Wanda Zevenboom

N2-fixing cyanobacteria: Why they do not become dominant in shallow hypertrophic lakes

SummaryPhytoplankton species shifts and succession phenomenona in lakes of increasing trophic state were considered, using the basic information on the growth kinetics of the species involved. One of the most obvious signs of advanced eutrophication is the dominance of cyanobacteria (blue-green algae). Striking examples are the shallow, hypertrophic Dutch lakes ‘The Veluwerandmeren’ (e.g., Wolderwijd and Veluwemeer), whereOscillatoria agardhii, a non-N2-fixing cyanobacterium, has become dominant over the green algae, diatoms and N2-fixing cyanobacteria (BERGER, 1975).We have studied the natural population ofO.agardhii during the growing season, by using physiological indicators, and could adduce that the natural population was successively growing under phosphorus, light, or nitrogen limitation (ZEVENBOOM and MUR, 1978a,b; ZEVENBOOMet al., 1982). One might expect that during the period of nitrogen limitation the N2-fixing speciesAphanizomenon flos-aquae would be favoured and would be able to outgrow the nitrogen-limitedO.agardhii. However, in these lakes,A. flos-aquae was present only in few numbers and a succession fromO. agardhii toA. flos-aquae did not occur. Although field observations may give some indication, they cannot give decisive answers to the question which factor is triggering the observed species shifts and species dominance in natural waters. Such answers can only be obtained from growth kinetic and physiological data of the species involved. In our opinion, the most important factor to consider is the availability of light energy, which decreases with increasing eutrophication.The hypothesis was proposed by Mur and coworkers (MURet al., 1978) that in hypertrophic lakes the prevailing light conditions (low light irradiance) are more favourable forO.agardhii, since this species has a much lower requirement of light energy for growth than green algae as a consequence of its lower specific maintenance rate constant, μe (VAN LIERE, 1979; GONS, 1977). Competition experiments, performed withO. agardhii andScenedesmus protuberans under lightlimiting conditions, confirmed the hypothesis (MURet al., 1978), Continuous culture experiments withA. flos-aquae showed that also this species had a higher energy requirement thanO. agardhii (ZEVENBOOM, 1980). The differences were not found in the value of μe, but in the growth efficiency. The higher energy requirement ofA.flos-aquae was expected, since energy is needed for heterocyst production and N2 fixation. Under light-limiting conditions and nutrient sufficiency (including nitrogen-nitrate) it can thus be expected that the N2-fixer will be outcompeted by the non-N2-fixing cyanobacterium. This was indeed observed (ZEVENBOOM et al., 1981).We further investigated the competitive interactions betweenA.flos-aquae, O. agardhii andS. protuberans under different sets of irradiance values and nitrate concentrations. We used the growth kinetic data of the species involved, which were obtained by means of continuous culture experiments (GONS, 1977; VAN LIERE. 1979; VAN LIERE and MUR, 1979; GONS and MUR, 1980; ZEVENBOOM and MUR, 1980; ZEVENBOOMet al., 1980; ZEVENBOOMet al., 1981). The competing species could be placed along the gradients of light irradiance values and nitrate concentrations, their positions being defined by their energy requirements and half-saturation constants for nitrate-limited growth, respectively. Distinct niches for the three species were found with respect to light and nitrate. Under conditions of low irradiance values and low (realistic) nitrate concentrations, nitrogen-limitedO.agardhii was able to outgrowA. flos-aquae andS. protuberans as a consequence of its low energy requirement and its high affinity for nitrate. The growth rates of the last two species were restricted by the limited availability of light. However, at high irradiance values,O.agardhii was inhibited in its growth rate and therefore failed to outgrow the other two species. The competition was then restricted to nitrogen-limitedS.protuberans and light-limitedA.flos-aquae; the latter could dominate at low nitrate concentrations. The results of competition experiments withO.agardhii andA.flos-aquae under different sets of irradiance values and nitrate concentrations agreed well with the ‘niche-model’ described above (Zevenboom, unpubl. results).In conclusion, kinetic data of growth, obtained with continuous culture experiments, can provide basic information to explain species shifts and dominance in lakes with increasing eutrophication. Nitrogen-limiting conditions favour N2-fixing cyanobacteria only when sufficient light is available for their growth (in less hypertrophic waters). The trophic state is thus of major importance and decisive with regard to which species will dominate.

Growth and photosynthetic response of the cyanobacterium Microcystis aeruginosa in relation to photoperiodicity and irradiance

AbstractGrowth and photosynthetic characteristics, Pmax (maximum light-saturated oxygen production rate) and α (photosynthetic affinity), of Microcystis aeruginosa were studied in continuous cultures under a range of photoperiod lengths and growth irradiances. Microcystis showed a low specific maintenance rate constant and a high growth affinity for light (typical cyanobacterial features), but required a dark period to obtain maximum growth rate. Pmax and α per unit dry weight increased, as did pigment content, when less light became available. By regulation in α and Pmax (crucial in light-limiting and high-light conditions, respectively) this buoyant species can flourish in low light, but also in high-light environments which may arise when buoyancy is lost.The two different types of light conditions affected growth, and photosynthesis, in different ways. One needs thus to discriminate between photoperiod- and irradiance-limitation, which restricts the utility of simple algal growth models. It was emphasized that photosynthetic adaptation patterns of light-limited species may resemble short-term nutrient uptake kinetics of nutrient-limited organisms.With prior knowledge of the growth limitation, we were able to assess the growth rate of a natural population of Microcystis from its photosynthetic response and from data of laboratory cultures of a known physiological state.

Effects of light on nitrate-limited Oscillatoria agardhii in chemostat cultures

The effects of the average light irradiance (〈I〉) on growth and nitrate uptake kinetics of the cyanobacterium Oscillatoria agardhii, in nitrate-limited chemostat cultures, were studied. Light was nonsaturating for 〈I〉 <9.4 Wm−2, for all growth rates (μ) studied. However, μ was throughout limited by the availability of nitrate. Under light-saturating conditions the kinetics of nitrate-limited growth could be adequately described by both the Monod and Droop equations. Under light-non-saturating conditions the internal nitrogen content (Q) was a function of both μ and 〈I〉, for which new formulas were derived. The high uptake capacity (Vmax) of nitrate-limited cells was independent of μ, but was significantly increased for cells growing at 〈I〉 <9.4 Wm−2. The half-saturation constant for nitrate uptake (Ksu) increased with increasing μ, but was independent of the prevailing light conditions. The effects of light during nitrate-limited growth were associated with the regulation in the nitrogen-containing pigments.The results reported herein have important consequences for the use of Q, Ksu and Vmax values as indicators of nutrient-deficiency of natural populations.

Growth ofOscillatoria agardhii Gom.

SummaryThe growth kinetics of the blue-green algaOscillatoria agardhii Gom. were studied both in batch culture and in chemostat culture; these allowed Ks and μm values for nitrogen (nitrate) limitation to be determined. There were large differences between the growth kinetics of this organism in batch culture compared with chemostat culture. Some information is further given regarding the influence of various growth limitations on pigmentation and cell composition.

Simultaneous Short-term Uptake of Nitrate and Ammonium by Oscillatoria agardhii Grown in Nitrate- or Light-limited Continuous Culture

The cyanobacterium Oscillatoria agardhii Gomont was grown in continuous culture under nitrate- or light-limited conditions. Short-term uptake rates of nitrate and ammonium were studied at various concentrations of nitrate and ammonium, both of which were present during the short-term assay. In nitrate-limited O. agardhii, the short-term ammonium uptake rate was not influenced by the presence of nitrate. Ammonium inhibited the rate of nitrate uptake in a non-competitive manner. An equation was derived for the short-term nitrate uptake rate which was a function of the ambient concentrations of both nitrate and ammonium. For a low ammonium concentration tested, the pattern of the nitrate-ammonium interaction in light-limited O. agardhii did not differ greatly from that found in nitrate-limited O. agardhii.

Growth limitation and growth rates of (pico)phytoplankton in the banda sea during two different monsoons

Abstract The types of growth limitation and growth rates of phytoplankton and picocyanobacteria in the Banda Sea were examined in August 1984 (southeast monsoon, upwelling, expected nutrient-rich) and February–March 1985 (northwest monsoon, down-welling, expected nutrien-poor). The sensitive indicator used to discriminate between the different types of phytoplankton growth limitations was the ratio of the initial saturated uptake rate (Vm) and the specific nutrient uptake rate (q). In addition, the ratio of carbohydrates and proteins was used. Specific growth rate was assessed from the ratio of Vm of the non-limiting nutrient and cellular nutrient content. In August 1984 the phytoplankton was not limited by nutrients, but most probably by light, except at one station (St. 53, to the south of Irian Jaya) where the surface phytoplankton was nitrogen-limited and growing at a very low rate. During February 1985 the surface phytoplankton was nitrogen-limited. In the middle part of the Banda Sea and N-limitation extended to deep water layers. However, heterogeneity in phytoplankton growth-limitation with depth was also found at other stations, where the deep small-sized photoautotrophs (mainly red-pigmented picocyano-bacteria) were growing at considerably higher rates, which often exceeded the growth rate of larger-sized species by a factor of three. These results support the view that picoplankton forms an important component of primary productivity in tropical waters. The assessment of growth limitation by the use of physiological indicators, rather than by the use of nutrient concentrations in seawater, will be discussed.

Picocyanobacteria in the Banda Sea during two different monsoons

Abstract The relative abundance of red-pigmented picocyanobacteria, a recently recognized component of ocean primary productivity, was examined in the Banda Sea during August 1984 (cruise 1, southeast monsoon, upwelling) and February/March 1985 (cruise 2, northwest monsoon, downwelling). These small-sized ( μ m) species are rich in the red pigment phycoerythrin (PE) and belong to the Synechococcus -type species that was studied in continuous culture. The cell concentrations were assessed by using the characteristic PE-absorbance peak at 545 nm in the in vivo absorption spectra as tracer and epifluorescence microscopy. Picocyanobacteria were found in relatively high concentrations (10 4 –10 5 cells·cm −3 ) at 75% and 96% of the Banda Sea stations of cruise 1 and 2, respectively. The cell-numbers were higher during the first cruise, but their relative importance (as part of the total phytoplankton-biomass) was higher during the second cruise. The species showed a preference for deeper layers where light intensities were low. Their low surface abundance seemed to show a diurnal pattern ( i.e. decreasing during the course of the day), correlated with surface irradiance. The occurrence of such a diurnal pattern is discussed in relation with results of light shift experiments with continuous cultures of Synechococcus .