Снижение pH океана, стехиометрия и динофлагелляты:
больше вопросов, чем ответов
Acidification, stoichiometry, and dinoflagellates: more questions than answers
Силкин В.А.
Vladimir A. Silkin
Южное отделение Института океанологии им. П.П. Ширшова РАН (г. Геленджик)
The Southern Branch of the P.P. Shirshov Institute of Oceanology RAS (Gelendzhik, Russia)
УДК 581.1:574.522
Чтобы предсказать структурные перестройки экосистем при изменении климата и снижении рН воды, необходимы фундаментальные знания влияния повышенных температур и повышения концентрации углекислоты на доминанты первично-продукционного звена. Накопленные экспериментальные данные касаются, прежде всего, изучения диатомового комплекса. Динофлагелляты – вторая по значимости группа фитопланктона, однако ей уделено значительно меньше внимания, что связано, прежде всего, с трудностями культивирования. В статье анализируются редкие работы по влиянию на физиолого-биохимические показатели динофлагеллят повышенных концентраций углекислоты и лимитирования элементами питания. Накопленный материал показывает, что реакция динофлагеллят на изменение указанных факторов не отличается существенно от реакции представителей других систематических групп.
Ключевые слова: снижение рН; элементы питания; фитопланктон; динофлагелляты; диатомовые; стехиометрия, изменение климата.
Climate change may significantly alter the structure and functioning of marine ecosystems, and species with new eco-physiological traits could outcompete and oust the former dominant species. These changes can result from decreasing pH of seawater (ocean acidification – OA) due to the increase in atmospheric CO2 (Kroecker et al., 2013). However, there is a lack of fundamental knowledge about the mechanisms of the effect of OA on the physiological and biochemical parameters of species, which makes it impossible to predict the phytoplankton responses in future OA scenarios. Despite the large number of publications devoted to the problem of OA (Riebesell, Gattuso, 2015), there are some problems in obtaining objective information about the impact of OA on the structure of phytoplankton species. The use of different methodological approaches and a large number of species makes it impossible to analyze the material, and the findings are often conflicting. In addition, studies have been conducted on various functional types of phytoplankton, and dinoflagellates have been given little attention. However, without the inclusion of this group of phytoplankton in the predictive models, the future structure of the community cannot be predicted (Dutkiewicz et al., 2015).
The atmospheric CO2 concentration is increasing, and as a consequence, temperature will inevitably lead to a higher heating of the surface of water, which will contribute to the formation of sharp gradients of seasonal thermoclines and reduce the thickness of the upper mixed layer. This will decrease the rates of the vertical transfer and consequently limit photosynthesis due to a lack of nutrients. In other words, with increasing concentration of dissolved CO2 and HCO3–, nitrogen and phosphorus concentrations will decrease and the average irradiance of phytoplankton will increase (Raven et al., 2011). These predictable processes raise questions regarding the adaptation potential of today's dominant phytoplankton species to these ecological shifts. Given that processes of carbon and nitrogen assimilation are interrelated, there is an obvious necessity for simultaneous studies of the effect of carbon concentration and nitrogen.
The effect of decreased pH was studied in single-species cultures. Easily cultivated species of diatoms and coccolithophorids were mainly used. The cultivation of dinoflagellates has its difficulties, which naturally affects the number of publications on representatives of this functional group. Interest in dinoflagellates is associated with two major problems.
First, the dinoflagellates are components of the phytoplankton succession, and their contribution to the production of biomass can be significant for the formation of the food chain (Margalef, 1978; Smayda, Reynolds, 2001). Second, the dinoflagellates form blooms with a strong toxic effect, and the causes are associated with changes in concentration of the nutrients (Anderson, 2002; Heisler et al., 2008). Cells stoichiometry is a powerful driver of toxin production (Van de Waal et al., 2014). This applies to dinoflagellates because OA can affect the toxins production (Hattenrath-Lehmann et al., 2015).
Dinoflagellates can use mixotrophic and heterotrophic strategies for carbon acquisition (Flynn et al., 2013). The large range of dinoflagellates and their variety of nutrients strategies allow them to have a wide variety of ecological niches (Smayda and Reynolds 2001). It is possible that these features of dinoflagellates have an effect on the response of these algae to OA.
When reducing the content of nitrogen in the cells (thus changing the C:N ratio), the preferred synthesis of carbon storage shifts to compounds that do not contain nitrogen or contain very little, which are usually polysaccharides (Raven 2014) or lipids (Hu et al. 2008). Lipid synthesis is more costly in terms of energy (Raven 2014), and therefore, it should be observed in conditions where there is a higher rate of photosynthesis; i.e., in the layers of water that are not limited by incident energy close to the surface. In other words, one species may have a vertical differentiation where lipids accumulate in the upper layers and carbohydrates accumulate in the lower layers. This may correspond to different species that are specialized in accumulating different compounds. In conditions of high nitrogen concentration, amino acids are synthesized in the cells. The conditions that limit the growth of diatoms by nitrogen lead to a reduction in cell size, pigment content, specific growth rate, and effective quantum yield (Li et al., 2012). Dinoflagellates have been shown to have inorganic carbon concentrating mechanisms (CCM) (Rost et al., 2006; Ratti et al., 2007), but the response of species to OA differs significantly (Eberlein et al., 2016). The variation of the nitrogen concentration changes the functioning of CCM (Raven et al., 2011). The data about the impact of the acidification process on the maximum specific growth rate of dinoflagellates are contradictory. Some experiments show that the specific growth rate increases with decreasing pH, but in another experiment, the reaction was absent (Fu et al. 2008; Fu et al. 2010; Pierangelini et al., 2014, Trimborn et al., 2014).
It has been noted that an increase in the carbon dioxide concentration in nitrogen- and phosphorus-rich media does not change the biochemical composition of cells, and the C:N ratio in particular remains relatively constant (Montechiaro and Giordano 2010). This suggests homeostasis. Pierangelini et al. (2016) examined to what extent this is true in circumstances where there is a concurrent increase in carbon dioxide concentration and the nitrogen concentration is changed. They studied the mutual influence of elevated CO2 concentrations (400, 1000, and 5000 ppmv, pH = 8,1) and of a variable or constant molar ratio of carbon to nitrogen (Ci :NO3–) on the biochemical and physiological parameters of the marine dinoflagellate Protoceratium reticulatum (specific growth rate, cell volume and dry weight, elemental and biochemical composition, enzyme activities, proteins parameters). This species is always present in the phytoplankton community in the seas of the Mediterranean basin, and it is potentially toxic.
The authors have shown that an increase in carbon dioxide concentration increases the maximum specific growth rate, regardless of the availability of nitrogen. Obviously, the specific growth rate increases due to decreasing costs of the synthesis and functioning of CCM at elevated carbon dioxide concentrations. Since the specific growth rate was estimated in the exponential growth phase, the growth by nutrients should not be limited. The dry cell weight was more than 40% higher at a constant Ci :NO3– ratio and pCO2 concentration of 400 ppmv compared with higher concentrations of carbon dioxide. The reduction of the dry weight of the cells results from an increase in the maximum specific growth rate. The carbon content in the cell was higher at 400 ppmv of pCO2, independent of the nitrogen and carbon supply mode (constant or variable).
The protein content was increased at a constant Ci:NO3– ratio and an elevated level of carbon dioxide. The lipid pool was higher at 400 ppmv of pCO2 and a constant Ci :NO3– ratio, and the carbohydrate content is not dependent on the level of carbon dioxide. Normally, lipid synthesis increases when there is nitrogen deficiency (increased cell C:N ratio) or excess energy, and this phenomenon is used in algal biotechnology (Hu et al., 2008). At low pCO2, a nitrogen deficit should not occur because the C:N ratio in the cell is constant. This fact of the variable lipid pool requires further investigation to explain the behavior.
Increasing the activity of nitrate reductase was observed with increasing pCO2 at only a constant Ci :NO3– ratio. Dinoflagellates have a higher half-saturation constant for the nitrogen uptake than coccolithophores and diatoms (Eppley et al., 1969; Clark, Flynn, 2000). We cannot answer the question of whether the dinoflagellates benefit from increasing OA, or in other words, whether the half-saturation constant for nitrogen uptake decreases. It was found that when nitrogen is lacking in the environment, the species could regulate the kinetic parameters of nitrogen acquisition (Kaffes et al., 2010). The maximum activity of nitrate reductase is reduced significantly with a 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 HCO3– acquisition.
Rubisco II content did not depend on the level of carbon dioxide at a variable Ci:NO3– ratio. This was surprising since other reactions are expected: a reduction of Rubisco, reduced energy consumption and nitrogen in the synthesis (Raven 2013), and changing cell stoichiometry. The cells showed a high production rate C at all concentrations of carbon dioxide and only when Ci :NO3– was constant.
In general, Protoceratium reticulatum shows a similar reaction to other species of other taxonomic groups upon photolithotroph growth when increasing the carbon dioxide concentration and changing the stoichiometry. It is possible that there will be a new response to changes in carbon dioxide concentration and stoichiometry during the transition to mixotrophic or heterotrophic nutrition. This work is important because it takes into account the important trend of transition from studying one factor to multiple drivers, and it makes a significant contribution to the understanding of the reaction of dinoflagellates to OA.
This work was supported by governmental project № 0149-2014-0056.
Работа выполнена в рамках темы Госзадания № 0149-2014-0056.
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Статья поступила в редакцию 11.09.2017
Acidification, stoichiometry, and dinoflagellates more questions than answers
Vladimir A. Silkin
Southern Branch of the P.P. Shirshov Institute of Oceanology of RAS (Gelendzhik, Russia)
To predict the structural rearrangements of ecosystems under climate change and a ocean acidification, fundamental knowledges of the effect of elevated temperatures and CO2 concentration on the dominants of the phytoplankton are needed. The accumulated experimental data concern, first of all, the study of the diatom complex. Dinoflagellates - the second most important group of phytoplankton, however, it is given much less attention, which is due, first of all, to the difficulties of cultivation. In this work, we analyze those rare works on the effect of elevated carbon dioxide concentrations, the limitation of food elements on the physiological and biochemical indices of dinoflagellates. The accumulated material shows that the reaction of dinoflagellate to a change in these factors does not differ significantly from the reaction of representatives of other systematic groups.
Key words: ocean acidification; nutrients; phytoplankton; dinoflagellates; diatoms; stoichiometry; climate change.
Об авторе
Силкин Владимир Арсентьевич - Silkin Vladimir Arsentyevitch
доктор биологических наук
заведующий лабораторией Экологии Южного отделения ФГБУН «Институт океанологии им.П.П.Ширшова РАН», Геленджик, Россия (Southern branch of the P.P. Shirshov Institute of Oceanology RAS, Gelendzhik, Russia)
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. Acidification, stoichiometry, and dinoflagellates more questions than answers // Вопросы современной альгологии. 2017. № 2 (14). URL: http://algology.ru/1169
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