Jörg Tittel

Mixotrophs combine resource use to outcompete specialists: Implications for aquatic food webs

The majority of organisms can be grouped into those relying solely on photosynthesis (phototrophy) or those relying solely on the assimilation of organic substances (heterotrophy) to meet their requirements for energy and carbon. However, a special life history trait exists in which organisms combine both phototrophy and heterotrophy. Such “mixotrophy” is a widespread phenomenon in aquatic habitats and is observed in many protozoan and metazoan organisms. The strategy requires investment in both photosynthetic and heterotrophic cellular apparatus, and the benefits must outweigh these costs. In accordance with mechanistic resource competition theory, laboratory experiments revealed that pigmented mixotrophs combined light, mineral nutrients, and prey as substitutable resources. Thereby, they reduced prey abundance below the critical food concentration of competing specialist grazers [Rothhaupt, K. O. (1996) Ecology 77, 716–724]. Here, we demonstrate the important consequences of this strategy for an aquatic community. In the illuminated surface strata of a lake, mixotrophs reduced prey abundance steeply. The data suggest that, as a consequence, grazers from higher trophic levels, consuming both the mixotrophs and their prey, could not persist. Thus, the mixotrophs escaped from competition with and losses to higher grazers. Furthermore, the mixotrophs structured prey abundance along the vertical light gradient, creating low densities near the surface and a pronounced maximum of their algal prey at depth. Such deep algal accumulations are typical features of nutrient-poor aquatic habitats, previously explained by resource availability. We hypothesize instead that the mixotrophic grazing strategy is responsible for deep algal accumulations in many aquatic environments.

Strong vertical differences in the plankton composition of an extremely acidic lake

Vertical differences in food web structure were examined in an extremely acidic, iron-rich mining lake in Germany (Lake 111; pH 2.6, total Fe 150 mg L -1 ) during the period of stratification. We tested whether or not the seasonal variation of the plankton composition is less pronounced than the differences observed over depth. The lake was strongly stratified in summer, and concentrations of dissolved organic carbon and inorganic carbon were consistently low in the epilimnion but high in the hypolimnion. Oxygen concentrations declined in the hypolimnion but were always above 2 mg L -1 . Light attenuation did not change over depth and time and was governed by dissolved ferric iron. The plankton consisted mainly of single-celled and filamentous bacteria, the two mixotrophic flagellates Chlamydomonas sp. and Ochromonas sp., the two rotifer species Elosa worallii and Cephalodella hoodi, and Heliozoa as top predators. We observed very few ciliates and rhizopods, and no heterotrophic flagellates, crustaceans or fish. Ochromonas sp., bacterial filaments, Elosa and Heliozoa dominated in the epilimnion whereas Chlamydomonas sp., single-celled bacteria and Cephalodella dominated in the hypolimnion. Single-celled bacteria were controlled by Ochromonas sp. whereas the lack of large consumers favoured a high proportion of bacterial filaments. The primarily phototrophic Chlamydomas sp. was limited by light and CO 2 and may have been reduced due to grazing by Ochromonas sp. in the epilimnion. The distribution of the primarily phagotrophic Ochromonas sp. and of the animals seemed to be controlled by prey availability. Differences in the plankton composition were much higher between the epilimnion and hypolimnion than within a particular stratum over time. The food web in Lake 111 was extremely species-poor enabling no functional redundancy. This was attributed to the direct exclusion of species by the harsh environmental conditions and presumably enforced by competitive exclusion. The latter was promoted by the low diversity at the first trophic level which, in turn was attributed to relatively stable growth conditions and the independence of resource availability (inorganic carbon and light) from algal density. Ecological theory suggests that low functional redundancy promotes low stability in ecosystem processes which was not supported by our data.

A new medium free of organic carbon to cultivate organisms from extremely acidic mining lakes (pH 2.7)

An algal culture medium was developed which reflects the extreme chemical conditions of acidic mining lakes (pH 2.7, high concentrations of iron and sulfate) and remains stable without addition of organic carbon sources. It enables controlled experiments e.g. on the heterotrophic potential of pigmented flagellates in the laboratory. Various plankton organisms isolated from acidic lakes were successfully cultivated in this medium. The growth rates of a Chlamydomonas isolate from acidic mining lakes were assessed by measuring cell densities under pure autotrophic and heterotrophic conditions (with glucose as organic C-source) and showed values of 0.74 and 0.40, respectively. Ein neues Medium, frei von organisch gebundenem Kohlenstoff, zur Kultivierung von Organismen aus extrem sauren Tagebauseen (pH = 2.7) Es wurde ein Kulturmedium entwickelt, welches die extreme chemische Situation von sauren Tagebauseen widerspiegelt (pH = 2.7, hohe Konzentrationen an Eisen und Sulfat) und ohne Zugabe von organischen Kohlenstoffverbindungen stabil bleibt. Es ermoglicht kontrollierte Experimente z. B. uber das heterotrophe Potential pigmentierter Flagellaten im Labor. Verschiedene Planktonorganismen, die aus sauren Seen isoliert wurden, konnten erfolgreich in diesem Medium kultiviert werden. Die Wachstumsraten eines isolierten Chlamydomonas-Stammes wurden uber die Zelldichten unter rein autotrophen bzw. heterotrophen Bedingungen (mit Glukose als organischer C-Quelle) aufgenommen und ergaben Werte von 0.74 bzw. 0.40.

Reservoirs as sentinels of catchments: the Rappbode Reservoir Observatory (Harz Mountains, Germany)

Reservoirs can be viewed as sentinels of their catchments and a detailed monitoring of reservoir systems informs about biogeochemical and hydrological processes at the catchment scale. We developed a comprehensive online monitoring system at Rappbode reservoir, the largest drinking water reservoir in Germany, and its inflows. The Rappbode Reservoir Observatory comprises of a set of online-sensors for the measurement of physical, chemical, and biological variables and is complemented by a biweekly limnological sampling schedule. Measurement stations are deployed at the four major inflows into the system, at the outlets of all pre-reservoirs, as well as in the main reservoir. The newly installed monitoring system serves both scientific monitoring and process studies, as well as reservoir management. Particular emphasis is paid to the monitoring of short-term dynamics and many variables are measured at high temporal resolution. As an example, we quantitatively documented a flood event which mobilised high loads of dissolved organic carbon and changed the characteristics of the receiving reservoir from eutrophic to dystrophic within a few days. This event could have been completely missed by conventional biweekly sampling programs, but is relevant for biogeochemical fluxes at the catchment scale. We also show that the high frequency data provide a deeper insight into ecosystem dynamics and lake metabolism. The Rappbode Reservoir Observatory; moreover, offers a unique study site to apply, validate, and develop state of the art lake models to improve their predictive capabilities.

Functions of Straw for In Situ Remediation of Acidic Mining Lakes

The addition of straw in combination with ‘Carbokalk’, a by-product from the sugar-industry, was successfully used to stimulate microbial alkalinity generation in an acidic mining lake. To get detailed information about functions of straw, anenclosure experiment was carried out. Straw bundles were placedat the sediment surface of an acidic mining lake (ML 111) and thephysiochemical conditions and the microbiology of the sediment-water contact zone were studied. Straw was degraded by anaerobic microorganisms and dissolved organic carbon (DOC) leached from straw bundles. Pigmented flagellates responded to the DOC supply in the water column anda considerable amount of algal carbon was transported to the sediment. Straw addition led to microbial reduction of iron andsulfate in the sediment. Sulfate reduction was observed at a pHof 5.5. The pH, however, was not high enough to precipitate H2S completely. Thus, some H2S diffused into the watercolumn, where it was reoxidized. Straw did not create orstabilize an anoxic water body above the sediment. Microbial sulfate reduction and pyrite formation only took place in the sediment,whereas iron reduction also took place in the straw. Straw, however, altered the flow conditions above the sediment surfaceand prevented complete mixing of the profundal water. Straw didnot serve as a substratum for a reactive biofilm. We conclude that the most important function of straw for mining lake remediation is to be a long-term nutrient source for microbialalkalinity generation in the sediment.

ALGAE AS COMPETITORS FOR GLUCOSE WITH HETEROTROPHIC BACTERIA

Dissolved organic carbon (DOC) constitutes the bulk of organic carbon in aquatic environments. The importance of DOC utilization by mixotrophic algae is unclear since heterotrophic bacteria are regarded as more efficient users. We tested the hypothesis that algae decrease the DOC concentration in the light to lower levels than in darkness resulting in competitive exclusion of heterotrophic bacteria according to the mechanistic competition theory. We investigated (a) the uptake kinetics of glucose as a model substrate by two cultured algae and mixed bacteria populations, (b) the competition for glucose between algae and bacteria in chemostats, (c) the effect of discontinuous glucose supply in chemostats, and (d) the minimum glucose concentrations achieved in cultures of algae and bacteria. Bacteria showed higher specific‐glucose‐uptake rates than algae. In chemostats, algae became extinct in the dark and coexisted in the light where they decreased bacteria to lower densities. Discontinuous glucose supply promoted the algae compared to continuous substrate addition. Several algae consumed glucose to lower concentrations in the dark than in the light and showed lower or equal residual glucose concentrations than bacteria. Residual concentrations were not related to allometric traits (cell volume) and photosynthetic potential (chl content). Overall, the hypothesis was not supported, and mechanisms of competition for DOC obviously differed from those for particulate prey. However, since some algae showed lower or equal residual glucose concentrations than bacteria, algal dark uptake of DOC may be important in deep layers of many waters.

Utilisation of terrestrial carbon by osmotrophic algae

Abstract.Terrestrial-derived dissolved organic carbon (DOC) contributes significantly to the energetic basis of many aquatic food webs. Although heterotrophic bacteria are generally considered to be the sole consumers of DOC, algae and cyanobacteria of various taxonomic groups are also capable of exploiting this resource. We tested the hypothesis that algae can utilise DOC in the presence of bacteria if organic resources are supplied in intervals by photolysis of recalcitrant DOC. In short-term uptake experiments, we changed irradiation in the range of minutes. As model substrates, polymers of radiolabelled coumaric acid (PCA) were used, which during photolysis are known to release aromatic compounds comparable to terrestrial-derived and refractory DOC. Three cultured freshwater algae readily assimilated PCA photoproducts equivalent to a biomass-specific uptake of 5–60% of the bacterial competitors present. Algal substrate acquisition did not depend on whether PCA was photolysed continuously or in intervals. However, the data show that photoproducts of terrestrial DOC can be a significant resource for osmotrophic algae. In long-term growth experiments, interval light was applied one hour per day. We allowed cultured Chlamydomonas to compete for ambient DOC of low concentration. We found higher abundances of Chlamydomonas when cultures were irradiated intermittently rather than continuously. These data suggest that photolysis of DOC supports algal heterotrophy, and potentially facilitates growth, when light fluctuations are large, as during the diurnal light cycle. We concluded that osmotrophic algae can efficiently convert terrestrial carbon into the biomass of larger organisms of aquatic food webs.

Occurrence of an Algal Mass Development in an Acidic (pH 2.5):, Iron and Aluminium‐rich Coal Mining Pond

A bloom of Chlamydomonas botryopara was observed in an extremely acid coal mining pond (pH 2.5) with high concentrations of iron and aluminium (1160...3760 mg L–1 Fe, 133...387 mg L–1 Al). Cell density of algae was counted as 6.45 · 106 mL–1 corresponding to 700 mg L–1 fresh weight and 2660 μg L–1 chlorophyll-a. The nutrient concentrations were 3.5 mg L–1 soluble reactive phosphorus and 0.15 mg L–1 dissolved inorganic nitrogen. This observation supports the hypothesis that a low nutrient availability rather than extreme conditions (e.g. high acidity and low pH) limit the development of phytoplankton in many acidified lakes. Auftreten einer Algenmassenentwicklung in einem sauren:, eisen- und aluminiumreichen Braunkohlerestgewasser In einem extrem sauren Braunkohlerestgewasser (pH = 2.5) mit hohen Eisen- und Aluminumkonzentrationen (1160...3760 mg L–1 Fe, 133...387 mg L–1 Al) wurde eine Algenblute von Chlamydomonas botryopara beobachtet. Die Algenzelldichte lag bei 6.45 · 106 mL–1, dem entsprechend das Frischgewicht bei 700 mg L–1 und die Chlorophyllkonzentration bei 2660 μg L–1. Die Nahrstoffkonzentrationen betrugen 3.5 mg L–1 geloster reaktiver Phosphor und 0.15 mg L–1 geloster anorganisch gebundener Stickstoff. Diese Beobachtung stutzt die Hypothese, dass eine geringe Nahrstoffverfugbarkeit wichtiger fur die Limitation von Algenentwicklungen in sauren Seen ist als extreme Umweltbedingungen (z. B. hohe Aziditat und niedrige pH-Werte).

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.

Phytoplankton Composition and Biomass Spectra Created by Flow Cytometry and Zooplankton Composition in Mining Lakes of Different States of Acidification

In most aquatic systems, phytoplankton organisms are the most important primary producers. Thus, any alterations in the phytoplankton community have strong effects on the whole system. Apart from the fulfillment of basic requirements such as temperature, dissolved oxygen, ion composition and pH, zooplankton abundance and community structure depend mainly on the amount and usability of phytoplankton as the main source of nutrition. Conversely, effects of zooplankton on the phytoplankton community can be found - feeding types, selection (cell size and shape) and release of nutrients - which can strongly alter phytoplankton abundance and diversity.