Release of dissolved organic matter by photosynthesizing algae in Lake Kinneret,Israel*

The incorporation of inorganic carbon in particulate and dissolved organic matter by natural populations of photosynthesizing algae has been studied in Lake Kinneret, Israel, from August 1972 to December 1973. The release of dissolved organic material was directly related to the rates of particulate productivity. However, the percentage of extracellular release (PER) of dissolved organic compounds showed an inverse relationship with chlorophyll a concentrations. Mean PER values (for the trophogenic layer) over the experimental period were 3·7%, and were lowest during the exponential growth phase of the annual dinoflagellate bloom (mean PER = 1·9%). Highest PER were measured in deep, light-limited samples (mean = 31·7%; s.d.· 21·9%). In a dense metalimnic layer of photosynthetic sulphur bacteria (Chlorobium phaeobacterioides), PER was not as extremely high as has been reported for a similar layer in Lake Wadolek, Poland. Although the amounts of dissolved organic matter released by phytoplankton in Lake Kinneret were low, they may have significance as growth modulators and as substrates for heterotrophic organism.     

Biomass and production of phyto- and bacterio-plankton in eutrophic Lake Tystrup, Denmark

SUMMARY.

• 1 Phytoplankton primary production and biomass were compared with bacterial secondary production estimated by means of frequency of dividing cells (FDC) in eutrophic Lake Tystrup. Denmark.
• 2 In the upper part of the photic zone, bacterial secondary production constituted 12% of the carbon fixed by the phytoplankton. In vertical profiles, bacterial secondary production ranged from 7.6% (early spring) to 121% (during August) of the carbon fixed by the algae.
• 3 A close relationship was found between occurrence and activity of bacteria and algae, suggesting that released organic products are of primary importance to the bacteria.
• 4 The annual phytoplankton primary production was estimated as 227 g C m^-2 compared to 102 g C m^-2 assimilated by the bacteria, so 45% of the carbon fixed by the phytoplankton went through pelagic bacteria.

     

Extracellular release in Chlorella vulgaris culture and the role of bacteria accompanying - algae in this process.

The effect of different concentrations of nitrogen and phosphorus on extracellular release was investigated. Phosphorus induced the enhanced extracellular release of metabolites by Chlorella vulgaris. No influence of nitrogen on extracellular release was observed. In the initial stages of C. vulgaris culture the algae release was observed. In the initial stages of C. vulgaris culture the algae release compounds readily assimilated by the accompanying bacteria, hence the observed drop of percentage of extracellular release (PER) in culture medium caused by the bacteria. Both, the glycolic acid and the products of photoassimilation released to the environment in the first stages of cultivation were assimilated by the bacteria accompanying-algae at a similar rate. The ageing of C. vulgaris culture resulted in the accumulation of extracellularly released metabolites and increase of PER. These products were not assimilated by the bacteria present in the algal culture.     

Pelagic food web processes in an oligotrophic lake

Major pelagic carbon pathways, including primary production, release of extracellular products (EOC), bacterial production and zooplankton grazing were measured in oligotrophic Lake Almind (Denmark) and in enclosures (7 m³) subjected to artificial eutrophication. Simultaneous measurements at three days interval of carbon exchange rates and pools allowed the construction of carbon flow scenarios over a nineteen day experimental period.The flow of organic carbon was dominated by phytoplankton EOC release, which amounted from 44 to 58% of the net fixation of inorganic carbon. Gross bacterial production accounted for 33 to 75% of the primary production. The lower values of EOC release (44%) and bacterial production (33%) were found in the enclosures with added nutrients. The release of recently fixed photosynthetic products was the most important source of organic carbon to the bacterioplankton. Uptake of dissolved free amino acids was responsible for 52 to 62% of the gross bacterial production. Thus, amino acids constituted a significant proportion of the EOC. Zooplankton (< 50 µm) grazing on algae and bacteria accounted only for a minor proportion of the particulate production in May. Circumstantial evidence is presented that suggests the chrysophycean alga Dinobryon was the most important bacterial remover.The results clearly demonstrated EOC release and bacterial metabolism to be key processes in pelagic carbon cycling in this oligotrophic lake.     

Plankton photosynthesis, extracellular release and bacterial utilization of released dissolved organic carbon (RDOC) in lakes of different trophy

The major objective of these studies was to assess the extent of the flow of released dissolved organic carbon (RDOC) from phytoplankton to heterotrophic bacteria. The second aim was to test Nalewajko and Schindler's (1976) hypothesis that the percentage of extracellular release (PER) of RDOC by phytoplankton is higher in oligotrophic than eutrophic waters. The studies on the relationship between the bacterial assimilation of RDOC and productivity of phytoplankton in the lakes of different trophy have shown a direct correlation. It was observed that higher utilization rate of phytoplankton RDOC occurred in lakes with higher primary production. The inverse relationship between productivity of lakes, i.e. trophy of waters, and amount of RDOC or PER is closely dependent on the heterotrophic activity of bacteria in waters.     

MIXOTROPHIC ALGAE CONSTRAIN THE LOSS OF ORGANIC CARBON BY EXUDATION1

Algae of various taxonomic groups are capable of assimilating dissolved organic carbon (DOC) from their environments (mixotrophy). Recently, we reported that, with increasing biomass of mixotrophs, heterotrophic bacteria did not increase. We hypothesized that algal uptake of external DOC may outweigh their release of DOC by exudation (H1). Here, we addressed an alternative hypothesis that algae did not assimilate external DOC but constrained the release of DOC (H2). In chemostat experiments, we cultured the mixotrophic Chlamydomonas acidophila Negoro together with heterotrophic bacteria. As external substrates, we used glucose, which was potentially available for both bacteria and algae, or fructose, which was available only for bacteria. We increased the biomass of algae by the stepwise addition of phosphorus. Bacterial biomass did not increase in experiments using glucose or when fructose was offered, suggesting that mechanisms other than algal mixotrophy (H1) kept concentrations of bacteria low. Measured exudation rates (percent extracellular release, PER) of mixotrophic algae (Cd. acidophila, Chlorella protothecoides W. Krüger) were very low and ranged between 1.0% and 3.5% at low and moderately high phosphorus concentrations. In contrast, an obligately phototrophic alga (Chlamydomonas segnis H. Ettl) showed higher exudation rates, particularly under phosphorus limitation (70%). The results support H2. If mixotrophy is considered as a mechanism to recycle organic exudates from near the cell surface, this would explain why algae retained mixotrophic capabilities although they cannot compete with bacteria for external organic carbon.     

Littoral-pelagial interchange and the decomposition of dissolved organic matter in a polyhumic lake

The small, polyhumic lake, Mekkojärvi (southern Finland), is bordered by a moss vegetation zone (Warnstorfia and Sphagnum species) which provides a habitat-rich and productive environment for many planktonic and periphytic animals. Impacts of moss on the metabolism of bacterioplankton, phytoplankton and zooplankton in polyhumic water were investigated in laboratory throughflow systems. Growing Warnstorfia (together with epiphytic algae and bacteria) suppressed the production of planktonic algae but had no clear effect on leucine uptake, and hence bacterial production, or on the decomposition of humic substances. Phenol uptake and mineralization rates, however, were lower in the littoral water than in the pelagial water. Excretion of organic carbon by Warnstorfia algae or Daphnia longispina (the predominant crustacean in the pelagial water) provided only a minor contribution to bacterial production; therefore, a major contribution had to be from humic substances. A bacterial production efficiency of 31–38% could account for the microbial respiration in the water. The results indicated that bacterial, or detrital matter (originating largely from the littoral zone), could not obviate the need for algal food, and that a great deal of particulate matter in the water was poor or useless food for Daphnia. In all, the bulk of dissolved organic matter in Lake Mekkojärvi was biochemically highly recalcitrant. Our results indicate that humic substances (from watershed or littoral area) which, through bacterial degradation, enter the planktonic food web of the lake are mainly lost through respiration by microorganisms.     

A microcosm study of nitrogen utilization in the Great Salt Lake,Utah

Microcosms were used to study the effects of two inorganic nitrogen sources (ammonia and nitrate) and two organic nitrogen sources (urea and glutamic acid) on the growth of algae and bacteria found in the Great Salt Lake, Utah. Ammonia, nitrate and urea stimulated bacterial growth indirectly through increased algal production of unknown organic substances. Glutamic acid, representing readily available organic carbon and nitrogen, stimulated the bacteria directly. No nitrification was observed in the microcosms although nitrite was found when the microcosms were supplemented with nitrate. Lake sediment contained a number of anaerobic bacteria producing hydrogen sulfide, methane and other gases. Production of these gases was stimulated in the columns with high algal and bacterial activity.     

Underwater light penetration,phytoplankton biomass and photosynthetic activity in Lake Xolotlán (Managua)

We measured underwater light penetration, phytoplankton biomass and photosynthetic activity during three years (1987–1990) in Lake Xolotlán (L. Managua), Nicaragua. Phytoplankton biomass governed the light climate of the photic zone, but as biomass also was composed of a varying proportion of dead algae, light availability for the potential biomass of actively photosynthesizing algae (170 mg Chl-a.m^–2) was reduced. The concentration of chlorophyll-a within the photic zone was thus lower and ranged between 58 and 141 mg Chl-a.m^–2. Still, photosynthetic activity was high (2,162 mg 02.m-2.h^–1) due to an extremely high specific rate of photosynthesis; light was the only factor that limited growth. As also other conditions in Lake Xolotlán, beside light limitation, met with the requirements of the models that have been used to analyse production and photosynthetic characteristics in tropical lakes there was a striking agreement between observed and predicted values.     

Phytoplankton and bacterioplankton production in a reed-covered water body

Between 1996 and 1998 phytoplanktonic primary production and bacterioplankton production were measured monthly at five sampling stations in the lower Kis-Balaton reservoir. The open water area of the reservoir was rich in phytoplankton and had hypertrophic characteristics, but inside the reed stand (80% of the surface area) phytoplankton biomass and production were substantially (30–50 times) lower. The algal removal efficiency of the lower Kis-Balaton reservoir was 96%. The reservoir had a considerably smaller effect on bacterioplankton removal than on the phytoplankton. The decrease of biomass and production of bacterioplankton in the through-flowing water was approximately 60%. Inside the reed stand the biomass and the production of planktonic bacteria exceeded that of the phytoplankton by several times, suggesting that the release of biodegradable dissolved organic (humic) substances from macrophytes stimulated the metabolism of bacterioplankton. The significant reduction of phytoplankton inside the dense reed stand was primarily the result of the shading effect of the reeds. In the open water area a shading experiment demonstrated that a 1-week residence period for planktonic algae in the reed-covered area was sufficient for their complete elimination. The decomposition of planktonic algae, reed material and the lack of primary production inside the reed stand created oxygen-deficient and phosphorus-rich conditions during the vegetative period. These results suggest that reed-covered water bodies can effectively retain suspended solids and planktonic algae, but because of decomposition processes they cannot retain biologically-available phosphorus.     

Aerobic Organic Carbon Mineralization by Sulfate-Reducing Bacteria in the Oxygen-Saturated Photic Zone of a Hypersaline Microbial Mat

The sulfate-reducing bacterium strain SRB D2 isolated from the photic zone of a hypersaline microbial mat, from Lake Chiprana, NE Spain, respired pyruvate, alanine, and α-ketoglutarate but not formate, lactate, malate, succinate, and serine at significant rates under fully oxic conditions. Dehydrogenase enzymes of only the former substrates are likely oxygen-tolerant as all substrates supported anaerobic sulfate reduction. No indications were found, however, that aerobic respiration supported growth. Although strain SRB D2 appeared phylogenetically closely related to the oxygen-tolerant sulfate-reducing bacterium Desulfovibrio oxyclinae, substrate spectra were markedly different. Most-probable-number (MPN) estimates of sulfate-reducing bacteria and aerobic heterotrophic bacteria indicated that the latter were numerically dominant in both the photic and aphotic zones of the mat. Moreover, substrate spectra of representative isolates showed that the aerobic heterotrophic bacteria are metabolically more diverse. These findings indicate that sulfate-reducing bacteria in the fully oxic photic zone of mats have to compete with aerobic heterotrophic bacteria for organic substrates. Porewater analysis revealed that total carbohydrates and low-molecular-weight carbon compounds (LMWC) made up substantial fractions of the total dissolved organic carbon (DOC) pool and that nighttime degradation of the former was concomitant with increased concentration of the latter. Our findings indicate that aerobic respiration by sulfate-reducing bacteria contributes to organic carbon mineralization in the oxic zone of microbial mats as daytime porewater LMWC concentrations are above typical half-saturation constants.     

Productivity and species composition of algal mat communities exposed to a fluctuating thermal regime

Algal mat communities growing in thermal effluents of production nuclear reactors at the Savannah River Plant, near Aiken, SC, are exposed to large temperature fluctuations resulting from reactor operations. Rates of primary production and species composition were monitored at 4 sites along a thermal gradient in a trough microcosm to determine how these large temperature fluctuations affected productivity and algal community structure. Blue-green algae (cyanobacteria) were the only phototrophic primary producers growing in water above 45°C. These thermophiles were able to survive and apparently adapt to ambient temperatures when the reactor was shut down. The algal mat communities exposed to <45°C were composed of blue-green and eukaryotic algae that adapted rapidly to ambient temperatures. An increase in the percentage extracellular release (PER) of¹⁴C-labeled dissolved organic compounds and a decrease in primary production were observed during periods of thermal fluctuation. The results show that the dominant phototrophs in this artificially heated aquatic habitat have been selected for their ability to survive large temperature fluctuations and are similar to those of natural hot springs.This paper was prepared in connection with work under Contract No. DE-AC09-76SR00001 with the U.S. Department of Energy.     

The estimation of extracellular release by phytoplankton and heterotrophic activity of aquatic bacteria.

The actual extracellular release of organic matter by algae was determined in water samples in which the heterotrophic activity of bacteria was inhibited by gentamycin. Gentamycin rapidly and efficiently inhibited the activity of aquatic bacteria without affecting phytoplankton metabolism. Aquatic bacteria utilized the products of algal extracellular release. The amount of algal photosynthetic products metabolized by bacteria can be taken as a measure of their heterotrophic activity in waters.     

Identification of acetate-utilizing Bacteria and Archaea in methanogenic profundal sediments of Lake Kinneret (Israel) by stable isotope probing of rRNA

Acetate is an important intermediate in the decomposition of organic matter in anoxic freshwater sediments. Here, we identified distinct microorganisms active in its oxidation and transformation to methane in the anoxic methanogenic layers of Lake Kinneret (Israel) profundal sediment by rRNA-based stable isotope probing (RNA-SIP). After 18 days of incubation with amended [U-(13)C]acetate we found that archaeal 16S rRNA was (13)C-labelled to a far greater extent than bacterial rRNA. We identified acetoclastic methanogens related to Methanosaeta concilii as being most active in the degradation and assimilation of acetate. Oxidation of the acetate-methyl group played only a minor role, but nevertheless 'heavy'(13)C-labelled bacterial rRNA templates were identified. 'Heavy' bacteria were mainly affiliated with the Betaproteobacteria (mostly Rhodocyclales and Nitrosomonadales), the Nitrospira phylum (related to 'Magnetobacterium bavaricum' and Thermodesulfovibrio yellowstonii), and also with the candidate phylum 'Endomicrobia'. However, the mode of energy gain that allowed for the assimilation of (13)C-acetate by these bacterial groups remains unknown. It may have involved syntrophic oxidation of acetate, reduction of chlorinated compounds, reduction of humic substances, fermentation of organic compounds, or even predation of (13)C-labelled Methanosaeta spp. In summary, this SIP experiment shows that acetate carbon was predominantly consumed by acetoclastic methanogens in profundal Lake Kinneret sediment, while it was also utilized by a small and heterogeneous community of bacteria.     

Dissolved primary production and the strength of phytoplankton- bacterioplankton coupling in contrasting marine regions

We analyzed the strength of phytoplankton–bacterioplankton coupling by comparing the rate of particulate (PPP) and dissolved primary production (DPP) with bacterial carbon demand (BCD) in four contrasting marine regions: offshore and coastal waters of the Southern Ocean, a coastal area of the NE Atlantic, and a coastal–offshore transect in the NW Mediterranean. We measured bacterial heterotrophic production (BHP) and estimated BCD from a literature model. Average phytoplanktonic percent extracellular release [PER = DPP/(DPP + PPP)] was 18–20% in the Antarctic (offshore and coastal, respectively), 16% in the NW Mediterranean, and 7% in the NE Atlantic. A significant inverse relationship was found between PER and total system productivity with pooled data. On average BHP amounted to <5% of total primary production in all regions. However, the strength of phytoplankton–bacterioplankton coupling, estimated as the potential importance of DPP in meeting BCD, differed greatly in the four regions. DPP was highly correlated to BCD in offshore Antarctic waters and was sufficient to meet BCD. In contrast, BCD exceeded DPP and bore no significant relationship in the remaining regions. The data suggest that a strong dependence of bacteria on algal extracellular production is only expected in open-ocean environments isolated from coastal inputs of DOC.     

Algal respiration and the regulation of phytoplankton biomass in a polymictic tropical lake (Lake Xolotlán,Nicaragua)

Community respiration in tropical Lake Xolotlán, Nicaragua, was assessed seasonally and during diurnal cycles, via oxygen consumption in bottle enclosures. Results were analysed in relation to phytoplankton biomass, mixing depth, depth of photic zone and phytoplankton production. A great part of community respiration was associated with the heterotrophic activity of the phytoplankton biomass or its degradation by bacteria and 80% of the variability in oxygen consumption was explained by the variation of chlorophyll-a. Specific rate of respiration was 1.5 mg O2 mg Chla-1 h-1 during diurnal cycles, which corresponded to less than 5% of the specific rate at optimum depth of production. Still, diurnal water column respiratory losses were always of the same magnitude as the total photosynthetic gains in the photic zone, since the mixing depth exceeded the depth of the photic zone. Total column net growth was zero at a ratio between depth of photic zone and mixing depth of 0.19. Water level variations however altered the mixing depth and affected this ratio and net growth. As a consequence, the phytoplankton biomass either increased or decreased until the ratio was re-established through changes of the photic zone depth, which was governed by the phytoplankton biomass itself through the chlorophyll-a light attenuation. This revised version was published online in July 2006 with corrections to the Cover Date.     

Seasonal variation of nutrients,organic carbon,ATP, and microbial standing crops in a vertical profile of Pyramid Lake,Nevada

Previous studies of Pyramid Lake, Nevada, led to the hypothesis that detritus could be an important food source for zooplankton because abundance of palatable algal species did not seem to be enough to support the zooplankton community throughout the year. Furthermore, a large portion of the annual primary productivity was attributed to a nonpalatable blue-green alga, Nodularia spumigena. We felt this alga became important to the Pyramid Lake aquatic community upon death, as edible detritus and a source of new nitrogen. Changes in pelagic detritus concentrations and microbial standing crops were monitored to determine the availability of these potential foods. Epilimnetic particulate organic carbon (POC) was primarily living phytoplankton. During holomixis and following spring primary production, hypolimnetic POC was 60–97% detrital, but these profundal POC concentrations were low (ca 650 µg l^-1). Detritus-bacteria aggregates were observed only following the September cyanophyte bloom. Although pelagic detritus availability for zooplankton was low, bacterial populations were sufficient to be at least a supplemental food source. Bacteria numbers ranged from 0.50 10⁶ to 24.7 10⁶ ml^-1 and increased in response to photosynthetic peaks. Microbial diversity, contribution to POC, and particle association were notable after July. The percentage of living carbon (assessed with ATP measurements) attributable to bacteria was highest in late summer and fall hypolimnetic samples. Patterns of change in organic phosphorus and nitrogen, the presence of a nitrogen-fixing cyanophyte, the N:P ratio, and results of other research demonstrated that non-nitrogen-fixing algae of Pyramid Lake are limited by inorganic nitrogen. The importance of N. spumigena to the aquatic community appeared to be as a source of new nitrogen, rather than as a forage; its mineralization is critical for the growth of palatable diatoms and green algae following winter mixing.     

Extracellular release of photosynthetic products by freshwater phytoplankton populations, with special reference to the algal species involved

SUMMARY. Over three successive years, depth profiles of C-fixation and excretion, chlorophyll- a concentrations, phytoplankton species composition and bacterial numbers were determined in Lake Vechten, a slightly eutrophic lake in The Netherlands. Special attention was given to the method used to measure extracellular release.
Excretion of dissolved organic ¹⁴C depended largely upon the photo-synthetic activity of the phytoplankton, ranging from 0–2.5 mg m^-1 h^-1, representing a percentage extracellular release (PER) of 0–25%.
During a period in August, however, a subsurface chlorophyll- a maximum at 5–7 m depth coincided with high excretion rates of up to 10 mg Cm^-3 h^-1 (PER = 55%). Phytoplankton analysis revealed a stratification in numbers of Mallomonas caudata with a maximum at 5–7 m depth.
The results suggest that in these water layers bacterial populations grew at the expense of the dissolved organic carbon compounds excreted by Mallomonas caudata. This means that extracellular release can temporarily function as an important nutrient source for the heterotrophie community in addition to the more or less constant dissolved organic carbon pool.     

Microbial sulfate reduction in a brackish meromictic steppe lake

Patterns of sulfate reduction were studied in water and sediments of Lake Shira, South Siberia, Russia. The lake was characterized by a high level of sulfate (91-116 mM). The concentration of hydrogen sulfide in the anoxic waters of the lake reached 0.6 mM. In summer the sulfate reduction rate in the water column, measured by radiometric technique, varied from 0.25 to 9.81 mol sulfate l^-1 d^-1. There were two peaks of sulfate reduction activity: just below the chemocline and near the sediment surface. Sulfate reduction rate in the profundal silts ranged from 4.1 to 90.6 mol l^-1 d^-1. The zone of the most active sulfate reduction was restricted to the surface sediment layers. The acceleration of sulfate reduction rate (up to 236 mol l^-1 d^-1) and the increase of density of viable sulfate reducers (up to 2 x 10⁵ cells ml^-1) were recorded in the littoral sediments adjacent to the mouth of the Son River and sewage discharge. It was apparently caused by the input of allochthonous organic substrates and also by a high environmental temperature. On an areal basis, sulfate reduction rate in the water was approximately 8 times higher than that in the profundal sediments. Sulfate reduction was the most important process of anaerobic oxidation of organic carbon in Lake Shira. In summer in the profundal zone of the lake, sulfate reducers were able to mineralize about 67% of the daily integrated primary production of phototrophic and chemotrophic organisms.     

Growth and release of extracellular organic compounds by benthic diatoms depend on interactions with bacteria

Phototrophic epilithic biofilms harbour a distinct assemblage of heterotrophic bacteria, cyanobacteria and photoautotrophic algae. Secretion of extracellular polymeric substances (EPS) by these organisms and the physicochemical properties of the EPS are important factors for the development of the biofilms. We have isolated representative diatom and bacteria strains from epilithic biofilms of Lake Constance. By pairwise co-cultivating these strains we found that diatom growth and EPS secretion by diatoms may depend on the presence of individual bacteria. Similar results were obtained after addition of spent bacterial medium to diatom cultures, suggesting that soluble substances from bacteria have an impact on diatom physiology. While searching for putative bacterial signal substances, we found that concentrations of various dissolved free amino acids (DFAA) within the diatom cultures changed drastically during co-cultivation with bacteria. Further, the secretion of extracellular carbohydrates and proteins can be influenced by bacteria or their extracellular substances. We have performed mass spectrometric peptide mapping to identify proteins which are secreted when co-cultivating the diatom Phaeodactylum tricornutum Bohlin and Escherichia coli. The identified proteins are possibly involved in signalling, extracellular carbohydrate modification and uptake, protein and amino acid modification, and cell/cell aggregation of diatom and bacteria strains. Our data indicate that diatom-bacteria biofilms might be regulated by a complex network of chemical factors involving EPS, amino acid monomers and other substances. Thus interactions with bacteria can be considered as one of the main factors driving biofilm formation by benthic diatoms.