59 Annales Universitatis Paedagogicae Cracoviensis Studia Naturae, 2: 59–68, 2017, ISSN 2543-8832 DOI: 10.24917/25438832.2.4 Sylwia Śliwińska-Wilczewska1*, Agata Cieszyńska2, Adam Latała1 1Institute of Oceanography, University of Gdańsk, Gdynia, Poland, *ocessl@edu.pl 2Institute of Oceanology of the Polish Academy of Science, Department of Marine Physics, Marine Biophysics Laboratory, Sopot, Poland The impact of temperature and photosynthetically active radiation on the growth and pigments concentration in Baltic picocyanobacterium Synechococcus sp. Introduction Chrococcoid cyanobacteria strain of the genus Synechococcus appears in marine, brackish, and freshwater ecosystems. Picoplanktonic organisms show a lot of adapta- tions, which enable them to spread in aquatic environments and to dominate and oc- cupy the niches inaccessible for other photoautotrophs. Owing to the fact that picocy- anobacteria exhibit the small size of cells and possess an advantageous surface area to volume ratio, they can assimilate trace amounts of nutrients. �erefore, in oligotroph- ic regions of seas and oceans, picoplankton can compete successfully with larger algae and determine the primary production of the whole water ecosystem (Six et al., 2007; Richardson, Jackson, 2007). Moreover, thanks to their small size and despite the ab- sence of the gas vesicles, picocyanobacteria can �oat e�ectively in the ocean water. �e distribution and growth intensity of picocyanobacteria are determined by their optimal ecological requirements, such as light and temperature. �ese factors in�uence metabolic processes, photosynthetic pigments, photosynthetic activity, and consequently, the rate of cell division and growth. Cyanobacterial strains show out- standing acclimation capability, which enable them to survive in environments with a great variability in conditions. Some cyanobacteria are tolerant to high temperatures up to 70°C and can survive at low intensities of about 5 μmol m-2 s-1 (Stal et al., 2003). Picocyanobacteria are a major component of oceanic ecosystems. Moreover, pico- cyanobacteria are important contributors to primary production in the ocean, particu- larly in warm nutrient-poor waters (Stockner, 1988). �is suggests that the contribu- tion of picocyanobacteria in temperate seas should be most important in the summer, when the water temperature is the highest and the seasonal thermocline limits the S yl w ia Ś liw iń sk a- W ilc ze w sk a, A ga ta C ie sz yń sk a, A da m L at ał a 60 supply of nutrients to the upper layer (Agawin et al., 1998). Unfortunately, coherent in- vestigations of physiological adaptations of picocyanobacterium Synechococcus sp. in aforementioned basins are scarce. �erefore, the objective of this work was to charac- terise the ecophysiological features of three di�erent Baltic picocyanobacterial strains of the genus Synechococcus. �e study was focused on estimating the e�ect of PAR and temperature on the wide range of changes in cell concentration and photosynthetic pigment content (Chl a and Car). �e autecological studies of the cyanobacterial spe- cies and the recognition of their reactions to the main environmental factor, such as light intensity and temperature, could be of great importance to recognise the phenom- enon of picocyanobacterial blooms in aquatic ecosystems and an important step in the way to improved understanding of bio-geo-physical couplings in the water mediums. Material and methods �e experiments were conducted on three di�erent picocyanobacterial strains from the genus Synechococcus: red BA-120, green BA-124 and brown BA-132. Depend- ing on pigment content, strains from the genus Synechococcus are classi�ed as red strains with phycoerythrin, green strains rich in phycocyanin, and brown strains with phycourobilin and phycoerythrin (Mazur-Marzec et al., 2013; Jodłowska, Śliwińska, 2014). �e strains were isolated from the coastal zone of the Gulf of Gdańsk (southern Baltic Sea) in late spring of 2002 and are maintained as unialgal cultures in the Cul- ture Collection of Baltic Algae at the Institute of Oceanography, University of Gdańsk, Poland (Latała et al., 2006). Tests on the ‘batch cultures’ were carried out in 25 ml glass Erlenmeyer �asks con- taining sterilised f2 medium (Guillard, 1975). �e media were prepared from arti- �cial sea water with a salinity of about 8. �e strains were incubated under a 16:8 h light : dark cycle at four PAR intensities (10, 100, 190, and 280 μmol m-2 s-1) and at four temperatures (10, 15, 20, and 25°C). As a lighting source �uorescent lamps, Sylvania cool-white 40 W and Sylvania 100 W halogen lamps for more intense light were used. �e intensity of PAR was measured by a LiCor LI-189 quantum-meter with a scalar collector. �e cultures were acclimated to every culture condition for 2 days, and then they served as inoculum for experimental cultures where the initial number was 106 cells per ml. �e test cultures were grown in three replicates and were incubated for one week. A�er that time in the exponential growth phase, the concentration of cells and contents of pigments were measured. �e number of Synechococcus sp. cells was determined using BD Accuri™ C6 �ow cytometer (Becton Dickinson, New Jersey, USA). �e amount of picocyanobacteria was counted at delivery rate of 14 µl min-1 and identi�ed using the Standard Optical Filter 670 nm (FL3) and 675/25 nm (FL4) (Marie et al., 2005). 61 Chlorophyll a and carotenoids were extracted with cold 90% acetone in the dark for 4 hours at -60°C. To remove cell debris and �lter particles, the pigment extract was centrifuged at 13000 rpm for 2 minutes (Sigma 2-16P, Osterode am Harz, Germany). �e extinction was determined at 750, 665, and 480 nm with a UV-VIS spectropho- tometer – DU 530 Beckman using 1 cm glass cuvette. �e concentration of carote- noids was calculated according to Strickland and Parsons (1972) with the formula: Car (µg ml-1) = 4(E480-E750)Va/Vb, while the concentration of chlorophyll a was estimat- ed with the formula: Chl a (µg ml-1) = 11.236(A665-A750)Va/Vb, derived from the factor by Strickland and Parsons (1972), where Va – extract volume (ml) and Vb – sample volume (ml). �e e�ects of PAR and temperature on the cell concentration and pigment content were examined by two-way analysis of variance method (ANOVA) at a signi�cance level of p < 0.05, and statistical calculations were performed using the STATISTICA® 13.1 program. Results �e concentration of cells of investigated Synechococcus strains were signi�cantly (p < 0.05) a�ected by intensity and temperature (Fig. 1). �e highest cell concentra- tions for strains BA-124 and BA-132 occurred in the highest light intensity (280 µmol m-2 s-1) and the highest temperature (25°C), and they were about 15.8-fold and 5.1- fold, respectively higher than the concentrations in the lowest light intensity of 10 µmol m-2 s-1 and 10°C. For BA-120, it was found that the highest cell concentrations occurred in the scenario of 190 µmol m-2 s-1 and the 25°C. Comparing the results de- rived within all experiments, the highest cell concentration (36·106 cell ml-1) was noted in for BA-124 in the scenario mentioned above (280 µmol m-2 s-1, 25°C), and the lowest cell concentration was observed for BA-120 (8·106 cell ml-1) in 280 µmol m-2 s-1, 10°C (Fig. 1). �e other striking observation is that the abundance of BA-120 in the highest PAR is lower than the abundance in 190 µmol m-2 s-1. �is tendency repeats for each temperature level (Fig. 1A). In general, for the three strains of Synechococcus, the cell-speci�c pigmentation was negatively a�ected by high PAR (Fig. 2). �e highest concentration of pigments were observed at the lowest light intensity (10 µmol m-2 s-1) and high temperature (25°C), except for Chl a and Car in BA-124 cells, where the highest pigments content was noted at 10 µmol m-2 s-1 and 10°C. �e cell-speci�c composition of pigments content was di�erent for di�erent strains. �e highest values of Chl a and Car were observed in the red strain BA-120 (0.23 pg cell-1 and 0.09 pg cell-1, respectively); whereas, in the green strain BA-124, the maximum value of this pigments was about 0.10 pg cell-1 and 0.07 pg cell-1, respectively. The im pact of tem perature and photosynthetically active radiation on the grow th and pigm ents concentration in B altic picocyanobacterium Synechococcus sp. S yl w ia Ś liw iń sk a- W ilc ze w sk a, A ga ta C ie sz yń sk a, A da m L at ał a 62 Discussion According to the present results, PAR and temperature are important factors con- trolling the growth of picocyanobacteria. �e signi�cance of light and temperature was also emphasised by Jasser and Arvola (2003), who pointed to the impact of these factors on the abundance and also the distribution of picocyanobacteria in the wa- ter medium. Moreover, following some already published research, it can be claimed that temperature and PAR may determine the abundance of the marine Synechococcus community (Jasser, Arvola, 2003; Jasser, 2006; Flombaum et al., 2013; Jodłowska, Śli- wińska, 2014). Fig. 1. Cell number of three strains of Synechococcus: BA-120 (A), BA-124 (B) and BA-132 (C) on day 7 of culturing at four PAR levels and at four temperatures. Values are means (± SD); n = 3 of independent replicates. �e scales in the sub-�gures were prepared di�erently for di�erent strains. �is was done in- tentionally in order to facilitate reading the values in sub-�gs A and C 63 In this study, it was found that elevated PAR and temperature have generally a positive e�ect on cell concentration for Synechococcus sp. However, the adaptation to very low-light and low-temperature conditions are also known for picoplanktonic or- ganisms. For instance, Ibelings (1996) noted that picocyanobacteria can bene�t from low light intensity reaching high growth rates. Moreover, this statement is consistent with the observations of picocyanobacterial high abundance at (or near) the end of the euphotic zone in coastal and o�shore marine waters (Callieri et al., 2005; Callieri, Fig. 2. �e photosynthetic pigment content (pg cell-1): a – chlorophyll a, b – carotenoids for three stains of Synechococcus: BA-120 (A), BA-124 (B) and BA-132 (C) on day 7 of culturing at four PAR levels and at four temperatures. Values are means (± SD); n = 3 of independent replicates The im pact of tem perature and photosynthetically active radiation on the grow th and pigm ents concentration in B altic picocyanobacterium Synechococcus sp. S yl w ia Ś liw iń sk a- W ilc ze w sk a, A ga ta C ie sz yń sk a, A da m L at ał a 64 2010). Additionally, under culture conditions, some major picoplanktons demon- strated the ability to survive and resume growth a�er periods of total darkness. Such a pronounced capacity for survival in the dark would enable these picoplanktonic organisms to survive the seasonal rhythm of winter darkness and sinking into the aphotic zone (Antia, 1976). On the other hand, Kana and Glibert (1987a,b) showed that Synechococcus WH7803 could also grow at an intensity as high as 2000 μmol m-2 s-1, but only if the cultivation of the strain was preceded by the acclimation in several intermediate intensities. Despite showing similar general growth responses to change- able environmental conditions, each strain also presents its speci�city. For instance, a kind of growth saturation was measured for BA-120 between 190 and 280 μmol m-2 s-1 at each temperature level, where the abundance decreased along with PAR increase (Fig. 1A). Moreover, the abundance functions dependent on PAR and temperature are di�erent for di�erent strains. For example, for both BA-124 and BA-132 PAR and temperature have a positive impact on the abundance in the whole domain but the plot lines di�er (Fig. 1B–C). Surface and near-surface populations experience extremely variable light and temperature conditions (Millie et al., 1990), and intensity is an important factor that a�ects the composition of photosynthetic pigments (Prézelin, 1981). �e results ob- tained for the two strains of Synechococcus BA-120 and BA-132 indicated that high intensity and low temperature had a generally negative e�ect on Chl a cell concentra- tion. For BA-124, the maximum value of Chl a content was noted at the lowest light and temperature. �e green strain BA-124 is rich in PC; whereas, the other two strains, red BA-120 and brown BA-132, have PE as the dominating photosynthetic pigment. Picocyanobacteria with a high concentration of PC are chromatically better adapted to harvest longer wavelengths of PAR than those with PE as a dominating pigment. �erefore, such picocyanobacteria (with PC) usually dominate in surface euphotic waters. On the other hand, the strains rich in PE usually occur deeper (Callieri, 2010). Moreover, picocyanobacteria, thanks to their high concentration of photosynthetic pigments, may occur in low light intensity waters (Stal et al., 2003). �e above is con- sistent with derived results, which showed that BA-120 and BA-132 are characterised by higher a pigment composition than BA-124. BA-120 and BA-132 are these strains that are more adapted to live in deeper parts of the water column than BA-124. Note that changes in the pigment content and in the ratio of di�erent pigments results in the optimisation of photosynthetic e�ciency (Defew et al., 2004). In the two strains of Synechococcus (BA-120 and BA-132), the highest Car content were observed at the lowest PAR and the highest temperature, whilst the highest Car content in BA-124 was measured at the lowest PAR and temperature. Carotenoids have a dual role in the cell, which is to maintain a high capacity for photosynthetic light absorption and to provide protection against photooxidation. �is feature ad- 65 ditionally explains why Synechococcus sp. is able to grow successfully both in the surface layer and in deeper waters (Stal, Walsby, 2000; Stal et al., 2003; Jodłowska, Śliwińska, 2014). �e experiments on Synechococcus strains demonstrated their tolerance to ele- vated light levels and temperatures. �ese strains were able to change the composi- tion of photosynthetic pigments to use light quanta better and to protect themselves from unfavourable environmental factors. �e ability of Synechococcus to sustain their growth in low light and temperature conditions and their lack (green and brown strain) or low photoinhibition (red strain) in exposure to high light intensi- ties and high temperatures could give picocyanobacteria an advantage in changeable aquatic ecosystems. �is study indicates the need to conduct further research on Synechococcus sp. as a whole and separately for each strain of this genus. 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Abstract �e experiments on three Baltic picocyanobacterial strains of Synechococcus (BA-120 – red strain, BA-124 – green strain and BA-132 – brown strain) were conducted at four scalar irradiances in Photosynthetically Active Radiation (PAR) and four temperature levels. �e main aim of this work was to estimate the e�ect of environmental conditions (temperature and PAR) on cell concentration and photosynthetic pigments (Chlorophyll a – Chl a and Carotenoids – Car) contents. �e ranges 67 of PAR and temperatures were 10, 100, 190, 280 μmol m-2 s-1 and 10, 15, 20, 25°C, respectively. �e experiment was carried in a medium of salinity of 8. �e number of Synechococcus sp. cells was determined using a BD Accuri™ C6 �ow cytometer. �e pigments contents were determined by a spectrophotometric method. In this work, it was found that elevated intensity and temperature have, on average, a positive e�ect on cell concentration for Synechococcus sp. �e highest cells concentrations were noted at the highest PAR (280 µmol m-2 s-1) and the highest T (25°C) for green and brown strains (BA-124 and BA-132, respectively) and at 190 µmol m-2 s-1 and 25°C for red strain (BA-120). Comparing the strains at each PAR level and temperature, the highest cell concentration was noted in green strain (36·106 cell ml-1), while the lowest was observed in red strain (8·106 cell ml-1). In general, in the two strains of Synechococcus (BA-120 and BA-132), the highest Car and Chl a contents were observed at the lowest light intensity and the highest temperature. On the other hand, Car and Chl a maximum content in BA-124 were noted at the lowest light and temperature. �e experiments on Synechococcus strains demonstrated their high capacity to acclimate to a wide range of PAR and temperature levels. �e three strains of Synechococcus showed adaptation capabilities, since they were able to change the composition of their photosynthetic pigments to use light quantity better and to protect the cells from the unfavourable e�ect of elevated light and temperature. Key words: picocyanobacteria, growth, PAR, photosynthetic pigments, temperature Received: [2017.07.14] Accepted: [2017.09.22] Wpływ temperatury i natężenia światła na wzrost i zawartość barwników fotosyntetycznych u bałtyckiej pikoplanktonowej sinicy Synechococcus sp. Streszczenie Badania przeprowadzono na trzech szczepach bałtyckiej pikoplanktonowej sinicy z rodzaju Synecho- coccus (BA-120 – szczep czerwony, BA-124 – szczep zielony oraz BA-132 – szczep brązowy), które hodowano w czterech różnych warunkach oświetlenia fotosyntetycznie aktywnego (PAR): 10, 100, 190, 280 μmol m-2 s-1 oraz w czterech temperaturach: 10, 15, 20 i 25°C. Głównym celem pracy było określenie wpływu wybranych zakresów PAR i temperatury na wzrost komórek oraz zawartość barw- ników fotosyntetycznych u analizowanych szczepów sinicy. Eksperyment przeprowadzono w medium o stałym zasoleniu równym 8. Liczebność komórek określana była za pomocą cytometru przepły- wowego BD Accuri™ C6. Pomiar oraz estymację zawartości barwników fotosyntetycznych określono metodą spektrofotometryczną. Na podstawie uzyskanych danych wykazano, że wysoka intensywność światła oraz wysoka temperatura mają na ogół pozytywny wpływ na liczebność komórek Synechococ- cus sp. Stwierdzono, że szczep zielony (BA-124) oraz szczep brązowy (BA-132) osiągnęły największą liczebność komórek w najwyższym oświetleniu (280 µmol m-2 s-1) i najwyższej temperaturze (25°C). Szczep czerwony BA-120 wykazał najwyższy wzrost w 190 µmol m-2 s-1 i 25°C. Ponadto zaobserwowa- no, że szczep zielony posiadał najwyższą liczebność komórek, która po tygodniu eksperymentu wyniosła 36·106 kom. ml-1, natomiast szczep czerwony był najmniej liczny (8·106 kom. ml-1). Ogólnie, szczepy BA-120 oraz BA-132 najwyższą zawartość chloro�lu a oraz barwników karotenoidowych wykazały w najniższym oświetleniu i najwyższej temperaturze. Maksymalną zawartość tych barwników szczep BA-124 osiągnął w najniższej temperaturze oraz natężeniu światła. Na podstawie przeprowadzonych doświadczeń wykazano wysoką aklimatyzację szczepów Synechococcus sp. do szerokiego zakresu natężenia PAR oraz temperatury. Wszystkie badane szczepy pikoplanktonowej sinicy były zdolne do zmiany proporcji swoich barwników fotosyntetycznych. Tego rodzaju umiejętność pozwala im lepiej wykorzystywać dostępne promieniowanie w procesie fotosyntezy oraz daje ochronę w przypadku ekspozycji na niekorzystne warunki środowiskowe. Słowa kluczowe: pikoplanktonowe sinice, wzrost, PAR, barwniki fotosyntetyczne, temperatura The im pact of tem perature and photosynthetically active radiation on the grow th and pigm ents concentration in B altic picocyanobacterium Synechococcus sp. S yl w ia Ś liw iń sk a- W ilc ze w sk a, A ga ta C ie sz yń sk a, A da m L at ał a 68 Information on the authors Sylwia Śliwińska-Wilczewska She is interested in allelopathy of cyanobacteria and microalgae, in particular, of picocyanobacteria Sy- nechococcus sp. Her study includes the in�uence of allelochemicals on the growth, chlorophyll �uores- cence, and photosynthesis irradiance curves of di�erent phytoplankton species. She is investigating what in�uences environmental factors have on produced allelopathic compounds on algae and cyanobacteria. Agata Cieszyńska She is focusing on improving the understanding of the in�uence of di�erent environmental conditions on phytoplankton blooms in the Baltic Sea. She is working on available data-bases and numerical models. Presently, she is working on the determination of the impact of ambient environment on picocyanobac- teria growth on the basis of previously arranged laboratory experiments. Additionally, she is using the laboratory results to develop a numerical algorithm for the Baltic picocyanobacteria life cycle. Adam Latała Wide experience in ecophysiology and ecotoxicology of marine benthic and planktonic algae. In�uence of the main environmental factors such as salinity, temperature and light on the photosynthesis, photo- acclimation, �uorescence, respiration and growth of algae from natural communities and cultured under laboratory conditions. Use of �uorescence techniques to determine algal and cyanobacterial ecophysio- logy and ecotoxicology.