124 Annales Universitatis Paedagogicae Cracoviensis Studia Naturae, 2: 124–134, 2017, ISSN 2543-8832 DOI: 10.24917/25438832.2.10 Sylwia Śliwińska-Wilczewska*, Arkadiusz Knitter, Daria Cisło, Adam Latała Institute of Oceanography, University of Gdansk, Gdynia, Poland; *ocessl@edu.pl Allelopathic activity of the Baltic picocyanobacterium Synechocystis sp. Introduction �e term “allelopathy” as �rst de�ned by Molisch (1937), who indicated that these are positive or negative biochemical interactions between plants. Rice (1979) included into this de�nition the interaction between micro-organisms, and Inderjit and Dak- shini (1994) indicated that allelopathic activity is also present in the aquatic environ- ment, especially between phytoplankton species. Allelopathic interaction is widespread and can occur in all aquatic ecosystems (Gross, 2003). Moreover, cyanobacterial allelopathy can be found in all aquatic envi- ronments where these primary producers are able to release active allelopathic com- pounds which can a�ect the functioning of the whole ecosystem (Żak, Kosakowska, 2015). Production of these allelopathic compounds is an important adaptation by which some cyanobacteria can achieve a competitive advantage over other primary producers (Poniedziałek et al., 2015). Allelopathy may be also one of the factors af- fecting the formation of massive and harmful cyanobacterial blooms in aquatic en- vironments. Over the past few decades, the world’s coastal waters have experienced an increase in the number of harmful bloom events (Anderson et al., 2012). Recent studies indicate that blooms of picocyanobacteria have grown signi�cantly in the last decades (Sorokin, Zakuskina, 2010), so it is important to determine the allelopathic interactions between the dominant species of picocyanobacteria. �e production and release of allelopathic compounds is an intriguing concept in which substances are secreted by the interacting species. Cyanobacteria are e�ective producers of many bioactive metabolites, including both acute toxins and allelopathic compounds (Burja et al., 2001; Berry et al., 2008; Leão et al., 2012). Mazur-Marzec et al. (2015) described Baltic cyanobacteria as a rich source of novel metabolites, e.g., cura- cin A, apratoxin D, dolastatin 10 and largazole, and di�erent peptides, e.g., anabaeno- peptins, cyanopeptolins, aeruginosins, spumigins, and nostocyclopeptides. However, 125 A llelopathic activity of the B altic picocyanobacterium Synechocystis sp. many of cyanobacteria remain unknown. Moreover, production of allelopathic sub- stances is common, but not identical for all species forming massive blooms, and there are no clear reasons for the synthesis of these compounds (Gross, 2003; Legrand et al., 2003). It is possible that their function enables the deterrence of predators and the inhibition of co-occurring species of phytoplankton (Liu et al., 2010). In addition, it is suggested that in the Baltic Sea cyanobacterial allelopathy may cause their dominance a�er the maximum concentration of cells is formed by environmental factors (Suikka- nen et al., 2004). Moreover, available studies indicate that the Baltic cyanobacteria may be allelopathic to other species, and this e�ect is dependent not only on the selected species, but even a strain of cyanobacteria (Śliwińska et al., 2011). �e use of biological tests is the �rst step in identifying which group of allelopathic compounds is respon- sible for causing harmful e�ects in the aquatic environment (Fistarol et al., 2004). �e main aim of this study was to estimate the allelopathic interaction between di�erent Baltic strains of picocyanobacteria of the genus Synechocystis. In this study, the in�uence of allelopathic compounds on the growth of analysed species was inves- tigated in monocultures and in mixed cultures. �ese results indicate that the allelo- pathic e�ect of Synechocystis sp. may be connected with the formation of a massive cyanobacterial bloom of these organisms in many aquatic ecosystems. Material and methods �e experiments were conducted on the three strains of the picocyanobacteria of the genus Synechocystis (BA-121, BA-122 and BA-153) (Fig. 1). �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 Culture 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 with a sa- linity of 8 psu, which was �ltered through Whatman GF/C glass �bre �lters, and autoclaved. Analysed picocyanobacteria were grown 7 days in constant conditions of 20°C and 8 psu, under a 16:8 h light:dark cycle at 10 μmol photons m-2s-1 and these were the control treatment conditions. Fluorescent lamps (Cool White 40W, Sylvania, USA) were used as a source of irradiance. �e intensity of PAR was measured using a LI-COR quantum-meter with a cosine collector. �e donor and target picocyano- bacteria were acclimated to these culture conditions for 7 days; a�erwards, actively 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 was studied by adding the �ltrate obtained from picocyanobacterial culture of S yl w ia Ś liw iń sk a- W ilc ze w sk a, A rk ad iu sz K ni tte r, D ar ia C is ło , A da m L at ał a 126 Synechocystis sp. BA-153 to tested picocyanobacteria Synechocystis sp. BA-121 and BA-122. �e culture of BA-153 was �ltered through 0.45-µm pore size Macherey-Nagel MN GF-5 �lters. �e cell-free �ltrate (V = 2 mL) was added to 25 mL Erlenmeyer �asks containing the tested cyanobacteria (V = 20 mL). In all experiments, the ratio of picocyanobacterium to target species in Erlenmeyer �asks was adjusted to 1:1 based on the chlorophyll a (Chl a) content (�nal Chl 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. �e number of cells in the experimental cultures was determined a�er the 1st and 7th day of the cyanobacteria exposure to the picocyanobacterial �ltrate. Tests were conducted in triplicate and all analysed species were obtained from the early exponential growth phase. Allelopathic interactions in mixed cultures were determined by using the modi�ed method proposed by Ji et al. (2011). Allelopathic activity was studied by adding the culture of donor picocyanobacteria Synechocystis sp. BA-153 to the tested organisms: Synechocystis sp. BA-121 or BA-122. In all experiments, the �nal Chl a concentration in the experimental cultures was 0.4 µg Chl a mL-1. �e culture of donor picocyanobacteria (V = 2 mL) was added to 25 mL Erlenmeyer �asks containing the tested cyanobacteria (V = 20 mL). As controls, both Synechocystis sp. BA-121 and BA-122 were cultured individually. Controls consisted in the addition of 2 mL of �ltrated f/2 medium to 25 mL Erlenmeyer �asks containing 20 mL of cell suspensions of the same cyanobacteria species. We measured the change in the density of target picocyanobacteria by directly counting the number of cells a�er the 1st and 7th day. �ree replicate �asks were used for each treatment, and all analysed species were obtained from the early exponential growth phase. �e experiments lasted 7 days. �e number of cells was counted using �ow cytometer BD Accuri™ C6 Plus (Fig. 2, 3). 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 1.000 per second. Events are recorded in standard �lters: 670 LP (Detector FL3) and 675/25 (Detector FL4) (Marie et al., 2005). Fig. 1. Picocyanobacterial strains of the genus Synechocystis used in this study: A) BA-121, B) BA-122 and C) BA-153. Scale bars = 10 µm 127 Analysis of variance (ANOVA) was used to test for di�erences in analysed pa- rameters between the target cultures treated with picocyanobacterial cell-free �ltrates or living cells and the control over the experimental period. A post hoc test (Tukeys HSD) was used to show which treatments for growth signi�cantly di�ered from the control and from each other. Data are reported as mean ± standard deviation (SD). Levels of signi�cance were * p < 0.05. �e statistical analyses were performed using the Statistica® 13.1 so�ware. Results �e e�ect of the cell-free �ltrate addition obtained from strain of Synechocystis BA-153 on the growth of Synechocystis BA-121 and BA-122 a�er 1 and 7 days of exposition to the �ltrates are shown in �gure 4. �e results demonstrated that the addition of A llelopathic activity of the B altic picocyanobacterium Synechocystis sp. Fig. 3. Cytograms obtained with mixed cultures of picocyanobacterial strains of the genus Synechocystis analysed using a BD Accuri™ C6 Plus �ow cytometer Fig. 2. Cytograms obtained with monocultures of three picocyanobacterial strains of the genus Synecho- cystis: A) BA-121, B) BA-122 and C) BA-153 analysed using a BD Accuri™ C6 Plus �ow cytometer S yl w ia Ś liw iń sk a- W ilc ze w sk a, A rk ad iu sz K ni tte r, D ar ia C is ło , A da m L at ał a 128 cell-free �ltrate from BA-153 decreased the number of cells of BA-121 compared to their control. A�er the �rst day of the experiment, for a �ltrate addition obtained from Synechocystis sp. BA-153 growth inhibition of Synechocystis sp. BA-121 expressed as a percent of culture density (% of control) constituted 45% (p < 0.05). On the other hand, it was found that the addition of �ltrate obtained from Synechocystis sp. BA-153 did not a�ect the number of cells of Synechocystis sp. BA-121 a�er 7 day of exposition (p > 0.05; Fig. 4A). In addition, it was observed that the cell-free �ltrate obtained from Synechocystis sp. BA-153 did not a�ect the number of cells of Synechocystis sp. BA-122 (p > 0.05, Fig. 4B). Fig. 5. �e e�ect of the addition of living cells from Synechocystis sp. BA-153 cultures on the growth of A) Synechocystis sp. BA-121 and B) Synechocystis sp. BA-122 a�er 1st and 7th day 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) Fig. 4. �e e�ect of the addition of cell-free �ltrate from Synechocystis sp. BA-153 cultures on the growth of A) Synechocystis sp. BA-121 and B) Synechocystis sp. BA-122 a�er 1st and 7th day of exposition, ex- pressed as a number of cells (N). �e values refer to means (n = 3, mean ± SD). Asterisk indicates signif- icant di�erence compared with control (p < 0.05) N um be r o f c el ls (N ∙ 10 5 ) Time (d) Time (d) N um be r o f c el ls (N ∙ 10 5 ) Time (d) A A B B 129 A�er the addition of live cells of the strain Synechocystis BA-153 to Synechocystis BA-121 culture, the decline in growth was observed (Fig. 5A). On the 1st day of the experiment, the minimum cell response of Synechocystis sp. BA-121 constituted 40% (p < 0.05) in comparison to the control treatment. On the other hand, the addition of live cells of strain Synechocystis BA-153 culture stimulated the growth of Synechocyst- is sp. BA-122, and at 7th day of experiment growth increased by 94% relative to control (p < 0.05, Fig. 5B) Discussion �e study of the allelopathy phenomenon focuses mainly on understanding the e�ects of allelopathic compounds on a variety of target organisms. �e modes of the action of allelochemicals depend on the nature of the interaction between donor and target organisms and the activity of these compounds. �ere are some reports of allelopathic e�ects, such as growth stimulation or inhibition caused by di�erent cyanobacteria (Suikkanen et al., 2006), but no information about the allelopathic potential of Baltic picocyanobacterium of genus Synechocystis on co-existing picocyanobacterial strains has been found. �erefore, the main goal of this study was to investigate the in�uence of metabolites obtained from picocyanobacterium Synechocystis sp. in monocultures and in mixed cultures. In most cases, allelopathic compounds cause the death of target organisms or re- duce their growth rate and biomass (Rzymski et al., 2014). Moreover, inhibition of the growth of the target organism by production allelopathic compounds is relatively widespread and the most frequently reported mode of action of cyanobacteria (Issa, 1999; Schagerl et al., 2002). In this study, we have demonstrated that the picocyano- bacterium strain of the genus Synechocystis BA-153 caused allelopathic e�ects against other strains of picocyanobacteria. It was found that strain BA-121 was strongly in- hibited by strain BA-153 in both the mixed culture and cell-free �ltrates. Picocy- anobacteria plays an important role in aquatic ecosystems but not much is known about their allelopathic activity. Information about the ability to allelopathic inter- actions of other picocyanobacterium Synechococcus sp. was described by Śliwińs- ka-Wilczewska et al. (2016a). In this study, the authors showed that the addition of the cell-free �ltrate obtained from the Baltic picocyanobacterium Synechococcus sp. had a signi�cant inhibitory e�ect on Nodularia spumigena. Additionally, Śliwińska-Wil- czewska et al. (2016b) showed the sensitivity of the diatom Navicula perminuta to allelopathic compounds produced by this picocyanobacterium. In this study, it was demonstrated that analysed picocyanobacterium reveals allelopathic activity that was regulated by the intensity of light, temperature, and salinity. Śliwińska et al. (2011) also showed that all analysed strains of Synechococcus sp. demonstrated the allelop- A llelopathic activity of the B altic picocyanobacterium Synechocystis sp. S yl w ia Ś liw iń sk a- W ilc ze w sk a, A rk ad iu sz K ni tte r, D ar ia C is ło , A da m L at ał a 130 athic activity and signi�cantly decreased the number of cells of Chlorella vulgaris. �e authors concluded that all three strains of Baltic picocyanobacterium from the genus Synechococcus (BA-120, BA-124, and BA-132) showed allelopathic activity; however, the BA-124 strain had the greatest negative impact on the growth of analysed green al- gae C. vulgaris. Moreover, Martins et al. (2008) describe the biological activities of ma- rine cyanobacteria strains belonging to the genus Synechocystis and Synechococcus iso- lated from Atlantic coast of Portugal. �e authors screened marine picocyanobacterial secondary metabolites for cytotoxic activity using primary rat hepatocytes and human HL-60 cells. In this study, the authors showed that marine picocyanobacterial strains of the genus Synechocystis and Synechococcus produce substances with inhibitory ef- fects on prokaryotic cells and with apoptotic activity in eukaryote cell lines. Moreover, Hamilton et al., (2014) demonstrated a signi�cant e�ect of Synechococcus strain on dark preference of black perch Embiotoca jacksoni. Costa et al. (2015) demonstrated that marine picocyanobacterium Cyanobium sp. inhibited Nannochloropsis sp. growth. Moreover, Paz-Yepes et al. (2013) have found a clear growth impairment of two strains of Synechococcus sp. (CC9311 and WH8102) when they are cultured in the presence of Synechococcus sp. CC9605. It is believed that selective inhibition of the growth of the target organism may a�ect the succession of selected cyanobacteria in an aquatic ecosystem (Legrand et al., 2003). Our results showed that Synechocystis allelopathy should be considered when estimating the potential interactions between picocyano- bacteria in aquatic ecosystems. Moreover, the results may in part explain the reasons for achieving a competitive advantage of picocyanobacterium Synechocystis in many aquatic ecosystems, including the Baltic Sea. It was also found that the addition of live cells of picocyanobacterium strain BA-153 stimulated the growth of Synechocystis sp. BA-122. Suikkanen et al. (2005) also indicated that cyanobacteria may stimulate natural plankton assemblages. �e authors showed that cyanobacterial �ltrates stimulated other cyanobacteria in the community. �e numbers of Snowella sp. and Pseudanabaena sp. were signi�cant- ly higher in all cyanobacterial treatments than in the control. Moreover, the addition of N. spumigena �ltrate signi�cantly increased the numbers of both N. spumigena and Anabaena sp. and Aphanizomenon sp. �ltrate and caused an over 50-fold increase in the cell numbers of Aphanizomenon sp. in the community. In the present study, picocyanobacterial exudates had the stimulatory e�ects on the growth of other picocyanobacterium from the same genus. �is suggests that the cyanobacteria released some autostimulatory, which accelerated the growth of the same and re- lated species. Our results con�rm that the picocyanobacterium Synechocystis sp. BA-153 is able to produced allelopathic compounds. Unfortunately, information on which metabolites mediate this and many other known allelopathic interactions are still scarce (Leão et 131 al., 2012). �e identi�cation and isolation of the compounds responsible for the allel- opathic e�ect detected in Synechocystis sp. in our studies will require further research. �ese results showed the allelopathic activity of Baltic Synechocystis, which either causes the inhibition or stimulation of the growth of selected picoplanktonic cy- anobacteria. Many studies indicated that cyanobacteria produced a wide spectrum of secondary metabolites (e.g., Berry et al., 2008). It is believed that allelopathy may be one of the important factors a�ecting the formation of massive cyanobacterial blooms in aquatic environments (Gross, 2003; Legrand et al., 2003). Despite the seriousness of the problem, relatively little is known about the allelopathic e�ect between picocy- anobacteria in the Baltic Sea. 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International Review of Hydrobiology, 101, 1–9. DOI: 10.1002/iroh.201501819 Żak, A., Kosakowska, A. (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 Allelopathic compounds produced by picocyanobacteria could a�ect the growth and development of bi- ological systems. �e main aim of this study was to investigate the in�uence of unknown allelochemicals obtained from picocyanobacterium Synechocystis sp. BA-153 in monocultures and in mixed cultures. In this study, we demonstrated that Synechocystis sp. BA-153 caused allelopathic e�ects against other strains of picocyanobacteria. It was found that Synechocystis sp. BA-121 was strongly inhibited by Synechocystis sp. BA-153 in both the mixed culture and cell-free �ltrates. On the other hand, the addition of live picocy- anobacterial culture of Synechocystis sp. BA-153 stimulated the growth of Synechocystis sp. BA-122. �ese results showed the allelopathic activity of Synechocystis sp. BA-153, which can cause either the inhibition or stimulation of growth of selected picoplanktonic cyanobacteria. Key words: allelopathy, picocyanobacteria, Synechocystis sp., growth, mixed culture, monoculture Received: [2017.05.27] Accepted: [2017.10.19] Zjawisko oddziaływania allelopatycznego bałtyckiej pikoplanktonowe j sinicy Synechocystis sp. Streszczenie Związki allelopatyczne produkowane przez pikoplanktonowe sinice mogą wpływać na wzrost i funkcjono- wanie gatunków �toplanktonu w ekosystemach wodnych. Głównym celem niniejszej pracy było wykazanie wpływu wciąż nierozpoznanych związków allelopatycznych produkowanych przez pikoplanktonową sinicę Synechocystis sp. BA-153 w monokulturach i hodowlach mieszanych. Na podstawie uzyskanych danych wykazano, że pikoplanktonowa sinica Synechocystis sp. BA-153 wykazywała oddziaływanie allelopatyczne na inne szczepy pikoplanktonowych sinic z tego samego rodzaju. Stwierdzono, że szczep Synechocystis sp. BA-153 silnie hamował wzrost Synechocystis sp. BA-121, zarówno w hodowlach mieszanych, jak i w eks- perymentach z dodaniem przesączu. Z drugiej strony, dodanie żywej kultury Synechocystis sp. BA-153 stymulowało wzrost Synechocystis sp. BA-122. Uzyskane wyniki potwierdzają aktywność allelopatyczną Synechocystis sp. BA-153 i wskazują, że może ona zarówno hamować, jak i stymulować wzrost wybranych szczepów pikoplanktonowych sinic. Słowa kluczowe: allelopatia, pikoplanktonowe sinice, Synechocystis sp., wzrost, hodowle mieszane, mo- nokultury A llelopathic activity of the B altic picocyanobacterium Synechocystis sp. S yl w ia Ś liw iń sk a- W ilc ze w sk a, A rk ad iu sz K ni tte r, D ar ia C is ło , A da m L at ał a 134 Information on the authors Sylwia Śliwińska-Wilczewska She is interested in the allelopathy of cyanobacteria and microalgae, in particular of picocyanobacteria Synechococcus sp. In her study, the in�uence of allelochemicals on the growth, chlorophyll �uorescence, and photosynthesis irradiance curves of di�erent phytoplankton species was investigated. She is also investigating what in�uences environmental factors have on produced allelopathic compounds on algae and cyanobacteria. Arkadiusz Knitter �e �eld of his interest is allelopathic interactions of picocyanobacterium Synechocystis sp. in mono- cultures and mixed cultures. He uses a �ow cytometer to determine allelopathic interactions between picocyanobacteria. Daria Cisło She is interested in allelopathy of picocyanobacteria, in particular of picocyanobacterium Synechocystis sp. She is investigating what in�uence allelopathic compounds have on those organisms in monocultures and mixed cultures. Adam Latała He has wide experience in ecophysiology and ecotoxicology of marine benthic and planktonic algae. His particular interest is on the in�uence of the main environmental factors, such as salinity, temperature, and light on the photosynthesis, photoacclimation, �uorescence, respiration, and the growth of algae from natural communities and cultured under laboratory conditions, including the use of �uorescence techniques to determine algal and cyanobacterial ecophysiology and ecotoxicology. He is the Curator of Culture Collection of Baltic Algae (CCBA) at the Institute of Oceanography, University of Gdańsk. Actually, CCBA maintains more than 100 Baltic strains from three taxonomic groups: blue-green algae, green algae, and diatoms.