35% mean biomass contribution) and flagellates.
4. The degree of benthic–pelagic coupling differed between taxonomic groups. Benthic and pelagic communities of ciliates showed little taxonomic overlap. In contrast, many heterotrophic flagellate species were found both in the benthos and in the pelagic. These benthic–pelagic species contributed significantly to the biomass of HF in the water column. The planktonic rhizopod community consisted of a subset of those species found in the benthos.
5. The abundance of benthic and pelagic protists was positively correlated at the shallow station, but taxonomic data indicate that the direct exchange between benthic and pelagic communities was only partly responsible.     

Enumeration and biomass estimation of planktonic bacteria and viruses by transmission electron microscopy.

Bacteria and virus particles were harvested from water samples by ultracentrifugation directly onto Formvar-coated electron microscopy grids and counted in a transmission electron microscope. With this technique, we have counted and sized bacteria and viruses in marine water samples and during laboratory incubations. By X-ray microanalysis, we could determine the elemental composition and dry-matter content of individual bacteria. The dry weight/volume ratio for the bacteria was 600 fg of dry weight microns-3. The potassium content of the bacteria was normal compared with previous estimates from other bacterial assemblages; thus, this harvesting procedure did not disrupt the bacterial cells. Virus particles were, by an order of magnitude, more abundant than bacteria in marine coastal waters. During the first 5 to 7 days of incubation, the total number of viruses increased exponentially at a rate of 0.4 day-1 and thereafter declined. The high proliferation rate suggests that viral parasitism may affect mortality of bacteria in aquatic environments.     

Enumeration and biomass estimation of planktonic bacteria and viruses by transmission electron microscopy

Bacteria and virus particles were harvested from water samples by ultracentrifugation directly onto Formvar-coated electron microscopy grids and counted in a transmission electron microscope. With this technique, we have counted and sized bacteria and viruses in marine water samples and during laboratory incubations. By X-ray microanalysis, we could determine the elemental composition and dry-matter content of individual bacteria. The dry weight/volume ratio for the bacteria was 600 fg of dry weight microns-3. The potassium content of the bacteria was normal compared with previous estimates from other bacterial assemblages; thus, this harvesting procedure did not disrupt the bacterial cells. Virus particles were, by an order of magnitude, more abundant than bacteria in marine coastal waters. During the first 5 to 7 days of incubation, the total number of viruses increased exponentially at a rate of 0.4 day-1 and thereafter declined. The high proliferation rate suggests that viral parasitism may affect mortality of bacteria in aquatic environments.