Почему доминируют кокколитофориды, или Физиологические механизмы доминирования Emiliania huxleyi
Vladimir A. Silkin
Южное отделение Института океанологии им. П.П. Ширшова РАН (г. Геленджик)
Цветения кокколитофорид, которые в основном представлены одним видом Emiliania huxleyi, занимают большие площади в океане и происходят длительное время. Какие механизмы обеспечивают выигрыш в конкуренции с другими доминатами – диатомеями? Существуют две гипотезы: первая объясняет переход от преобладания диатомей к доминированию кокколитофорид исчерпанием кремния, что часто наблюдается в океане. Вторая связывает исход конкуренции со способностью кокколитофорид успешно существовать при низких концентрациях азота, что происходит в Черном море, когда кокколитофориды доминируют на фоне высоких концентрациях кремния. В работе рассмотрены физиологические механизмы, обеспечивающие доминирование кокколитофорид при низких концентрациях азота.
Ключевые слова: кокколитофориды; Emiliania huxleyi; элементы питания; фитопланктон; физиологические механизмы; стехиометрия.
Diatoms and coccolithophores are the main elements of a primary production level of marine ecosystems and they perform different biogeochemical functions. Coccolithophorids are one of the most successful taxonomic groups, the distribution of which occupies a large space and is abundant (Iglesias-Rodriguez et al., 2002; Paasche, 2002). Interestingly, only the species Emiliania huxleyi is successful in terms of distribution. The number of cells during the bloom of this species are of the order of several million cells per liter, but there are examples of fantastic values, where the abundance can reach hundreds of millions of cells per liter (Turkoglu, 2008). During this period, the contribution of coccolithophorids to total phytoplankton biomass approaches 100%. What physiological mechanisms are used by this species to ensure their absolute dominance?
Emiliania huxleyi shows high temperature flexibility (Paasche, 2002) and this species exists practically in all biogeographic zones. Usually, in the northern hemisphere, E. huxleyi blooms begin in late spring and can be seen in the second half of the summer, as happens in the northern seas – the Barents and Bering (Sukhanova and Flint, 1998; Burenkov et al., 2011; Giraudeau et al., 2016). In the warm seas, this phenomenon usually occurs in late spring and early summer, but sometimes occurs in late autumn and winter (Sukhanova, 1997; Turkoglu, 2010; Silkin et al., 2013).
There are many hypotheses about the fundamental mechanisms that cause coccolithophorid dominance in blooms (Tyrrell, Merico, 2004). To form the coccolithophorid bloom, a seasonal thermocline is necessary (Iglesias-Rodriguez et al., 2002) and the greatest coccolithophorid abundance is usually on the layers closest to the surface of the water. Therefore, coccolithophorids have intensive growth in conditions of weak vertical exchange under low mixing. This indicates that the main regulators in the diatom-coccolithophorid system are the nutrients.
The most simple and attractive hypothesis was that diatom growth is limited by the silicon concentration (Egge, Aksnes, 1992). Namely, coccolithophorids gain an advantage after the spring bloom of diatoms, which dispose of the entire stock of silicon in the layer of water above the seasonal thermocline. Indeed, the silicon concentration in the coccolithophorid bloom in the northern seas is very low. For example, in early July, in the Barents Sea, it is about 0,53 μM (our data). But at the same time, coccolithophorids bloom in the north-eastern part of the Black Sea in late spring and early summer, when the silicon concentration is maximal (up to 8 μM) during the annual cycle (Yakushev et al., 2007; Pakhomova et al., 2014). This value significantly exceeds the level characteristic of the half-saturation constant for silicon uptake in many species of diatoms (Krause et al., 2012).
The second-most important question – what factor (concentration of nitrogen and phosphorus) limits coccolithophorid growth? Views on this matter are contradictory. There are indications that E. huxleyi is a poor competitor for nitrogen, and this factor limits the growth of the coccolithophorids; the opposite conclusion holds for phosphorus (Riegman et al., 2000). The study of the phytoplankton dynamics at various nitrogen and phosphorus additions in the mesocosms showed that coccolithophores dominate at high nitrogen-to-phosphorus (N:P) ratios (Egge, Heimdal, 1994); this indicates that this species takes advantage at low concentrations of phosphorus or has the lower half-saturation constant for this nutrient’s uptake, compared to the diatoms. However, field studies of E. huxleyi blooms in the North Atlantic and the Bering Sea have shown that this event occurs mainly in the N:P ratio, which is less than the Redfield value (Merico et al., 2004; Lessard et al., 2005). In the Black Sea, during the coccolithophorid dominance in late May and early June, the recorded value N:P ratio is always lower than the Redfield value (Silkin et al., 2014). The nitrogen concentration is relatively low in the Barents Sea and in the Black Sea and the phosphorus concentration is high, so when E. huxleyi bloomed in June 2006 in the north-eastern part of the Black Sea, the coccolithophorid contribution to the total phytoplankton biomass was more than 90%; it is obvious that only this species defined the residual concentration of nutrients in the sea. At this time, the average concentrations of nitrogen and phosphorus, respectively, were 0,8 and 0,27 μM, and their ratio was 2,96. The nitrogen addition does not lead to any increase in the biomass, but the phosphorus addition notably increased the number of cells (Silkin et al., 2014). In the Barents Sea, during the E. huxleyi bloom (over 90% of the total biomass and the cells number to 12x106 cells / l) the nitrogen concentration was even lower – 0,34 μM – and the N:P = 3,03. All this indicates that this species has the ability to function at low concentrations of nitrogen and therefore E. huxleyi has a low half-saturation constant for this element’s uptake, but this species demands high phosphorus concentrations for intensive growth. What mechanisms support this pattern? Indeed, in 1969 (Eppley et al., 1969) it was found that E. huxleyi has a low half-saturation constant for the nitrate uptake process, compared to diatoms. Study of the purified nitrate reductase of this species showed that this enzyme has a high molecular weight and operates very actively when NADH acts as an electron donor; its concentration in the cytosol should be high compared to that of the diatoms (Iwamoto, Shiraiwa, 2003). This requires additional energy consumption, which requires a high rate of photosynthesis and, consequently, high light intensity, which is only possible in the upper water layers.
It was found that when nitrogen is lacking in the environment, this species can regulate the kinetic parameters of nitrogen acquisition (Kaffes et al., 2010). The maximum activity of nitrate reductase and nitrite reductase are reduced significantly with the lack of nitrogen in the environment, but the half-saturation constant also decreases, which significantly increases the affinity of cells for the nitrogen. Interestingly, it also reduces the half-saturation constant for the acquisition of HCO3‾.
Limiting by nitrogen promotes the synthesis of new transporters for different forms of nitrogen (McKew et al., 2015). Likewise, phosphorus deficiency induces the synthesis of alkaline phosphatase (Riegman et al., 2000; Xu et al., 2006; McKew et al., 2015).
Coccolithophorids have a more economical adaptation strategy to deal with nitrogen deficiency (starvation) because their photosynthetic function lasts longer than the similar function of diatoms (Zhao et al., 2015a). Under conditions of periodic nitrogen supply, the diatoms rapidly restore photosynthetic function, the rate of cell division is rapidly increased, and diatoms gain competitive advantages over coccolithophorids (Zhao et al., 2015b). This regularity was also confirmed in computational experiments with models; the periodic nitrogen supply in the chemostat contributed to the dominance of diatoms (Cermeño et al., 2011). The high sensitivity of the photosynthetic apparatus of the diatoms to nitrogen limitation in comparison with E. huxleyi was observed in the stationary phase of batch culture (Franklin et al., 2012). The high stability of coccolithophorid photosystem II under nitrogen deficiency conditions is supported during 38 days, while for the diatoms it is supported for only 8–10 days (Loebl et al., 2010). At the same time, coccolithophorids are very sensitive to phosphorus deficiency: photosynthetic function is reduced by the 7th day of phosphorus starvation.
All the above data indicate that the coccolithophorids have physiological mechanisms for successful operation in conditions of nitrogen deficiency, and this gives them a major competitive advantage in comparison to their main competitors – diatoms.
Considering phosphorus as a regulator in the diatom-coccolithophorid system, it should be noted that some researchers point out that E. huxleyi is a good competitor for phosphorus, while others believe that low phosphorus concentrations limit coccolithophorid growth. What hypothesis does not contradict the data of field observations and experimental data? There are indications that at low phosphorus concentrations, the process of calcification is stimulated, and the cell division rate is decreased, which leads to an increase in cell volume (Shiraiwa, 2003). In phosphorus-replete cultures, the growth rate increases, the size of the cells decreases, and the cells contain little coccoliths. As a consequence, coccolithophorid bloom can be distinguished by at least two phases. In the first phase, nutrients and, especially, phosphorus are sufficient to achieve the maximum growth rate. In the second phase comes the decreasing of the coccolithophorid growth by phosphorus concentration; this stimulates the process of calcification, the cells increase in volume, and a large number of free coccoliths are observed in water. These patterns can be confirmed by field data. During the intensive growth of E. huxleyi (N:P = 3,06) in the beginning of July in the Barents sea, mainly the cells with diameters of 4–5 micrometers predominated. In the period of the bloom decline in late July, the cells with diameters of 6–7 microns and many coccoliths prevailed, indicating that the growth was limited by the phosphorus concentration. Intensive coccolithophorid growth was observed in the Black Sea in late May and early June, when the N:P ratio was below the Redfield, but in late June, the phosphorus concentration is significantly reduced and the N:P ratio is higher than the Redfield value. Coccolithophorids leave the photic zone and large diatoms are dominant. Low temperatures increase the calcification rate in situations of phosphorus deficiency (Satoh et al., 2009). In winter, low temperatures contribute to a significant increase in cell size in E. huxleyi blooms (Türkoğlu, 2010).
Obviously, not all of the mechanisms that allow coccolithophorids to dominate and conquer large areas are disclosed. It is possible that a significant contribution to the competitiveness of E. huxleyi is due to E. huxleyi’s adaptation mechanisms to high light intensity (Harris et al., 2005; McKew et al., 2013). This adaptation mechanism is the most often discussed but also may be other mechanisms that promote coccolithophorid dominance (Tyrrell, Merico, 2004). In our analysis, we identified only the cells' ability to demonstrate high production properties in the conditions of inorganic nitrogen deficiency. We believe that this mechanism plays a fundamental role in the formation of phytoplankton community structure and explains the patterns of succession in the sea.
Thus, the evolutionary adaptation of the coccolithophorids was to establish the physiological mechanisms to construct a perfect machine capable of successfully operating under a nitrogen deficiency. This species has the advantage when competing for inorganic nitrogen, not only with photoautotrophs, but also with heterotrophic bacteria (Løvdal et al., 2008). The cost for this are the high demands of the coccolithophores for phosphorus.
This work was supported by governmental project № 0149-2014-0056.
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Статья поступила в редакцию 11.11.2017
Why coccolithophorids dominate
Vladimir A. Silkin
Southern Branch of the P.P. Shirshov Institute of Oceanology of RAS (Gelendzhik, Russia)
Coccolithophorids blooms, which are mainly represented by one species of Emiliania huxleyi, occupy large areas in the ocean and occur for a long time. What mechanisms provide a benefites in competition with other dominates – diatoms? There are two hypotheses: the first explains the transition from the prevalence of diatoms to the dominance of coccolithophores by the exhaustion of silicon, which is often observed in the ocean. The second relates the outcome of competition to the ability of coccolithophoride to successfully exist at low nitrogen concentrations, which occurs in the Black Sea when coccolithophorides dominate the background of high concentrations of silicon. Physiological mechanisms ensuring the dominance of coccolithophoride at low nitrogen concentrations are considered.
Key words: coccolithophorids; Emiliania huxleyi; nutrients; phytoplankton; the physiological mechanisms; stoichiometry.
Силкин Владимир Арсентьевич - Silkin Vladimir A.
доктор биологических наук
Корреспондентский адрес: Россия, 353470, Краснодарский край, г. Геленджик, ул. Просторная 1-г. Телефон/факс 8-861-41-280-89.
ССЫЛКА НА СТАТЬЮ:
Силкин В.А. Почему доминируют кокколитофориды, или Физиологические механизмы доминирования Emiliania huxleyi // Вопросы современной альгологии. 2017. № 3 (15). URL: http://algology.ru/1185
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