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Article

Responses of Marine Diatom–Dinoflagellate Interspecific Competition to Different Phosphorus Sources

by
Anglu Shen
1,†,
Hongyue Liu
1,†,
Quandong Xin
2,
Qingjing Hu
2,
Xinliang Wang
2 and
Jufa Chen
2,*
1
College of Marine Ecology and Environment, Shanghai Ocean University, Shanghai 201306, China
2
Key Laboratory of Sustainable Development of Marine Fisheries, Ministry of Agriculture and Rural Affairs, Yellow Sea Fisheries Research Institute, Chinese Academy of Fishery Sciences, Qingdao 266071, China
*
Author to whom correspondence should be addressed.
†
These authors contributed equally to this work.
J. Mar. Sci. Eng. 2022, 10(12), 1972; https://doi.org/10.3390/jmse10121972
Submission received: 21 November 2022 / Revised: 5 December 2022 / Accepted: 8 December 2022 / Published: 11 December 2022
(This article belongs to the Special Issue New Insights in the Study of Harmful Algal Bloom)
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Abstract

:
Phosphorus (P) is an essential nutrient element of phytoplankton, as well as a limiting factor for phytoplankton growth. It controls the succession of blooms from diatoms to dinoflagellates, especially in the East China Sea (ECS), where the eutrophication is serious. Most studies have only considered a single aspect of dissolved inorganic phosphorus (DIP) or dissolved organic phosphorus (DOP). In contrast, we investigated the growth interactions among the major bloom-forming marine diatom Skeletonema costatum and dinoflagellates Prorocentrum donghaiense and Karenia mikimotoi by using bi-algal cultures combined with DIP and DOP. Our results revealed that (1) P. donghaiense and K. mikimotoi have survival strategies that are superior to those of S. costatum in a bi-algal culture, whether under P-sufficient or P-deficient conditions, and (2) P. donghaiense has a slight competitive advantage over K. mikimotoi when P is sufficient, but the reverse is true when P is deficient. The difference in interspecific competition results at different P concentrations with DIP and DOP mainly arises from the variation in the utilization abilities of different species as regards different P sources, a finding which can also provide strong evidence for revealing the succession of diatoms and dinoflagellates blooms in the ECS.

1. Introduction

Occurrences of harmful algal blooms (HABs) have become increasingly frequent and have become a major marine ecological disaster along the coasts of China in recent decades, mainly due to eutrophication [1,2]. Large-scale HABs in the Yangtze River estuary and the adjacent area of the East China Sea (ECS) in late spring and early summer have been recorded in the past few decades, with the main bloom-forming species consisting of Prorocentrum donghaiense, Skeletonema costatum, and Karenia mikimotoi [3]. Changes in nutrient concentration, composition, and structure can affect the utilization efficiency of phytoplankton; in turn, such influence might cause a change in the phytoplankton community structure in the marine environment [4,5,6]. For example, the “diatom–dinoflagellate–diatom” succession pattern has often been observed in spring and summer in the ECS since 2000 [7] and inevitably involves the interspecific competition between diatom and dinoflagellate species. However, the competing mechanisms of diatoms and dinoflagellates for nutrients are still limited at present [8].
Phosphorus (P), as one of the necessary nutrients for phytoplankton growth, is involved in the production of adenosine triphosphate (ATP), phospholipids, nucleic acids, and other cell components, and it plays an important role in photosynthesis, metabolism, and heredity [9]. Inorganic phosphorus (phosphate—Pi) is generally the preferred form of P for the growth of most phytoplankton because it can be used directly. However, most oceans exhibit a shortage of dissolved inorganic phosphorus (DIP, mainly orthophosphate HPO42− and PO43−). For example, the Yangtze River Estuary has a low DIP concentration of approximately 0.1–0.3 μM in spring and summer, a feature regarded as among the main limiting factors controlling phytoplankton growth in this area [10]. In contrast, dissolved organic phosphorus (DOP) concentration in the surface water of ECS is often close to or higher than that of DIP [11,12]. DOP can also be used as an alternative P source to maintain phytoplankton growth [13,14]. Some species can hydrolyze DOP as an alternative P source under the action of various enzymes, such as alkaline phosphatase (AP), particularly when DIP availability is limited [15,16]. Many studies confirmed that phytoplankton can utilize different forms of organic P sources, such as glucose-6-phosphate, ATP, ribonucleic acid, and lecithin [17,18,19,20]. Consequently, the abilities of different algal species to use DOP may affect the results of interspecific competition among them and might be involved in the succession of phytoplankton communities in natural conditions [21,22,23].
Reports on the effects of DIP on phytoplankton population competition, however, mostly focus on the conditions of DIP sufficiency/deficiency or different P sources. The conclusions from these studies are as follows. Firstly, diatoms have a stronger competitive advantage under DIP-rich conditions [24,25] but dinoflagellates exhibited a survival strategy superior to that of diatoms under DIP-deficient conditions [25,26]. Diatoms (e.g., S. costatum) can grow rapidly to maintain their competitive advantage over other species through efficient utilization of nutrients through low-affinity transporters used at high P conditions [9]. Additionally, the high-affinity transporter in dinoflagellates (e.g., P. donghaiense) upregulates at low external P and low cellular P conditions, thereby ensuring that algae can obtain P from the environment [9]. Secondly, relative to diatoms, dinoflagellates can use DOP more effectively under DIP-deficient conditions, and AP has been considered as an inducible ectoenzyme produced under P stress [27]. For example, more AP production sites were found in P. donghaiense and Alexandrium catenella than in S. costatum [28], indicating that the former had higher affinities to DOP and are more likely to maximize the metabolized DOP in the water [14]. Moreover, prior research highlighted interspecies competition with single DIP or DOP as phosphorus sources [18,24,26], an aspect which differs from the P structure in the ECS. Field investigation confirmed that the proportion of DIP and DOP in the surface water of the ECS often reaches approximately 1:1 in spring and summer [12], but research on algal interspecific competition combined with both DIP and DOP in the ECS has not yet been found. For the main bloom-forming species S. costatum, P. donghaiense, and K. mikimotoi, some researchers reported S. costatum has strong competitiveness against P. donghaiense under DIP-rich conditions, and others gained the opposite competition results that appeared under DIP-deficient conditions in the laboratory experiments [24,29,30] and mesocosm experiments [25,31]. S. costatum also has strong competitiveness against K. mikimotoi under DIP-rich conditions regardless of the N:P ratio [32]. Some studies also showed that the interspecific competition between P. donghaiense and K. mikimotoi had its own advantages at different initial concentrations under DIP-rich conditions [33,34]. In addition, Ou et al. [18] found that S. costatum outcompeted P. donghaiense irrespective of the DIP or DOP substrate.
In view of the fact that DIP and DOP coexist in the ocean [12], the results of interspecific competition experiment conducted with a single P source as a phytoplankton nutrient may be different from the real results. This is because different algae have different abilities and mechanisms to utilize DIP or DOP [27,28], which may lead to differences in the results of interspecific competition. However, so far, no further research has been conducted in this regard. We hypothesized that DIP and DOP, as coexisting P sources, play a key role in the interspecific competition of algae, and may have different results from single P sources. In this study, in order to clarify the mechanism between the succession of diatom–dinoflagellate blooms in the ECS in spring and summer, with the premise of being as close as possible to the marine environmental conditions (such as approximately 20 °C water temperature, coexistence of DIP and DOP, and low light-intensity when dinoflagellate blooms occurred in May and June, P. donghaiense and K. mikimotoi have the ability to maintain growth under these conditions [35]). Laboratory experiments were conducted to investigate the responses of the growth characteristics and interspecific competition among S. costatum, P. donghaiense, and K. mikimotoi in (1) both mono- and bi-algal cultures under different P concentrations and (2) under a (1:1) DIP and DOP structure ratio, and we use the classic interspecific competition model (the Lotka–Volterra model) to estimate interspecific competition parameters [36]. Furthermore, the growth of each species in the bi-algal culture was fitted with a mathematical model to specify and quantify the observed growth relationships. The changes in the DIP, DOP, and AP activities in the cultures were also determined. The resulting information will help explain the bloom succession of diatom–dinoflagellate species in the ECS.

2. Methods and Materials

2.1. Algae and Culture Conditions

Algal cultures of the diatom S. costatum (GY-H11) and the dinoflagellates P. donghaiense (GY-H40) and K. mikimotoi (GY-H36) were purchased from Shanghai Guang Yu Biological Science and Technology Co. Ltd., Shanghai, China. The algal cultures were placed in 1000 mL flasks supplied with 600 mL of sterile-filtered f/2 artificial seawater medium [37] at a salinity of 30. Artificial seawater made up of Redsea brand sea salt without nutrients was filtered by Millipore membranes (0.45 μm) and then autoclaved (121 °C, 20 min). S. costatum, P. donghaiense, and K. mikimotoi were maintained at 20 °C under 40 μmol m−2 s−1 of cool-white fluorescent illumination (400–700 nm) with a light:dark cycle of 12:12 h. The batch cultures were routinely shaken 2–3 times daily until the cells reached the exponential growth phase and were then harvested to be used in subsequent experiments. At the same time, we measured the effective quantum yield (Fq′/Fm′, representing the photosynthetic physiological state) of algae using a pulse amplitude modulated fluorometer (PHYTO-PAM-ED, Walz, Effeltrich, Germany) before each subsequent experiment. The Fq′/Fm′ values of S. costatum, P. donghaiense, and K. mikimotoi with a light intensity of 40 μmol m−2 s−1 were 0.60 ± 0.02, 0.54 ± 0.04, and 0.54 ± 0.03, respectively, and there was no significant difference from the data measured under high light with 125 μmol m−2 s−1 (p < 0.05). We ensured the Fq′/Fm′ values of algae were above 0.5 to ensure the vitality of algae was normal. The same conditions were used in all the experiments. The cell densities were ascertained by direct counting using a phytoplankton counter frame (CC-F, Beijing Purity Instrument, Co., Ltd., Beijing, China) under an optical inverted microscope (Nikon Ti-S; Nikon, Tokyo, Japan).

2.2. Experimental Design

Before treatment with different P sources, exponentially growing cells in f/2 medium were collected via centrifugation at 4000 rpm for 10 min, washed three times with a P-free medium, and then inoculated in a P-free medium for 3 days to remove the excess Pi of the cell.
After the Pi starvation, we selected two P sources (DIP: NaH2PO4·2H2O, DOP: ATP) and the P concentrations of (1) 10 μM DIP + 10 μM DOP (high) and 0.2 μM DIP + 0.2 μM DOP (low). Both mono- and bi-algal cultures were conducted in 1000 mL flasks with 600 mL of f/2 medium. The initial cell density of each species was 1.3 × 104 cells mL−1, and three replicates were used for each treatment. The mono-algal cultures were employed as the control. The mono- and bi-algal cultures of S. costatum, P. donghaiense, and K. mikimotoi were carried out for 8 days under the same culture conditions described above. The cell density was counted every 24 h, and total dissolved phosphorus (TP) and DIP concentrations were measured every 48 h. The DOP concentration was then calculated by subtracting DIP from TP. In addition, the AP activity was fluorometrically determined according to the release of 3-0-methylfluorescein from 3-0-methylfluorescein phosphate (Sigma, St. Louis, MO, USA) in accordance with the method described by Ou et al. [38] for the purpose of comparing the ATP utilization of different algae. To avoid precipitation or wall growth of algal cells, each culture flask was gently agitated and randomly repositioned every 8 h. The cells were fixed in 1.5% Lugol’s solution and counted under an inverted microscope (Nikon Ti-S) every 24 h. The molybdenum blue method, as developed by Murphy and Riley [39], was employed to determine the concentration of DIP. Finally, the TP content was ascertained using the potassium persulfate digestion technique from Jeffries et al. [40].

2.3. Data Analysis

2.3.1. Growth Simulation in Bi-Algal Cultures

The following logistic function models the environmental carrying capacity (K) and the inherent growth rate (r) of each alga in the mono-algal culture:
P(t) = K/[1 + exp(a − rt)],
where P(t) is the cell density at time t. The logistic function can be rewritten as Equations (2) and (3) for algae bi-algal culture, a feature which is included in the effect of interspecific and intraspecific competition [36]. Here, we illustrate the example of interspecific competition between diatom and dinoflagellate, or two dinoflagellates.
dx/dt = rxx[1 − (x + αy)/Kx−1];
dy/dt = ryy[1 − (βx + y)/Ky−1];
where x and y are the cell densities of two focal species from three options (S. costatum: Sc, P. donghaiense: Pd, and K. mikimotoi: Km) in a bi-algal culture. Kx and Ky are the environmental carrying capacities of species x and species y, and rx and ry denote the inherent growth rate of species x and y when each species is grown in a mono-culture. α and β are dimensionless parameters that indicate the degree of inhibition by the other species in a bi-algal culture compared with self-interference.
Equations (2) and (3) can be approximated with the following equations:
(lnxi+1 − lnxi−1)/(ti+1 − ti−1) = rx − rxxi/Kx − rxαyi/Kx;
(lnyi+1 − lnyi−1)/(ti+1 − ti−1) = ry − ryβxi/Ky − ryyi/Ky;
where xi and yi are the cell densities of two species at time ti in the bi-algal culture. If we set α = β = 0 when each species is grown in the mono-algal culture, then the logistic parameters (Kx, Ky, rx, and ry) can be estimated by Equations (4) and (5) using the mono-algal culture data. α and β can also be calculated by Equations (4) and (5) using the bi-algal culture data.

2.3.2. Statistical Analysis

Data were presented as mean ± standard deviation (SD). To ascertain if data were normally distributed (Shapiro–Wilk test) and exhibited homogeneous variance (Levene’s test), differences between groups were analyzed by t-test or one-way ANOVA followed by Tukey’s multiple comparison test. p < 0.05 was considered statistically significant. All statistical analyses were performed using the SPSS 26.0 Version (IBM SPSS Software, Armonk, NY, USA).

3. Results

3.1. Growth Competition of S. costatum and P. donghaiense

The relationship between the growth curves for S. costatum and P. donghaiense is shown in Figure 1. When P was sufficient, S. costatum revealed similar growth trends in mono- and bi-agal cultures, but its cell density in the bi-algal culture was significantly lower than that in the mono-algal counterpart from days 4–6 (p < 0.05). No significant differences were observed by the end of the experiment (Figure 1A). In contrast, P. donghaiense exhibited the same growth trends in mono- and bi-algal cultures on days 1–4 of the experiment, but its growth was dramatically suppressed in the bi-algal culture from days 5–8 (p < 0.05, Figure 1A). The competition parameters simulated from the Lotka–Volterra competition model are presented in Table 1, with the Kx for S. costatum (KSc) and Ky for P. donghaiense (KPd) calculated as 848,978 and 173,978 cells mL−1, respectively. The corresponding growth rates for S. costatum (rSc) and P. donghaiense (rPd) were estimated at approximately at 2.298 and 0.378 d−1. Using the equations, we also calculated the competitive inhibition parameter of S. costatum by P. donghaiense α as 6.740 and P. donghaiense by S. costatum β as 0.320. Then, we obtained the degree of inhibition of S. costatum by P. donghaiense A as 1.481 × 10−5 mL cell−1 s−1 and P. donghaiense by S. costatum B as 6.963 × 10−7 mL cell−1 s−1. Thus, the strength of the inhibitory effect that P. donghaiense exerts on S. costatum was approximately 21 times higher than the same effect S. costatum exerts on P. donghaiense. Furthermore, P. donghaiense has a survival strategy that is superior to that of S. costatum in the bi-algal culture under P-sufficient conditions, but no outcompeting was observed by the end of the experiment.
When P was deficient, S. costatum had almost the same growth trends in the mono and bi-algal cultures, but its cell density was lower in the bi-algal culture from days 2–4 and higher in the mono-algal culture on days 7–8 of the experiment (p < 0.05, Figure 1B). P. donghaiense had similar growth trends in mono- and bi-algal cultures, but its cell density was lower in the bi-algal culture on day 5 and 7 (p < 0.05, Figure 1B). In addition, the cell density of S. costatum was significantly higher than that of P. donghaiense in days 1–6 for both mono- and bi-algal cultures (p < 0.05), but by the end of the experiment, the cell density of P. donghaiense was prevalent over that of S. costatum in both mono- and bi-algal cultures (Figure 1B). Table 2 presents the competition parameters of two species, with KSc and KPd as 162,903 and 32,733 cells mL−1, respectively. The corresponding values of rSc and rPd were estimated to be approximately 1.818 and 0.677 d−1. We also calculated α for S. costatum as 2.729 and β for P. donghaiense as 0.059. Then, we obtained the values of A for S. costatum as 3.045 × 10−5 mL cell−1 s−1 and B for P. donghaiense as 1.217 × 10−6 mL cell−1 s−1. These outcomes indicated that the strength of the inhibitory effect that P. donghaiense exerts on S. costatum was approximately 25 times higher than that which S. costatum exerts on P. donghaiense. Thus, P. donghaiense has a survival strategy that is superior to that of S. costatum in a bi-algal culture under P-deficient conditions. Taken together with the changes in cell densities (Figure 1B), our results suggest that P. donghaiense will outcompete S. costatum in a longer culture time under P-deficient conditions.

3.2. Growth Competition of S. costatum and K. mikimotoi

When P was sufficient, S. costatum had a significantly lower cell density in the bi-algal culture relative to the mono-algal counterpart from days 4–8 (p < 0.05, Figure 2A). In contrast, K. mikimotoi had similar growth trends in mono- and bi-algal cultures during the first 4 days, but its cell density in the bi-algal culture was significantly lower from days 6–8 (p < 0.05, Figure 2A). In addition, KSc and rSc were greater than KKm and rKm, and the values of α for S. costatum and β for K. mikimotoi were 12.577 and 0.087, respectively (Table 1). The value of A for S. costatum was 2.762 × 10−5 mL cell−1 s−1 and of B for K. mikimotoi was 4.013 × 10−7 mL cell−1 s−1, and these outcomes indicate that the strength of the inhibitory effect that K. mikimotoi exerts on S. costatum was approximately 69 times higher than that which S. costatum exerts on K. mikimotoi. These results suggest that K. mikimotoi has an absolute advantage over S. costatum in the bi-algal culture under P-sufficient conditions, but no outcompeting was observed by the end of the experiment.
When P was deficient, S. costatum had similar growth trends in mono- and bi-algal cultures, but its cell density was lower in the bi-algal culture from days 3–6 (Figure 2B). K. mikimotoi also had similar growth trends in mono- and bi-algal cultures, but its cell density was significantly lower in the bi-algal culture from days 3–5 and on day 7 (p < 0.05, Figure 2B). Moreover, KSc and rSc were greater than KKm and rKm (Table 2), and the competition parameters of α for S. costatum and β for K. mikimotoi were 5.499 and 0.076, respectively. We then obtained the values of A for S. costatum as 6.136 × 10−5 mL cell−1 s−1 and B for K. mikimotoi as 3.547 × 10−7 mL cell−1 s−1, which indicated that the strength of the inhibitory effect that K. mikimotoi exerts on S. costatum was approximately 173 times higher than that which S. costatum exerts on K. mikimotoi. Thus, these results confirm that K. mikimotoi has an absolute advantage over S. costatum. Combined with the changes in cell densities (Figure 2B), our outcomes suggest that K. mikimotoi will outcompete S. costatum in a longer culture time under P-deficient conditions.

3.3. Growth Competition of P. donghaiense and K. mikimotoi

When P was sufficient, P. donghaiense had similar growth trends in mono- and bi-algal cultures, but its cell density was significantly lower in the bi-algal culture from days 1–8 (p < 0.05, Figure 3A). The cell density of K. mikimotoi in the bi-algal culture was markedly lower than that in the mono-algal counterpart from days 1–8 (p < 0.05, Figure 3A). Furthermore, the calculation of the Lotka–Volterra competition model (Table 1) reveals KPd (173,978 cells mL−1) and rPd (0.378 d−1) that were greater than KKm (77,077 cells mL−1) and rKm (0.355 d−1). The values of α for P. donghaiense and β for K. mikimotoi were also 2.735 and 1.306, respectively (Table 1). Then, we obtained the value of A for P. donghaiense as 5.950 × 10−6 mL cell−1 s−1 and B for K. mikimotoi as 6.010 × 10−6 mL cell−1 s−1, which indicated the inhibitory effect of one species by the other, but the strength of the inhibitory effect of two species was almost the same.
When P was deficient, P. donghaiense had a markedly lower cell density in the bi-algal culture than in the mono-algal counterpart from days 1–8 (p < 0.05, Figure 3B). In contrast, K. mikimotoi had similar growth trends in mono- and bi-algal cultures during the first 5 days, but its cell density was lower in the bi-algal culture in the last 3 days (p < 0.05, Figure 3B). In addition, KPd (32,733 cells mL−1) was lower than KKm (41,390 cells mL−1), while rPd (0.667 d−1) was higher than rKm (0.193 d−1). The values of α for P. donghaiense and β K. mikimotoi were 1.549 and 1.200, respectively. We then obtained the values of A for P. donghaiense as 3.205 × 10−5 mL cell−1 s−1 and B for K. mikimotoi as 5.609 × 10−6 mL cell−1 s−1, which indicated that the strength of the inhibitory effect that K. mikimotoi exerts on P. donghaiense was approximately six times higher than that which P. donghaiense exerts on K. mikimotoi. Thus, K. mikimotoi has a survival strategy that is superior to that of P. donghaiense in a bi-algal culture. Taken together with the changes in cell densities (Figure 3B), our findings indicate that K. mikimotoi will outcompete P. donghaiense in a longer culture time under P-deficient conditions.

3.4. Changes in DIP, DOP, and TP

The DIP, DOP, and TP concentration changes in S. costatum, P. donghaiense, and K. mikimotoi in mono-algal cultures are illustrated in Figure 4. When P was sufficient (Figure 4A–C), the initial DIP and DOP concentrations were approximately 10 μM with an initial proportion of 1:1, and the concentrations of different P sources (DIP, DOP, and TP) decreased gradually with time in each treatment. Furthermore, the DIP and TP concentrations in S. costatum culture decreased more sharply than those in the P. donghaiense and K. mikimotoi cultures during the first 4 days (p < 0.05), and then remained at low levels (Figure 4A,C). However, the DOP concentration in the K. mikimotoi culture was significantly higher than those in other cultures during the experiment (p < 0.05, Figure 4B). When P was deficient (Figure 4D–F), no significant differences occurred in the DIP and TP concentrations in all mono-algal cultures (Figure 4D,F, p > 0.05). The DOP concentrations in the S. costatum and P. donghaiense cultures decreased in the first two days and then remained at low levels, but the counterpart in the K. mikimotoi culture rapidly decreased to the lowest level on day 4 and then increased again (Figure 4E).
The DIP, DOP, and TP concentrations of S. costatum, P. donghaiense, and K. mikimotoi in bi-algal cultures are shown in Figure 5. When P was sufficient (Figure 5A–C), the DIP and TP concentrations in the S. costatum and P. donghaiense/K. mikimotoi cultures decreased more sharply than those in the P. donghaiense and K. mikimotoi culture (p < 0.05, Figure 5A,C). Moreover, the DOP concentration in the S. costatum and P. donghaiense culture was significantly lower than those in other cultures during the first four days and in the P. donghaiense and K. mikimotoi culture until the end of the experiment (p < 0.05, Figure 5B). Overall, when P was deficient (Figure 5D–F), the concentrations of different P sources (DIP, DOP, and TP) decreased in the first two or four days and then increased slightly until the end.

3.5. Changes in AP Activity

The AP activities in P-sufficient cultures were significantly lower than those in P-deficient cultures for both mono- and bi-algal cultures (p < 0.05, Figure 6). Furthermore, the AP activities in the S. costatum mono- and bi-algal cultures were also significantly lower than those in the P. donghaiense and K. mikimotoi mono-algal cultures whether under P-sufficient or P-deficient conditions, except on day 8 (p < 0.05, Figure 6A,B,D,E). On the contrary, the AP activities in the K. mikimotoi mono- and bi-algal cultures were significantly higher than those in the P. donghaiense counterparts under P-sufficient conditions (p < 0.05, Figure 6C). The AP activities in the K. mikimotoi mono-algal culture were also significantly higher than those in the P. donghaiense mono-algal culture and P. donghaiense and K. mikimotoi bi-algal cultures under P-deficient conditions (p < 0.05, Figure 6F).

4. Discussion

4.1. Interspecific Competition Mechanism under P-Sufficient Condition

Numerous studies have used the Lotka–Volterra model [36] to simulate the growth interaction between two species in bi-algal cultures [41,42,43,44,45]. In this study, the competition parameters simulated from the Lotka–Volterra competition model and under P-sufficient conditions showed that P. donghaiense and K. mikimotoi have survival strategies that are superior to those of S. costatum in the bi-algal culture, with the ratio of A and B at approximately 21 times for the S. costatum–P. donghaiense competition and 69 times for the S. costatum–K. mikimotoi competition (Table 1). These results are in accordance with the findings of Wang et al. [44], who confirmed a higher inhibition of P. donghaiense on S. costatum than that of S. costatum on P. donghaiense under different nutrient conditions. Similarly, Si et al. [32] established that K. mikimotoi has a survival strategy that is superior to that of S. costatum when N:P was 25 under P-sufficient conditions. Moreover, the inhibition effect of P. donghaiense or K. mikimotoi on S. costatum in this study was higher than those reported by Wang et al. [44] and Si et al. [32]. In contrast with our findings, other research documented that S. costatum has an absolute advantage over P. donghaiense under high-nutrient conditions in laboratory and mesocosm experiments [24,25,31,41]. For example, Wang et al. [24] verified that S. costatum exerts an inhibitory effect on P. donghaiense that was approximately three times higher than that exerted by P. donghaiense on S. costatum. Other researchers also proposed and analyzed a model of phytoplankton dynamics which includes Michaelis–Menten–Monod uptake of nutrients, Droop’s growth, and Liebig’s law of the minimum [46]. Considering the complex marine environmental conditions, we will try to apply this submodel to interspecific competition study in the future and compare it with the classical model.
However, prior works that conducted experiments with only DIP or DOP may have different interspecific competition results from those under sea environment conditions when blooms occurred. Therefore, to simulate the succession of bloom-forming species in the ECS in spring and summer, we set the different P concentrations with two P sources in this study. To our knowledge, this is the first report about marine diatom–dinoflagellate interspecific competition to different phosphorus sources with both DIP and DOP. The presence of DOP is likely to change the final results of interspecific competition because the DOP utilization ability of dinoflagellate is higher than that of the diatom. One possible reason for this discrepancy is that despite the higher DIP absorption rate by S. costatum relative to that of P. donghaiense and K. mikimotoi (0.55 × 10−3, 0.24 × 10−3, and 0.30 × 10−3 μM·cells−1·h−1, respectively, Figure 4), when DIP was low in the late stage of the experiment, S. costatum cell density decreased significantly and its competitive advantage was reversed by dinoflagellates. In comparison to diatoms, dinoflagellates have higher AP affinity (this feature can indicate the ability of algae to hydrolyze DOP) to the DOP substrate and can express more AP [14,28], thus improving the utilization rate of DOP [47]. In the present research, the AP activities in the P. donghaiense and K. mikimotoi mono-algal cultures were significantly higher than those in the S. costatum mono- and bi-algal cultures whether under P-sufficient or P-deficient conditions (p < 0.05, Figure 6). Therefore, P. donghaiense or K. mikimotoi has a stronger ability to hydrolyze DOP with AP relative to S. costatum.
In addition, the competition parameters simulated from the Lotka–Volterra competition model showed that P. donghaiense and K. mikimotoi have inhibitory effects on each other, and the strength of the inhibitory effect that P. donghaiense exerts on K. mikimotoi is slightly higher than that which K. mikimotoi exerts on P. donghaiense. This outcome could be explained by the fact that their competition mechanism mainly arises from the variation in the temperature adaptability of different algae. Temperature acts as an important driver of the results of interspecific competition of algae in laboratory experiments [48,49]. In this work, our primary aim is to examine the effects of different P sources on interspecific competition, so only one temperature gradient was set (20 °C). Previous experiments showed that the optimum temperature for the growth of P. donghaiense was approximately 20 °C [50], and for the growth of K. mikimotoi, it was approximately 24 °C [50,51]. The ecological dynamics model reported by Li [52] also revealed that temperature was the key factor in the seasonal succession of dinoflagellates during spring and summer in the Yangtze River Estuary and its adjacent water. Additionally, the higher growth rate of P. donghaiense may be affected by the surface/volume ratio of the cell. Many studies revealed that small algae cells usually have high material transport efficiency and fast absorption rate of nutrients due to their higher surface/volume and smaller diffusion boundary layer thickness; thus, it tended to achieve a higher specific growth rate and maximum cell density [53,54]. Huang et al. [33] found that the cell volume ratio of K. mikimotoi and P. donghaiense was approximately 2. The cell size of P. donghaiense was smaller and its specific surface area was higher, indicating P. donghaiense could propagate and absorb phosphorus nutrients more quickly. Therefore, future investigation of the effects of different phosphorus sources and temperatures on interspecific competition between P. donghaiense and K. mikimotoi is necessary. Furthermore, regarding the biodiversity loss of phytoplankton due to the outbreak of large-scale blooms, the interspecific competition between the bloom-forming species will lead to the simplification of species, affecting the stability of the marine ecosystem [55]. Hence, further investigations are needed to explore the underlying effects of the “diatom–dinoflagellate–diatom” bloom succession on marine biodiversity.

4.2. Interspecific Competition Mechanism under P Deficient Conditions

A succession from diatom blooms to dinoflagellate (e.g., P. donghaiense and K. mikimotoi) blooms occurs in the ECS in spring [14,56,57,58]. After the diatom blooms, the DIP concentration declines to approximately 0.10 µM, and this characteristic seems to play an important role in the diatom–dinoflagellate blooms succession [5,6]. When the P is deficient in the culture, P. donghaiense or K. mikimotoi exhibit a survival strategy that is superior to that of S. costatum in the bi-algal culture (Table 2). Our results are remarkably consistent with those of previous studies, such as those of Wang et al. [44] who reported that the inhibition ability of P. donghaiense to S. costatum was higher than that of S. costatum to P. donghaiense when the P concentration was 2 μM. Other works also confirmed that P. donghaiense exhibited a survival strategy superior to that of S. costatum in environments with low Pi [29,30]. Multiple reasons explained these observations. First, P plays a key role in interspecific competition. Some research suggested that the diatom P. tricornutum appeared to have high requirements for nutrients (r-strategy), and the dinoflagellate P. minimum outcompeted the diatoms in low-nutrient conditions (K-strategy) [4]. These differences in survival strategies can be further explained by the physiological characteristics of P absorption. That is, diatoms have low-affinity Pi transporters at high P conditions, and dinoflagellates have high-affinity Pi transporters at low external P and low cellular P conditions, which ensure that algae can obtain P from the environment [9]. Second, dinoflagellates generally exhibit higher AP activities on a per cell basis compared to diatoms [9,18] and account for the majority of the AP activity in the phytoplankton community [12,38,59]. Ou et al. [28] also found that AP covers most of the cell, including its production sites, which are mainly on the cell surface; some sites could be observed inside P. donghaiense cells, but only one or two AP sites on the cell surface could be detected in S. costatum. Our results also verified that the AP activity in mono-algal cultures of P. donghaiense or K. mikimotoi were significantly higher than those in both mono- and bi-algal cultures of S. costatum under P-deficient conditions except on day 8, a variation which may arise from the rapid decline of algal density, while the expression of AP did not decrease synchronously in the water (Figure 6D,E). Finally, in the face of the complex environment of the sea area during HAB, HAB community assembly and dynamics reflect two basic selection features—life-form and species-specific selection, in which commonly held life-form properties override phylogenetic properties in bloom-species selection [8]. Some studies reported that three primary adaptive strategies consistent with C-S-R strategies recognized among freshwater phytoplankton species characterize the component dinoflagellate species [60,61,62], and they have also been successfully applied in the succession of marine HAB species [8].
Moreover, the P pool in dinoflagellate cells is larger than that in the diatom cells [63], and the dissimilarity in P pool sizes may play an important role in their interspecific competition, especially under P-deficient conditions. The mechanism for storing P in phytoplankton involves the formation of polyphosphate [64], and our recent unpublished data also confirmed that the concentrations of polyphosphate in P. donghaiense and K. mikimotoi at 21.13 ± 3.12 and 18.81 ± 1.81 fmol cell−1, respectively, were significantly (p < 0.05) higher than that in S. costatum (1.96 ± 0.17 fmol cell−1). Finally, allelochemicals also have a significant impact on interspecific competition. The previous studies documented that the autoallelopathy of S. costatum plays an important role in the competition and succession between S. costatum and P. donghaiense, especially under P-deficient conditions [24,65]. However, as far as we know, the allelopathic effect of P. donghaiense or K. mikimotoi filtrate on the growth of S. costatum remains unclear. Given strong evidence of the autoinhibitory effect in S. costatum, the role of the allelopathic effect of P. donghaiense or K. mikimotoi in their competitions should be studied further.
For the competition of the two dinoflagellates, our results suggested that K. mikimotoi has a survival strategy that is superior to that of P. donghaiense in the bi-algal culture (Table 2). The presence of this competition outcome may be the main reason that the two kinds of algae have different abilities to use DOP. To further examine this possibility, we simultaneously analyzed the AP activities in the P. donghaiense and K. mikimotoi mono-algal cultures under P-deficient conditions. The average AP activities in the K. mikimotoi mono-algal cultures were significantly higher than those in the P. donghaiense counterparts during the experiment (p < 0.05, Figure 6F). These data indicate that K. mikimotoi has a higher AP hydrolysis capacity than P. donghaiense and can make more use of ATP, so as to gain advantages in competition. Xia [66] reported that the AP gene of P. donghaiense is located on the cell membrane and that of K. mikimotoi is in the extracellular matrix, a difference which may also affect the ability of algae to hydrolyze AP. In addition, K. mikimotoi cells exhibited the ability to utilize the Pi released from ATP and to take up its partial hydrolysis products (adenosine monophosphate or diphosphate) [22]. Another possible reason for this discrepancy is the allelopathy between the two algae under P-deficient conditions. The allelopathy of some algal species is also enhanced under low-nutrient conditions [67,68,69,70]. Li et al. [71] established that allelopathic compounds (or toxins) were the main antialgal mechanism of K. mikimotoi. Moreover, K. mikimotoi could produce lipophilic toxins, a characteristic volatile compound (cubenol), a reactive oxygen species with hemolytic and cytotoxic activity, and could cause cell burst in other plankton [71]. In contrast, P. donghaiense is a non-toxic dinoflagellate and does not release known phytotoxins [72]. In addition, this phenomenon also occurs in interspecific competition among other algae; for example, the results reported by Ji et al. [73] suggested that P. micans inhibited the growth of S. costatum and K. mikimotoi by the release of allelochemical(s). Wang et al. [74] found that A. minutum growth was inhibited when grown in S. costatum filtrate, but the filtrate of A. minutum exerted no allelopathic activity on S. costatum. Accordingly, further studies are required to clarify these aspects.

5. Conclusions

We investigated the interspecific competition of diatom S. costatum and dinoflagellates P. donghaiense and K. kimotoi by bi-algal culture under P-sufficient/deficient conditions with a (1:1) proportion of DIP and DOP. The Lotka–Volterra competition model indicated that the two dinoflagellates have a survival strategy that is superior to that of S. costatum whether under P-sufficient or P-deficient conditions because of the difference in the DOP utilization ability of diatoms and dinoflagellates. In addition, P. donghaiense and K. mikimotoi have different competitive advantages against each other, given their dissimilar optimum growth temperatures under P-sufficient conditions and their differing abilities to use DOP or achieve allelopathy under P-deficient conditions. These findings support universal recognition of diatom–dinoflagellate interspecific competition under P-deficient conditions, but they are different from the outcomes of the competition between diatoms and dinoflagellates of previous studies under P-sufficient conditions, especially when DIP and DOP coexist, suggesting that different P sources play a critical role in the interspecific competition between diatoms and dinoflagellates. These findings provide new insights to reveal the succession of diatom and dinoflagellate blooms in the ECS. Future work should focus on different temperature and allelopathic effects in bloom-forming species to refine our understanding of the ecological consequences of the diatom–dinoflagellate competition.

Author Contributions

Conceptualization, A.S. and J.C.; investigation, H.L.; writing—original draft preparation, A.S. and H.L.; writing—review and editing, Q.X., Q.H., X.W. and J.C. All authors have read and agreed to the published version of the manuscript.

Funding

The study was supported by grants from the National Key Research and Development Program of China (2019YFD0901401) the National Natural Science Foundation of China (41506194).

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

All the data involved in this study are reflected in the relevant figures and tables, and there is no additional data to be provided.

Acknowledgments

We thank Tao Jiang for his suggestion on this paper, and thank the three anonymous reviewers for their valuable comments.

Conflicts of Interest

The authors declare no conflict of interest.

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Jmse 10 01972 g001 550
Figure 1. Growth curves of S. costatum and P. donghaiense in mono- and bi-algal cultures under P-sufficient (A)/deficient (B) conditions. The values are the mean ± S.D. (n = 3), with * represent significant differences (p < 0.05) between mono-algal and bi-algal cultures.
Figure 1. Growth curves of S. costatum and P. donghaiense in mono- and bi-algal cultures under P-sufficient (A)/deficient (B) conditions. The values are the mean ± S.D. (n = 3), with * represent significant differences (p < 0.05) between mono-algal and bi-algal cultures.
Jmse 10 01972 g001
Jmse 10 01972 g002 550
Figure 2. Growth curves of S. costatum and K. mikimotoi in mono- and bi-algal cultures under P-sufficient (A)/deficient (B) conditions. The values are the mean ± S.D. (n = 3), with * represent significant differences (p < 0.05) between mono-algal and bi-algal cultures.
Figure 2. Growth curves of S. costatum and K. mikimotoi in mono- and bi-algal cultures under P-sufficient (A)/deficient (B) conditions. The values are the mean ± S.D. (n = 3), with * represent significant differences (p < 0.05) between mono-algal and bi-algal cultures.
Jmse 10 01972 g002
Jmse 10 01972 g003 550
Figure 3. Growth curves of P. donghaiense and K. mikimotoi in mono- and bi-algal cultures under P-sufficient (A)/deficient (B) conditions. The values are the mean ± S.D. (n = 3), with * represent significant differences (p < 0.05) between mono-algal and bi-algal cultures.
Figure 3. Growth curves of P. donghaiense and K. mikimotoi in mono- and bi-algal cultures under P-sufficient (A)/deficient (B) conditions. The values are the mean ± S.D. (n = 3), with * represent significant differences (p < 0.05) between mono-algal and bi-algal cultures.
Jmse 10 01972 g003
Jmse 10 01972 g004 550
Figure 4. Concentration changes of DIP, DOP, and TP of P. donghaiense, S. costatum and K. mikimotoi in mono-algal culture under P-sufficient (A–C)/deficient (D–F) conditions, respectively. The values are the mean ± S.D. (n = 3), with the different lower-case letters indicate significant (p < 0.05) differences among the different mono-algal cultures.
Figure 4. Concentration changes of DIP, DOP, and TP of P. donghaiense, S. costatum and K. mikimotoi in mono-algal culture under P-sufficient (A–C)/deficient (D–F) conditions, respectively. The values are the mean ± S.D. (n = 3), with the different lower-case letters indicate significant (p < 0.05) differences among the different mono-algal cultures.
Jmse 10 01972 g004
Jmse 10 01972 g005 550
Figure 5. Concentration changes of DIP, DOP, and TP of P. donghaiense, S. costatum, and K. mikimotoi in bi-algal culture under P-sufficient (A–C)/deficient (D–F) conditions, respectively. The values are the mean ± S.D. (n = 3), with the different lower-case letters indicating significant (p < 0.05) differences among the different bi-algal cultures.
Figure 5. Concentration changes of DIP, DOP, and TP of P. donghaiense, S. costatum, and K. mikimotoi in bi-algal culture under P-sufficient (A–C)/deficient (D–F) conditions, respectively. The values are the mean ± S.D. (n = 3), with the different lower-case letters indicating significant (p < 0.05) differences among the different bi-algal cultures.
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Jmse 10 01972 g006 550
Figure 6. The AP activity changes of P. donghaiense, S. costatum and K. mikimotoi in mono- and bi-algal cultures under P-sufficient (A–C)/deficient (D–F) conditions, respectively. The values are the mean ± S.D. (n = 3), with the different lower-case letters indicate significant (p < 0.05) differences among the two mono-algal cultures and bi-algal culture.
Figure 6. The AP activity changes of P. donghaiense, S. costatum and K. mikimotoi in mono- and bi-algal cultures under P-sufficient (A–C)/deficient (D–F) conditions, respectively. The values are the mean ± S.D. (n = 3), with the different lower-case letters indicate significant (p < 0.05) differences among the two mono-algal cultures and bi-algal culture.
Jmse 10 01972 g006
Table
Table 1. Estimates of model parameters for the mono- and bi-algal cultures of S. costatum, P. donghaiense, and K. mikimotoi under P-sufficient conditions.
Table 1. Estimates of model parameters for the mono- and bi-algal cultures of S. costatum, P. donghaiense, and K. mikimotoi under P-sufficient conditions.
SpeciesMaximum Biomass (K) (Cells mL−1)Growth Rate (r) (d−1)Interaction Rate
α or βA or B (mL Cell−1 s−1)
Sc848,9782.2986.7401.481 × 10−5
Pd173,9780.3780.3206.963 × 10−7
Sc848,9782.29812.5772.762 × 10−5
Km77,0770.3550.0874.013 × 10−7
Pd173,9780.3782.7355.950 × 10−6
Km77,0770.3551.3066.010 × 10−6
Table
Table 2. Estimates of model parameters for the mono- and bi-algal cultures of S. costatum, P. donghaiense, and K. mikimotoi under P-deficient conditions.
Table 2. Estimates of model parameters for the mono- and bi-algal cultures of S. costatum, P. donghaiense, and K. mikimotoi under P-deficient conditions.
SpeciesMaximum Biomass (K) (Cells mL−1)Growth Rate (r) (d−1)Interaction Rate
α or βA or B (mL Cell−1 s−1)
Sc162,9031.8182.7293.045 × 10−5
Pd32,7330.6770.0591.217 × 10−6
Sc162,9031.8185.4996.136 × 10−5
Km41,3900.1930.0763.547 × 10−7
Pd32,7330.6771.5493.205 × 10−5
Km41,3900.1931.2005.609 × 10−6
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Shen, A.; Liu, H.; Xin, Q.; Hu, Q.; Wang, X.; Chen, J. Responses of Marine Diatom–Dinoflagellate Interspecific Competition to Different Phosphorus Sources. J. Mar. Sci. Eng. 2022, 10, 1972. https://doi.org/10.3390/jmse10121972

AMA Style

Shen A, Liu H, Xin Q, Hu Q, Wang X, Chen J. Responses of Marine Diatom–Dinoflagellate Interspecific Competition to Different Phosphorus Sources. Journal of Marine Science and Engineering. 2022; 10(12):1972. https://doi.org/10.3390/jmse10121972

Chicago/Turabian Style

Shen, Anglu, Hongyue Liu, Quandong Xin, Qingjing Hu, Xinliang Wang, and Jufa Chen. 2022. "Responses of Marine Diatom–Dinoflagellate Interspecific Competition to Different Phosphorus Sources" Journal of Marine Science and Engineering 10, no. 12: 1972. https://doi.org/10.3390/jmse10121972

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