jurnal isol ing

8/12/2019 Jurnal Isol Ing.

1/12

The outcome of competition between the two chrysomonads

Ochromonassp. and Poterioochromonas malhamensis depends

on pH

Michael Moserand Thomas Weisse

Institute for Limnology of the Austrian Academy of Sciences, Herzog Odilostrae 101, 5310

Mondsee, Austria

Abstract

We investigated the effect of pH on the competition of two closely related chrysomonad species,Poterioochromonas malhamensisoriginating from circumneutral Lake Constance, andOchromonassp. isolated from a highly acidic mining lake in Austria (pH 2.6). We performed

pairwise growth experiments between these two species at four different pH ranging from 2.5 to7.0. Heterotrophic bacteria served as food for both flagellates. Results were compared to growthrates measured earlier in single species experiments over the same pH range. We tested thehypothesis that the acidotolerant species benefits from competitive release under conditions ofacid stress. The neutrophilic strain numerically dominated over the acidotolerant strain at pH 7.0,but was the inferior competitor at pH 2.5. At pH 3.5 and 5.0 both strains coexisted. Surprisingly,P. malhamensisprevailed over Ochromonassp. under moderately acidic conditions, i.e. at the pHwhere growth rates of the latter peaked when grown alone. Since bacterial food was not limiting,resource competition is improbable. It appears more likely that P. malhamensisingested cells ofits slightly smaller competitor. Adverse effects mediated via allelopathy, either directly on thecompeting flagellate or indirectly by affecting its bacterial food, might also have affected theoutcome of competition.

Keywords

Competition; pH; Ochromonas; Poterioochromonas malhamensis; Acid mining lake

Introduction

The chrysophyte genera Ochromonasand Poterioochromonasare commonly found in abroad range of aquatic habitats (Bochat et al. 2007; Boenigk et al. 2005). A likely reasonfor their ecological success is that species within both genera can have different nutritionalmodes. Mixotrophy, the combination of autotrophic growth via photosynthesis with theuptake of dissolved organic matter or bacteria, is widespread in these chrysomonads(Aaronson and Baker 1959; Bennett et al. 1990; Sanders et al. 1990). Another reason for

their ecological success is their ability to produce toxins that may adversely affect potentialpredators such as cladocerans and rotifers (Boenigk and Stadler 2004). Recently, Blom and

2011 Elsevier GmbH.

Corresponding author. Tel.: +43 6232 312512; fax: +43 6232 3578. [email protected].

This document was posted here by permission of the publisher. At the time of deposit, it included all changes made during peerreview, copyediting, and publishing. The U.S. National Library of Medicine is responsible for all links within the document and forincorporating any publisher-supplied amendments or retractions issued subsequently. The published journal article, guaranteed to besuch by Elsevier, is available for free, on ScienceDirect.

Sponsored document from

European Journal of Protistology

Published as: Eur J Protistol. 2011 May ; 47(2): 7985.

Spon

soredDocument

SponsoredDocument

SponsoredDocument


2/12

Pernthaler (2010) reported antibiotic effects of Ochromonas danicaand the samePoterioochromonasstrain as used in the present investigation on freshwater bacteria. Theantibiotic effects were not only strain-specific, but depended also on the nutritional mode ofthe flagellates.

Chrysophytes reach the highest relative abundances in oligotrophic lakes where resourcesare limiting (Sandgren 1988). Generally, mixotrophy is a successful life style that enables

the organisms to overcome unfavourable conditions and to colonize harsh environments(Jones 1994). In accordance with this view, several species of the genus Ochromonasbelongto the most important pioneer colonists in oligotrophic, man-made acid mining lakes(Nixdorf et al. 1998). Acidic mining lakes (AML) are extreme aquatic habitats (pHoften < 3) with strongly reduced biodiversity (Gaedke and Kamjunke 2006; Geller et al.1998) and are found on all continents. The organisms thriving in these lakes may be highlyspecialized new colonizers (acidophilic species), or they may be generalists (acidotolerantspecies) taking refuge from otherwise superior competitors or predators that are less tolerantof the harsh environmental conditions (Tittel et al. 2003; Wollmann et al. 2000).

The definitions of acidophilic, acidotolerant and neutrophilic are somewhat ambiguousacross different taxa (Moser and Weisse 2011a). We define an acidophilic species as aspecies that shows a clear fitness optimum under highly acidic conditions. An acidotolerant

species is able to grow both at circumneutral and acidic pH, but thrives at moderately acidicconditions. A neutrophilic species has its fitness optimum at circumneutral conditions.

Due to the low pH, supply of CO2is limited in AML because of the absence of thebicarbonate pool (Gross 2000). As a consequence, the relative contribution of mixotrophicflagellates to the algal community is higher in AML than in circumneutral water bodies(Gaedke and Kamjunke 2006). Ochromonasspp. are the most important bacterial grazers,removing up to 88% of the daily bacterial production in the epilimnion of AML (Schmidtkeet al. 2006). Experimental evidence demonstrated that the mixotrophs may even outcompetebacterivorous specialists (Tittel et al. 2003).

The goal of this study was to test the competitiveness of an acidotolerant chrysomonadisolated from an AML vs. a closely related, neutrophilic species under varying experimental

pH. We assumed that the species dwelling in the AML would be the superior competitor atlow pH, while the neutrophilic species would outcompete the specialist at circumneutral pH.We assessed population growth rates that can be used as a proxy for fitness in asexuallyreproducing protists (Weisse 2006). Our hypothesis was that the acidotolerant species wouldbenefit from competitive release under conditions of acidic stress. An as yet unidentifiedOchromonassp. strain isolated from a highly acidic (pH 2.6) mining lake in Austriarepresented the acidotolerant species. Poterioochromonas malhamensisstrain DS that hadbeen isolated from weakly alkaline Lake Constance (Stabel 1998) served as a model for aneutrophilic species. Most of the chrysomonad flagellates tested thus far for their pHtolerance were tolerant to widely changing pH ranging from 3 to 11 (Boenigk 2008).Previous experiments in our laboratory revealed that P. malhamensisis able to survive underacidic conditions, and that Ochromonassp. can tolerate circumneutral pH for severalgenerations (Moser and Weisse 2011a). In pursuit of the above hypothesis, we performed

pairwise competition experiments with these two species over a pH range from 2.5 to 7.0.

Material and Methods

Study sites and organisms

The mixotrophic flagellates used in this study originated from an acid mining lake in Langau(Lower Austria, 4850N, 1543E) and from Lake Constance (4735N, 928E). Isolation of

Moser and Weisse Page 2

Published as:Eur J Protistol. 2011 May ; 47(2): 7985.

SponsoredDocument

SponsoredDocument

SponsoredDocument


3/12

a species of the genus OchromonasVysotskii, 1887 from the acid mining lake was achievedvia dilution of lake water and individually pipetting of several cells. The species identity ofOchromonassp. was verified by sequencing of the 18S rDNA and consecutive BLASTsearch (GenBank accession number FN429125). Accordingly, this flagellate belongs to thegenus Ochromonaswithin the C3 cluster of the Spumella-like flagellates identified byBoenigk et al. (2005).

Several strains of Poterioochromonas malhamensis(Pringsheim 1952) Pterfi, 1969(basionym Ochromonas malhamensis) have been used previously to investigate their growthand grazing rates (Zhang and Watanabe 2001), phototrophy vs. phagotrophy (Sanders et al.1990), and antibiotic effects and toxicity (Blom and Pernthaler 2010; Boenigk and Stadler2004). The P. malhamensisstrain DS from Lake Constance used in the latter two citedstudies and in the present investigation was isolated by Doris Springmann in the late 1980s.Since then it has been kept in batch cultures on a bacterial diet in our laboratory. Thetaxonomic identity of this strain was confirmed previously by molecular taxonomy. A fullsequence of the SSU rDNA gene is available in GenBank (accession number AM981258.1).Sequence similarity of the 18S rDNA gene is 94% between the two flagellate strains used inthis study. The cell size of P. malhamensis(5.52 0.93 m) was significantly larger(P< 0.001) than that of Ochromonassp. (4.01 0.58 m) in our experimental treatments.

Flagellate stock cultures were maintained in modified Woods Hole Medium (MWC) asnonclonal, nonaxenic batch cultures at a continuous light intensity of 90100 mol m2s1

and 17.5 C. In the flagellate stock cultures originating from the acid mining lake, pHranged from 2.6 to 3.0 because the natural pH of the acid mining lake is in the range of 2.33.7. The pH varied seasonally, but was mostly close to 2.6 (Moser and Weisse 2011b). Dueto the oxidation of pyrite and marcasite this lake has been acidified from its beginning. As aconsequence of this oxidation, this lake exhibits high iron (110430 mg l1) and sulphate(11001600 mg l1) concentrations and, therefore, a high conductivity (Moser and Weisse2011b). Poterioochromonas malhamensiswas kept at pH 7.0 because Lake Constance is aneutral to weakly alkaline lake (Stabel 1998). All flagellate stock cultures were suppliedwith a wheat grain to stimulate growth of their bacterial food.

Experimental design

Experiments were conducted in 50-ml culture tissue flasks at moderate continuous lightintensity (100 mol m2s1) provided from above by an Osram L 8W/954 Lumilux deLuxe Daylight lamp. Light intensity was measured with a spherical light sensor (Li-Cor 193,Li-Cor, Lincoln, Nebraska, USA). For technical reasons, we could not measure lightintensity in the experimental containers. It is obvious that light intensity was somewhatreduced with increasing cellular abundance in the course of the experiments. If we assumethat light intensity ranged from 90 to 100 mol m2s1in the experimental containers, thisintensity corresponds to the light level that is common in the upper 5 m of the AML atLangau (Moser and Weisse 2011b). The experimental volume in each flask was 40 ml. Weperformed pairwise competition experiments between the two flagellates at four different pH(2.5, 3.5, 5.0, and 7.0) and at a temperature of 17.5 C. Prior to the beginning of theexperiments, the two flagellate strains were stepwise acclimated to the different pH at theexperimental temperature. The pH was adjusted by adding small amounts of 0.1 mol l1or1 mol l1NaOH or HCl, respectively. It was increased or decreased by 0.5 pH units per day,until the culture reached the final pH. The experimental cultures had been acclimated to theirfinal pH levels for at least 34 days. To minimize the risk of an initial lag-phase, flagellatecultures were diluted with MWC medium to reach the experimental abundances 34 h priorto the beginning of the experiments. All flagellate cultures were supplied with a wheat grainto stimulate bacterial growth thus providing saturating food levels.



SponsoredDocument

SponsoredDocument

SponsoredDocument


4/12

The competition experiments were designed to yield initial abundances of50,000 cells ml1of each of the two flagellate strains. Each experiment was run intriplicate and lasted for seven to eight days. The pH was measured at the beginning of theexperiments and thereafter twice a day. If the pH differed by more than 0.2 units from thetarget value, it was adjusted by the addition of small amounts of 0.1 mol l1or 1 mol l1

NaOH or HCl, respectively. All pH measurements were conducted with a pH meter (MettlerToledo, Seven Easy pH Meter S20) to the nearest 0.01 unit. The pH sensor was three-point

calibrated with standard buffer solutions of pH = 4.01, pH = 7.00, and pH = 9.21 prior toeach measurement.

Every 24 h, 4-ml subsamples from each experimental container were fixed with formalin(2%, vol/vol final concentration) for measurements of flagellate and bacterial abundances.Each time before pH measurement and subsampling, the culture flasks were shaken toprevent wall growth of the flagellates and cell clumping. Cell numbers of the two flagellatesand bacteria were measured with a flow cytometer (FacsCalibur, Becton Dickinson), usingthe software programmes Cellquest and Attractors (Becton Dickinson). In thecompetition experiments, the two flagellate strains differed according to their red vs. orangefluorescence signals and formed non-overlapping regions (gates) in the corresponding 2Ddot plots. Bacterial abundance was measured by means of their green fluorescence afterstaining with Syto 13 (Gasol and del Giorgio 2000).

Linear regression of ln cell numbers vs. time was used to assess the growth rates of theflagellates (, d1) over the period of exponential growth; was obtained as the slope(=regression coefficient) of the respective regression. Correlation coefficients of all linearregressions reported were significant (P< 0.05). Growth rates obtained in the competitionexperiments were pairwise compared (Student's t-test) to growth rates measured earlier insingle species experiments at the respective pH (Moser and Weisse 2011a). All statisticalanalyses were performed with Sigma Plot 11.0 and Sigma Stat 2.03 (SPSS Inc.).

Results

Irrespective of pH, cell numbers of both flagellate species decreased during the first 24 h ofthe experiments. In the experiment conducted at pH 2.5, cell numbers of both strains were

similar and relatively constant during the initial 4 days (Fig. 1A), ranging from 40,000 to65,000 cells ml1. Beginning on day 4 of the experiment, the abundance of Ochromonassp.increased exponentially until the end of the experiment. The slope of the regression linecorresponded to an average of 0.39 d1during days 38, i.e. growth of Ochromonassp. inthe competition experiment was not statistically different from when grown alone at pH 2.5(Fig. 2A). The final abundance of Ochromonassp. was close to 300,000 cells ml1, whilethe final abundance of P. malhamensiswas lower than at the beginning of the experiment.

At pH 3.5, cell numbers of both flagellate strains developed similarly. An initial lag-phasewas followed by an exponential phase that lasted for the following six days (Fig. 1B).Growth rates calculated from the regression equations were 0.25 d1for Ochromonassp.and 0.18 d1for P. malhamensis, i.e. growth rates of both species were significantly reduced(P= 0.003 and P= 0.001, respectively) relative to the single species experiments at the same

pH (Fig. 2).The experiments conducted at pH 5.0 and 7.0 yielded qualitatively similar results. After aninitial reduction of both flagellate populations, cell numbers of P. malhamensisincreasedexponentially. At pH 5.0, the exponential phase lasted until the end of the experiment (Fig.1C). At pH 7.0, the exponential growth phase of P. malhamensiswas restricted to the periodafter day 1 and before day 5 of the experiment (Fig. 1D). Growth rates derived from theregression lines were 0.31 d1at pH 5.0 and 0.58 d1at pH 7.0, i.e. significantly lower



SponsoredDocument

SponsoredDocument

SponsoredDocument


5/12

(P< 0.001 at pH 5.0; P= 0.008 at pH 7.0) than when the strain was grown without acompetitor (Fig. 2B).

Ochromonassp. showed a continuous weak increase from the third to the last day of theexperiment conducted at neutral pH (Fig. 1D). Growth rate calculated from the shortexponential phase between days 2 and 4 was 0.49 d1, which is not significantly differentfrom the single growth experiment (Fig. 2A). At pH 5.0, cell numbers of Ochromonassp.

remained constant between days 2 and 3, and then increased to reach final cell numbers thatwere close to the initial abundances (Fig. 1C). The linear regression yielded = 0.44 d1

during days 36, i.e. growth of Ochromonassp. was drastically reduced compared to itsgrowth rate measured in the respective single species experiment (Fig. 2A). Both at pH 5.0and 7.0, the final population sizes of Ochromonassp. were several times lower than those ofP. malhamensis.

Bacterial abundances ranged from 0.8 106to 10.7 106cells ml1in the course of thevarious experiments (Table 1). In all experiments, the final bacterial abundance exceededthe initial bacterial cell numbers.

Discussion

Although pH is a major environmental factor limiting the distribution of protist species inaquatic habitats (Packroff and Woelfl 2000; Weisse 2006), only a few studies investigatedthe pH response of protists experimentally (Boenigk 2008; Weisse and Stadler 2006; Weisseet al. 2007; this study). We reported the pH response of the two species used in the presentstudy and another Ochromonassp. isolated from a similar AML in Germany in a previousstudy (Moser and Weisse 2011a). This earlier work revealed that the Ochromonassp. strainfrom Langau showed maximum growth rates at pH 45 (= 1.41 0.19 d1) when grownalone. Growth rates of P. malhamensispeaked at pH 7.0 (= 0.73 0.09 d1) in thesesingle strain experiments. Growth rates of Ochromonassp. were significantly higher thanthat of P. malhamensisat all pH tested (2.5, 3.0, 3.5, 4.0, 5.0, 6.0 and 7.0) except at pH 3.5and 7.0 (Moser and Weisse 2011a).

Resource competition has been identified as a key process shaping the structure of aquaticfood webs (Belgrano et al. 2005; Gliwicz 2003) and has been studied experimentally sincethe pioneering work of Gause (1932, 1934). Several decades later, competition was studiedin much detail with freshwater autotrophic protists testing Tilman's mechanistic resourcecompetition theory (Tilman 1977, 1981). However, studies dealing with competitionbetween heterotrophic and mixotrophic protists, and between protists and multicellularorganisms are still rare. Rothhaupt (1996) demonstrated experimentally that Ochromonassp.is able to outcompete obligate bacterivorous flagellates in the light. Following up this study,Tittel et al. (2003) reported that an Ochromonassp. strain isolated from an AML inGermany (pH 2.63.3) is able to reduce its phagotrophic competitor, the ciliate Oxytrichasp., to low numbers in the light. These authors also reported a strong reduction of theflagellate's bacterial and algal prey in illuminated surface strata of its habitat.

To our knowledge this is the first study analyzing the competition of two different, butclosely related chrysomonad species in relation to pH. Since we know from our earlierexperiments (Moser and Weisse 2011a) that both species can survive at the entire pH rangefrom 2.5 to 7.0, the conditions for coexistence are met. It did not astonish that Ochromonassp. dominated over P. malhamensisat pH 2.5 and that the latter performed better than theformer at pH 7.0 because Ochromonassp. originated from a highly acidic environment andP. malhamensiswas isolated from a circumneutral lake. The main question was what willhappen when the two flagellate strains live in competition with each other under moderatelyto highly acidic conditions? At pH 3.5, growth rates of Ochromonassp. were slightly higher



SponsoredDocument

SponsoredDocument

SponsoredDocument


6/12

than that of P. malhamensis, thus confirming qualitatively our results measured in the singlespecies treatments (Fig. 2). Competition reduced of both species at a similar rate,compared to the single species experiments. Accordingly, the two chrysomonads coexistedat pH 3.5. Based upon our earlier results (Moser and Weisse 2011a), Ochromonassp. shouldbe the superior competitor in the competition experiments at pH 5.0 (Fig. 2). Contrary toexpectations, both species reached similar growth rates and coexisted during the experiment(Fig. 1C). The growth rate of P. malhamensiswas more constant and less reduced than that

of Ochromonassp., relative to the respective growth rates measured in the single speciesexperiments (Fig. 2). It appears unlikely that the numerical dominance of P. malhamensisatpH 5.0 was due to exploitative competition because this would imply that bacterial levelsfell below the satiating concentrations in the course of the experiments. This was not thecase in our experiments, because bacterial abundances remained at >2 106cells ml1in allexperiments conducted at pH 5.0. Final bacterial cell numbers even exceeded the initialabundances (Table 1). However, since we did not assess the bacterial species composition,we cannot rule out that some palatable bacterial strains were reduced in the course of theexperiment.

Caron et al. (1990) reported a bacterial threshold abundance of 1 106ml1, above whichP. malhamensisswitched nearly completely from phototrophic growth to heterotrophicgrowth. Sanders et al. (1990) measured slow growth (0.3 d1) of P. malhamensiswhen

grown phototrophically; even the maximum rate of photosynthesis accounted for only 7% ofthe total carbon budget of this mixotroph when sufficient bacteria were present. Sanders etal. (1990) considered phototrophic nutrition to be an evolutionary strategy for long-termsurvival of P. malhamensis. While light intensity and pH ranging from 4.0 to 7.9 had noeffect on phagotrophy, bacterial density was the primary factor influencing phagotrophicgrowth (Sanders et al. 1990). In our study, the bacterial concentrations did not fall below thereported threshold in the treatments at pH 3.5, 5.0, and 7.0 at any time. Similar to P.malhamensis, the preferred nutritional mode of Ochromonassp. isolated from AML isphagotrophy, both in the light and in the dark (Bochat et al. 2007; Schmidtke et al. 2006;Tittel et al. 2003). We conclude that both flagellates behaved phagotrophically in theexperiments reported in this study. Only in the experiment conducted at pH 2.5, bacterialabundance was close to and sometimes even below the threshold of 106bacteria ml1.Similar to Sanders et al. (1990), we observed survival but only negligible growth of P.

malhamensisat this low bacterial level. We conclude that P. malhamensiscannot reachsustainable growth if bacteria drop below 106cells ml1and light is limiting photosynthesis(


7/12

malhamensisis known to be cannibalistic (Caron et al. 1990) and can also ingest algae andother flagellates that may be even larger than itself (Pringsheim 1952; Zhang and Watanabe2001). Similarly, an Ochromonassp. isolated from an AML in Germany that is closelyrelated to the Ochromonassp. strain used in the present investigation (Moser and Weisse2011a) feeds on the larger green alga Chlamydomonassp. (Kamjunke et al. 2004; Tittel etal. 2003). Predation might thus be responsible for the reduction of the flagellates observed atthe beginning of the experiments at the two highest pH.

Another factor that may have played a role in the competition experiments is allelopathy.Allelopathic effects are known from species of both genera, i.e. OchromonasandPoterioochromonas(Blom and Pernthaler 2010; Boenigk and Stadler 2004). The productionand excretion of allelopathic secondary metabolites of P. malhamensishas toxic effects onrotifers that do not require ingestion of the flagellate (Boxhorn et al. 1998). Boenigk andStadler (2004) reported that heterotrophic and mixotrophic strains of these chrysomonadswere toxic to zooplankton at abundances exceeding 104flagellates ml1. In our experimentsthe flagellate abundances always exceeded the threshold of 104cells ml1. Recently, Blomand Pernthaler (2010) demonstrated that metabolites of P. malhamensismay selectivelyaffect the growth of some aquatic bacteria even in very small doses. Therefore, we cannotrule out that allelopathic secondary metabolites of the two flagellate strains influenced eachother either directly or indirectly, via their bacterial prey, in our competition experiments.

The results obtained support our hypothesis that, because Ochromonassp. is an inferiorcompetitor under neutral to moderately acidic conditions, it must take refuge fromcompetition in inhospitable habitats such as AML. We conclude that the competitive abilityof Ochromonassp. increases under suboptimal pH conditions because its potentialcompetitors are affected more strongly by the adverse conditions including low food levels.The competitors may have a higher bacterial threshold for phagotrophy than Ochromonassp. Ochromonassp. dominated over P. malhamensisonly at the lowest pH tested (2.5) thatwas close to the pH of its habitat of origin. Our results suggest that P. malhamensismay beexcluded from highly acidic environments if acidophilic or acidotolerant species such asOchromonassp. are present. To our knowledge, the genus Poterioochromonashas not yetbeen reported from extremely acidic mining lakes (pH < 3) (reviewed by Packroff andWoelfl (2000)).

The lack of more efficient competitors has been postulated as the primary reason for theobserved shift in the rotifer and crustacean species community with decreasing pH (Deneke2000; Wollmann et al. 2000). We provide the first experimental evidence that acidotolerantprotist species may also benefit from competitive release under acidic stress.

References

Aaronson S. Baker H. A comparative biochemical study of two species of Ochromonas. J. Protozool..1959; 6:282284.

Belgrano, A.; Scharler, U.M.; Dunne, J.; Ulanowicz, R.E. Oxford University Press; Oxford: 2005.Aquatic Food Webs An Ecosystem Approach.

Bennett S.J. Sanders R.W. Porter K.G. Heterotrophic, autotrophic, and mixotrophic nanoflagellates:

seasonal abundances and bacterivory in a eutrophic lake. Limnol. Oceanogr.. 1990; 35:18211832.Blom J. Pernthaler J. Antibiotic effects of three strains of chrysophytes (Ochromonas,

Poterioochromonas) on freshwater bacterial isolates. FEMS Microbiol. Ecol.. 2010; 71:281290.[PubMed: 19919604]

Bochat I.G. Weithoff G. Krger A. Gcker B. Adrian R. A biochemical explanation for the success ofmixotrophy in the flagellate Ochromonassp. Limnol. Oceanogr.. 2007; 52:16241632.



SponsoredDocument

SponsoredDocument

SponsoredDocument


8/12

Boenigk J. Stadler P. Potential toxicity of chrysophytes affiliated withPoterioochromonasand relatedSpumella-like flagellates. J. Plankton Res.. 2004; 26:15071514.

Boenigk J. Pfandl K. Stadler P. Chatzinotas A. High diversity of the Spumella-like flagellates: aninvestigation based on the SSU rRNA gene sequences of isolates from habitats located in sixdifferent geographic regions. Environ. Microbiol.. 2005; 7:685697. [PubMed: 15819851]

Boenigk J. Nanoflagellates: functional groups and intraspecific variation. Denisia. 2008; 23:331335.

Boxhorn J.E. Holen D.A. Boraas M.E. Toxicity of the chrysophyte flagellate Poterioochromonas

malhamenisto the rotifer Brachionus angularis. Hydrobiologia. 1998; 387/388:283287.Caron D.A. Porter K.G. Sanders R.W. Carbon, nitrogen, and phosphorus budgets for the mixotrophicphytoflagellate Poterioochromonas malhamensis(Chrysophyceae) during bacterial ingestion.Limnol. Oceanogr.. 1990; 35:433443.

Deneke R. Review of rotifers and crustaceans in highly acidic environments of pH values


9/12

Tilman D. Resource competition between planktonic algae: an experimental approach. Ecology. 1977;58:338348.

Tilman D. Test of resource competition theory using four species of Lake Michigan algae. Ecology.1981; 62:802815.

Tittel J. Bissinger V. Zippel B. Gaedke U. Bell E. Lorke A. Kamjunke N. Mixotrophs combineresource use to outcompete specialists: implications for aquatic food webs. Proc. Natl. Acad. Sci.U.S.A.. 2003; 100:1277612781. [PubMed: 14569026]

Weisse T. Freshwater ciliates as ecophysiological model organisms lessons from Daphnia, majorachievements, and future perspectives. Arch. Hydrobiol.. 2006; 167:371402.

Weisse T. Stadler P. Effect of pH on growth, cell volume, and production of freshwater ciliates, andimplications for their distribution. Limnol. Oceanogr.. 2006; 51:17081715.

Weisse T. Scheffel U. Stadler P. Foissner W. Local adaptation among geographically distant clones ofthe cosmopolitan freshwater ciliate Meseres corlissi. II. Response to pH. Aquat. Microb. Ecol..2007; 47:289297.

Weithoff G. Moser M. Kamjunke N. Gaedke U. Weisse T. Lake morphometry strongly shapes theplankton community structure in acidic mining lakes. Limnologica. 2010; 40:161166.

Wollmann K. Deneke R. Nixdorf B. Packroff G. Dynamics of planktonic food webs in three mininglakes across a pH gradient (pH 24). Hydrobiologia. 2000; 433:314.

Zhang X. Watanabe M.M. Grazing and growth of the mixotrophic chrysomonad Poterioochromonasmalhamensis(Chrysophyceae) feeding on algae. J. Phycol.. 2001; 37:738743.

Acknowledgments

We thank P. Stadler and U. Scheffel for technical assistance in the laboratory. This work was supported by theAustrian Science Fund (FWF Project P20118-B17).



SponsoredDocument

SponsoredDocument

SponsoredDocument


10/12


11/12

Fig. 2.

Growth rates of Ochromonassp. (A) and Poterioochromonas malhamensis(B) in thecompetition experiments reported in this study (hatched bars) compared to their growth ratesobtained by Moser and Weisse (2011a) in single species experiments (black bars). The barsindicate mean values of triplicates; the error bars denote 1 SD.



SponsoredDocument

SponsoredDocument

SponsoredDocument


12/12

SponsoredDocument

SponsoredDocument

SponsoredDocumen

t


Table 1

Bacterial abundance (in 106ml1) in the course of the experiments. The data shown are mean values oftriplicates 1 SD.

pH

Time (d) 2.5 3.5 5.0 7.0

0 1.10 1.26 3.55 2.58

1 1.40 0.41 2.10 1.46 2.45 0.17 10.70 6.64

2 0.87 0.24 5.36 2.78 2.62 1.02 7.04 1.68

3 1.03 0.34 10.20 5.04 6.56 2.53 5.33 0.44

4 0.82 0.13 10.60 5.13 3.40 0.97 4.51 1.78

6 1.64 0.17 6.86 3.45 2.70 1.71 4.81 1.99

7 1.36 0.28 3.67 2.12 10.40 3.27 4.91 1.19


jurnal isol ing

Documents