114 Annales Universitatis Paedagogicae Cracoviensis Studia Naturae, 2: 114–123, ISSN 2543-8832 DOI: 10.24917/25438832.2.9 Zofia Konarzewska, Sylwia Śliwińska-Wilczewska*, Adam Latała Institute of Oceanography, University of Gdańsk, Gdynia, Poland, *ocessl@edu.pl Allelopathic effect of the Baltic picocyanobacterium Synechococcus sp. on selected diatoms Introduction �e allelopathy phenomenon was originally de�ned as a harmful e�ect between plants. �is de�nition was used for the �rst time by Professor Hans Molisch (1937). As the result of the development of science and a better understanding of this phenomenon, the de�nition of allelopathy has evolved. �e International Allelopathy Society (IAS, 1996) established the de�nition of allelopathy as the process in which the compounds secreted by di�erent organism (vascular plant, algae, bacteria and fungi) in�uenced the growth and development of the both plant and animal organisms (Legrand et al., 2003). �ese chemical substances were called allelopathic compounds or allelochem- icals (Le�aive, Ten-Hage, 2007), and organisms used them to protection against pred- ators, and avoid competitors (Granéli et al., 2008). In aquatic ecosystems, allelopathic interactions are still not very well recognised, because the distance between organisms which are able to secreting secondary metab- olites is crucial to observe the allelopathic e�ect (Wolfe, 2000). Allelopathy in fresh- water, brackish, and marine ecosystems depends on the production and secretion of active allelopathic compounds and their e�ective spread to other organisms (Lew- is, 1986). �erefore, to demonstrate allelopathy between photoautotrophs, scientists need to perform a number of laboratory experiments. It has been proven that several groups of phytoplankton, such as cyanobacteria, dino�agellates, prymnesiophytes, green algae, and diatoms product allelopathic com- pounds (Subba Rao, Smith, 1995; Chiang et al., 2004; Żak, Kosakowska, 2015). More- over, published data indicated that allelopathic e�ects have the competitive advantage of some phytoplankton species by eliminating physiologically more sensitive species (Sarkar et al., 2006). Moreover, the structure of phytoplankton (Legrand et al., 2003) and the formation of cyanobacterial and algal blooms may be determined by allelopathic 115 interactions (Smayda, 1997; Weissbach et al., 2010). Massive and harmful cyanobacte- rial and algal blooms are a serious problem a�ecting not only the ecology but also the economy of the aquatic ecosystem (Anderson, 1989; Anderson et al., 2002). Massive blooms are formed by cyanobacteria (also picocyanobacteria from the genus Synechoc- occus), green algae, dino�agellates, and diatoms (Beardall, 2008; Błaszczyk et al., 2010). Little is known about the in�uence of cyanobacteria on diatoms (Sivonen, Jones 1999), and the speci�c mechanism of action of the allelopathic interactions is unexam- ined. It is impossible to demonstrate allelopathy in natural conditions, which is why it is important to contribute controlled experiments in laboratory environment. �ere- fore, in this study, we investigated the allelopathic e�ect of picocyanobacterium Syne- chococcus sp. on diatoms Nitzschia fonticola (Grunow) Grunow, Fistulifera saprophila (Lange-Bertalot & Bonik) Lange-Bertalot, Navicula perminuta Grunow and Amphora co�eaeformis (C.Agardh) Kützing. In this study, the in�uence of picocyanobacteria was examined by adding the cell-free �ltrate of Synechococcus sp. to studied diatoms. �e re- sults of this experiment may provide further information about allelopathic interactions between cyanobacteria and diatoms, which could be important to the understanding of cyanobacterial and algal blooms in aquatic ecosystems, including the Baltic Sea. Material and methods �e experiments were conducted on the strain of picocyanobacterium Synechococcus sp. (BA-124) and four diatoms: Nitzschia fonticola (BA-34), Fistulifera saprophila (BA- 56), Navicula perminuta (BA-30), and Amphora co�eaeformis (BA-16) (Fig. 1). �ese species are typical representatives of Baltic diatoms; therefore, they were selected for the allelopathic experiment. �e strains were isolated from the coastal zone of the Gulf of Gdańsk (southern Baltic Sea) and are maintained as uni-algal cultures in the Cul- ture Collection of Baltic Algae (CCBA) at the Institute of Oceanography, University of Gdańsk, Poland (Latała et al., 2006). �e tests on the ‘batch cultures’ were carried out in 25 mL glass Erlenmeyer �asks containing sterilised f/2 medium (Guillard, 1975). �e media were prepared from Baltic water, which was �ltered through Whatman GF/C glass �bre �lters, and autoclaved. Analysed organisms were grown 7 days in constant conditions of 18°C and 8 psu, under a 16:8 h light : dark cycle at 10 μmol photons·m-2 s-1 and this were the control treatment conditions. Fluorescent lamps (Cool White 40W, Sylvania, USA) were used as source of irradiance. �e intensity of PAR was measured using a LI-COR quantum-meter with a cosine collector. �e donor and target organisms were acclimated to these culture conditions for 7 days; a�erwards, ac- tively growing cultures were used for the establishment of the allelopathic experiment. Allelopathic interactions in monocultures were determined by using the modi�ed method proposed by Suikkanen et al. (2004). Allelopathic interaction A llelopathic effect of the B altic picocyanobacterium Synechococcus sp. on selected diatom s Zo fia K on ar ze w sk a, S yl w ia Ś liw iń sk a- W ilc ze w sk a, A da m L at ał a 116 was studied by adding the �ltrate obtained from the picocyanobacterial culture of Synechococcus sp. BA-124 to tested diatoms. �e culture of picocyanobacteria was �ltered through 0.45-µm pore size Macherey-Nagel MN GF-5 �lters. �e cell- free �ltrate (V = 10 mL) was added to 25 mL Erlenmeyer �asks containing the tested diatoms (V = 10 mL). In all experiments, the ratio of picocyanobacterium to target species in Erlenmeyer �asks was adjusted to 1:1, based on the chlorophyll a content (�nal chlorophyll a concentration in the experimental cultures was 0.4 µg chl a mL-1). Control samples were prepared by adding mineral medium f/2 with a volume equal to the added cell-free �ltrate. Tests were conducted in triplicate, and all analysed species were obtained from early exponential growth phase. �e number of cells was counted using �ow cytometer BD Accuri™ C6 Plus. Events are recorded in list mode. To avoid generating large �les, samples can be run for 40s at a delivery rate of 14 µl·min-1, and the number of events is kept at less than 1000 per second. Events are recorded in standard �lters: 670 LP (Detector FL3) and 675/25 (Detector FL4) (Marie et al., 2005). �e number of cells in the experimental cultures was determined a�er the 1st and 7th day of the diatoms exposure to the picocyanobacterial �ltrate. Fig. 1. Diatoms strains used in this study: Nitzschia fonticola (A), Fistulifera saprophila (B), Navicula perminuta (C) and Amphora co�eaeformis (D); scale bars = 10 µm A B C D 117 Chlorophyll a �uorescence was measured with a Pulse Amplitude Modulation (PAM) �uorometer (FMS1, Hansatech), using a 594 nm amber modulating beam with 4 step frequency control as a measuring light. Analysed species were taken for chlorophyll �uorescence analysis a�er the 7th day of exposure to the �ltrate. Before measurements, each sample taken from the culture was �ltered through 13 mm glass �bre �lters (Whatman GF/C). Before starting the experiment, the �lter sample was adapted in the dark for about 10 minutes. �e maximum quantum yield of PSII pho- tochemistry (Fv/Fm) and e�ective quantum yield of PSII photochemistry (ΦPSII) was calculated (Campbell et al., 1998). Analysis of variance (one-way ANOVA) was used to test for di�erences in an- alysed parameters between the target cultures treated with picocyanobacterial cell- free �ltrates and the control over the experimental period. Data are reported as mean ± standard deviation (SD). Levels of signi�cance were * p < 0.05. �e statistical analy- ses were performed using the Statistica® 13.1 so�ware. Results �e e�ect of the cell-free �ltrate addition obtained from Synechococcus sp. cultures on the growth of analysed diatoms Nitzschia fonticola, Fistulifera saprophila, Navicula perminuta and Amphora co�eaeformis a�er 1 and 7 days of exposition to the �ltrates Fig. 2. �e e�ect of the addition of cell-free �ltrate from Synechococcus sp. BA-124 cultures on the growth of Nitzschia fonticola (A), Fistulifera saprophila (B), Navicula perminuta (C) and Amphora co�e- aeformis (D) a�er the 1st and 7th days of exposition, expressed as a number of cells (N). �e values refer to means (n = 3, mean ± SD); asterisk indicates signi�cant di�erence compared with control (p < 0.05) A llelopathic effect of the B altic picocyanobacterium Synechococcus sp. on selected diatom s Zo fia K on ar ze w sk a, S yl w ia Ś liw iń sk a- W ilc ze w sk a, A da m L at ał a 118 are shown in �gure 2. �e results showed that addition of cell-free �ltrate from Syn- echococcus sp. increased the number of cells of N. fonticola and F. saprophila com- pared to their control. A�er the 7th day of the experiment for a �ltrate addition, growth stimulation of N. fonticola and F. saprophila constituted 105% and 107%, respectively (ANOVA, p < 0.05). In addition, it was observed that the cell-free �ltrate obtained from picocyanobacterium did not a�ect the number of cells of N. perminuta and A. co�eaeformis (ANOVA, p > 0.05). �e e�ect of the addition of cell-free �ltrate from Synechococcus sp. cultures on the �uorescence parameters Fv/Fm and ФPSII of analysed diatoms a�er one week of exposition is showed in �gure 3. �e study indicated that the addition of cell-free �ltrate obtained from Synechococcus sp. signi�cantly a�ected the Fv/Fm and ФPSII of N. fonticola and N. perminuta. A�er the 7th day of exposition, it was noted that the addition of the �ltrate resulted in increase of �uorescence parameters of analysed dia- toms, which was higher by 29% and 4%, respectively, for Fv/Fm and 56% and 14%, re- spectively for ФPSII, compared to a control (ANOVA, p < 0.05). Based on the results, it was found that the �ltrate obtained from Synechococcus sp. also caused signi�cant changes of the ФPSII value of F. saprophila. A�er one week of the experiment, the �u- orescence parameter of this diatom was higher by 6%, compared to control (ANOVA, p < 0.05). On the other hand, it was noted that �ltrate obtained from picocyanobacte- rium caused the inhibition of the Fv/Fm parameter of A. co�eaeformis, which constitut- ed 96% (ANOVA, p < 0.05). Fig. 3. �e e�ect of the addition of cell-free �ltrate from Synechococcus sp. BA-124 cultures on the �uo- rescence parameters Fv/Fm and ФPSII of Nitzschia fonticola (A), Fistulifera saprophila (B), Navicula per- minuta (C) and Amphora co�eaeformis (D) a�er the 7th day of exposition; the values refer to means (n = 3, mean ± SD); asterisk indicates signi�cant di�erence compared with control (p < 0.05) 119 Discussion It is believed that cyanobacterial allelopathy may be one of the important factors af- fecting the formation of massive algal blooms in the aquatic ecosystems (e.g., Antunes et al., 2012; Rzymski et al., 2014). Picocyanobacteria plays an important role in aquatic ecosystems but not much is known about their allelopathic activity. �ere- fore, the main aim of this study was to investigate the allelopathic e�ect of picocy- anobacterium Synechococcus sp. on growth and �uorescence parameters of Nitzschia fonticola, Fistulifera saprophila, Navicula perminuta, and Amphora co�eaeformis. Allelopathic e�ects of the growth of the target organism by the production allelo- pathic compounds are the most frequently reported mode of the action of cyanobac- teria and microalgae (Rzymski et al., 2014). In this study, we have also demonstrated that picocyanobacterium caused allelopathic e�ects against Baltic diatoms. �e results showed that addition of cell-free �ltrate from Synechococcus sp. increased the number of cells of N. fonticola and F. saprophila. In addition, it was observed that the cell-free �ltrate obtained from picocyanobacterium did not a�ect the number of cells of N. perminuta and A. co�eaeformis. Only a few studies have documented the in�uence of the allelopathic e�ect of cyanobacteria on diatoms species. Information about the allelopathic interactions of Synechococcus sp. on Baltic diatom N. preminuta was de- scribed by Śliwińska-Wilczewska et al. (2016). In this study, the authors demonstrated that the addition of the cell-free �ltrate obtained from the picocyanobacterium had an inhibitory e�ect on analysed diatom. Moreover, the study reveals that allelopathic ac- tivity was regulated by the intensity of light, temperature, and salinity. Keating (1977, 1978) also demonstrated the growth inhibition of selected diatom by the addition of �ltrate obtained from a lake in which cyanobacteria was dominated. Similar results were reported by La�orgue et al. (1995), who showed that the low biomass of Fragilar- ia crotonensis Kitton in Lake Aydat was the result of the allelochemicals obtained from Anabaena sp. More detailed data on the allelopathic e�ects of Baltic cyanobacteria on diatoms were provided by Suikkanen et al. (2004). In this study, the allelopathic e�ects of Baltic Nodularia spumigena Mertens ex Bornet & Flahault, Anabaena lem- mermannii P.G.Richter and Aphanizomenon �osaquae Ralfs ex Bornet & Flahault on the diatom �alassiosira weiss�ogii (Grunow) G.Fryxell & Hasle were demonstrated. �e authors showed that, a�er a single addition of the �ltrate, all three analysed cyano- bacteria had a generally negative e�ect on the tested diatom. Moreover, on the basis of the research, it was noted that the diatom of T. weiss�ogii showed some tolerance for a single addition of the �ltrate, but its growth a�er repeated additions of the �ltrate was signi�cantly inhibited. Di�erent characteristics, such as membrane permeability, may contribute to the sensitivity of some phytoplankton species to allelopathic compounds (Suikkanen et al., 2004). �e sensitivity of organisms may also depend on the nature of A llelopathic effect of the B altic picocyanobacterium Synechococcus sp. on selected diatom s Zo fia K on ar ze w sk a, S yl w ia Ś liw iń sk a- W ilc ze w sk a, A da m L at ał a 120 allelopathic compounds to which they are exposed, because the same target organisms may react di�erently to the �ltrate derived from di�erent donor organisms. �ere are also only a few reports on the growth stimulation of target organisms caused by allelochemicals produced by cyanobacteria. Suikkanen et al. (2005) showed that some Baltic cyanobacteria may stimulate natural plankton communities. �e authors found that the addition of N. spumigena �ltrate signi�cantly increased the numbers of cells of N. spumigena and Anabaena sp. In our study, allelochemicals pro- duced by Synechococcus sp. had the stimulatory e�ects on the growth of diatoms N. fonticola and F. saprophila. �is indicated that the picocyanobacteria released some compounds that accelerated the growth of selected and co-existing diatoms. Another possible e�ect of allelopathic compounds is their e�ect on the photosyn- thetic activity of target organisms. Measurements of chlorophyll a �uorescence are non-invasive methods. Moreover, �uorescence measurements are a useful tool in the study of the allelopathy and ecophysiology of cyanobacteria and microalgae (Prince et al., 2008). In this study, it was found that the addition of �ltrate stimulated and inhibited the �uorescence parameters Fv/Fm and ΦPSII of analysed diatoms. Pub- lished data indicated that the allelopathic compounds produced and released by some cyanobacteria can a�ect the photosynthesis, and detailed studies have shown that they act mainly on the photosystem II (PSII). Issa (1999) presented the inhibitory e�ect of the donor Oscillatoria sp. and Calothrix sp. on photosynthesis of Chlorella fusca Shihira & R.W.Krauss. More detailed studies were conducted Prince et al. (2008). �e authors analysed the impact of Karenia brevis (C.C.Davis) Gert Hansen & Ø.Moes- trup on �uorescence parameter Fv/Fm of target diatoms Amphora sp., Asterionellopsis glacialis (Castracane) Round and Skeletonema costatum (Greville) Cleve. Inhibition of photosynthetic yield by extract obtained from K. brevis coincided with a negative e�ect on the growth of target organisms. �e e�ect of allelopathic compounds may be due to the di�erent sensitivity of the target species (Mulderij et al., 2003), and this may explained the dominance of some species over other photoautotrophs. 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(2015). �e in�uence of extracellular compounds produced by selected Baltic cyano- bacteria, diatoms and dino�agellates on growth of green algae Chlorella vulgaris. Estuarine, Coastal and Shelf Science, 167, 113–118. DOI: 10.1016/j.ecss.2015.07.038 Abstract It is commonly believed that the structure of phytoplankton and the formation of cyanobacterial and algal blooms may be explained by allelopathic interactions. �e main aim of this study was to investigate the al- lelopathic e�ect of picocyanobacterium Synechococcus sp. on the following growth and �uorescence param- eters: the maximum quantum yield of PSII photochemistry (Fv/Fm), and the e�ective quantum yield of PSII photochemistry (ΦPSII) of selected diatoms – Nitzschia fonticola, Fistulifera saprophila, Navicula perminuta and Amphora co�eaeformis. In this study, it was demonstrated that picocyanobacterium caused allelopathic 123 e�ects against Baltic diatoms. �e results showed that the addition of cell-free �ltrate from Synechococcus sp. increased the number of cells of N. fonticola and F. saprophila. Moreover, it was found that picocyano- bacterium was stimulated �uorescence parameters of N. fonticola, F. saprophila, and N. perminuta. On the other hand, it was noted that �ltrate obtained from picocyanobacterium caused the inhibition of Fv/Fm parameter of A. co�eaeformis. �e results of this experiment may provide further information about allelo- pathic interactions between Baltic picocyanobacteria and diatoms that are crucial to the understanding of algal blooms in aquatic ecosystems. Key words: allelopathy, Baltic Sea, diatom, growth, �uorescence, picocyanobacteria Received: [2017.07.22] Accepted: [2017.10.27] Zjawisko oddziaływania allelopatycznego bałtyckiej pikoplanktonowej sinicy Synechococcus sp. na wybrane gatunki okrzemek Streszczenie Powszechnie uważa się, że oddziaływanie allelopatyczne może mieć wpływ na strukturę �toplanktonu oraz tworzenie masowych zakwitów sinic oraz mikroglonów. Głównym celem niniejszych badań było wykaza- nie oddziaływania allelopatycznego pikoplanktonowej sinicy Synechococcus sp. na wzrost oraz parametry �uorescencji, charakteryzujące maksymalną wydajność fotosystemu II (Fv/Fm) oraz rzeczywistą wydajność fotosystemu II na świetle (ΦPSII) wybranych gatunków okrzemek: Nitzschia fonticola, Fistulifera saprophila, Navicula perminuta i Amphora co�eaeformis. Zaobserwowano, że pikoplanktonowa sinica wykazywała al- lelopatyczne właściwości na badane bałtyckie okrzemki. Na podstawie uzyskanych danych zanotowano, że dodanie przesączu z sinicy Synechococcus sp. stymulowało wzrost N. fonticola i F. saprophila. Ponadto zaob- serwowano znaczący wzrost parametrów �uorescencji u N. fonticola, F. saprophila i N. perminuta. W pracy również wykazano, że przesącz powodował obniżenie wartości parametru Fv/Fm u A. co�eaeformis. Wyniki uzyskane w niniejszej pracy dostarczają szerszych informacji odnoście oddziaływania allelopatycznego, wy- stępującego pomiędzy wybranymi gatunkami sinic i okrzemek, które w znaczący sposób mogą przyczynić się do zrozumienia pojawiających się w wielu ekosystemach wodnych masowych zakwitów sinic i mikroglonów. Słowa kluczowe: allelopatia, Morze Bałtyckie, okrzemki, wzrost, �uorescencja, pikoplanktonowe sinice Information on the authors Zo�a Konarzewska �e �eld of her interest is allelopathic interactions of picocyanobacterium Synechococcus sp. and Baltic diatoms in monocultures. In her studies, she uses �ow cytometer and PAM �uorymetry to determine allelopathic interactions between picocyanobacteria and selected diatoms – Nitzschia fonticola, Fistulifera saprophila, Navicula perminuta and Amphora co�eaeformis. Sylwia Śliwińska-Wilczewska In her research, she is interested in the allelopathy of cyanobacteria and microalgae, and particularly picocyanobacteria Synechococcus sp. Allelopathy plays an important role in interspeci�c competition and contributes to cyanobacterial bloom maintenance. In her study, the in�uences of allelochemicals on the growth, chlorophyll �uorescence, and photosynthesis irradiance curves of di�erent phytoplankton spe- cies were investigated. She is also investigating what in�uences environmental factors have on produced allelopathic compounds on algae and cyanobacteria. Adam Latała His subjects of research include wide experience in the ecophysiology and ecotoxicology of marine ben- thic and planktonic algae, the in�uence of the main environmental factors such as salinity, temperature, and light on the photosynthesis, photoacclimation, �uorescence, respiration, and growth of algae from natural communities and cultured under laboratory conditions, and the use of �uorescence techniques to study algal and cyanobacterial ecophysiology and ecotoxicology. A llelopathic effect of the B altic picocyanobacterium Synechococcus sp. on selected diatom s