Fish Sci (2013) 79:285–291 DOI 10.1007/s12562-013-0597-6
ORIGINAL ARTICLE
Environment
Effects of temperature, salinity and their interaction on growth of toxic Ostreopsis sp. 1 and Ostreopsis sp. 6 (Dinophyceae) isolated from Japanese coastal waters Yuko Tanimoto • Haruo Yamaguchi • Takamichi Yoshimatsu • Shinya Sato • Masao Adachi
Received: 5 November 2012 / Accepted: 15 January 2013 / Published online: 7 February 2013 Ó The Japanese Society of Fisheries Science 2013
Abstract Some species belonging to Ostreopsis, a benthic dinoflagellate genus, are known to produce palytoxin analogues. Around the coastal regions of Japan, the toxic Ostreopsis sp. 1 and Ostreopsis sp. 6 which are genetically divergent from other species of Ostreopsis are present from the southern to northern regions and in the southern region, respectively. The present study examined the growth responses of these strains to seven temperatures (15–35 °C) in combination with five salinities (20–40) and discusses the effects of temperature and salinity on their distribution and bloom dynamics in Japan. Tolerable temperatures and salinities ranged 15–30 °C and 25–40 for Ostreopsis sp. 1, and 17.5–30 °C and 20–40 for Ostreopsis sp. 6. The optimal temperature ranges which gave growth rates of [90 % of maximal growth rate of each strain were 22–25 °C for Ostreopsis sp. 1 and 24–30 °C for Ostreopsis sp. 6. Therefore, Ostreopsis sp. 1 is putatively tolerant to lower
Y. Tanimoto The United Graduate School of Agricultural Sciences, Ehime University, 3-5-7 Tarumi, Matsuyama, Ehime 790-8566, Japan e-mail:
[email protected] H. Yamaguchi T. Yoshimatsu M. Adachi (&) Faculty of Agriculture, Kochi University, 200-Otsu, Monobe, Nankoku, Kochi 783-8502, Japan e-mail:
[email protected] H. Yamaguchi e-mail:
[email protected] T. Yoshimatsu e-mail:
[email protected] S. Sato Royal Botanic Garden Edinburgh, 20 Inverleith Row, Edinburgh EH3 5LR, UK e-mail:
[email protected]
temperatures and thus possesses adaptability to colder waters of relatively higher latitude regions of Japan, whereas Ostreopsis sp. 6 presumably possesses adaptability to warmer waters of the southern region. We conclude that growth responses of Japanese toxic Ostreopsis sp. 1 and Ostreopsis sp. 6 to temperature-salinity affect their distribution and bloom dynamics in Japan. Keywords Ostreopsis sp. 1 Ostreopsis sp. 6 Palytoxin Temperature Salinity Growth
Introduction Marine benthic dinoflagellates of the genus Ostreopsis producing palytoxin (PTX) and PTX analogues such as ovatoxin and ostreocin are causative agents potentially for toxification of marine organisms, such as shellfish [1, 2], sea urchins [3] and finfish [4]. PTX analogues originating from Ostreopsis spp. can be also spread as poisonous aerosols, exposing humans to the risk of respiratory illness through inhalation [5–8]. PTX-like toxification of marine organisms and outbreaks of PTX-like poisonous aerosols have been recognized to be associated potentially with blooms of toxic Ostreopsis spp. [1–8]. Thus, it is important to clarify the bloom dynamics of toxic Ostreopsis for assessing the risk of toxification of marine organisms and on public health. The genus Ostreopsis in Japanese coastal waters consists of various clades as well as morpho-species: Ostreopsis ovata [9–12], Ostreopsis cf. ovata (=clade A), Ostreopsis sp. 1 (=clade B), Ostreopsis sp. 2, Ostreopsis sp. 5 (=clade C), Ostreopsis sp. 6 (=clade D) [13], Ostreopsis siamensis [9–12] and Ostreopsis sp. [4, 12]. Ostreopsis sp. 1 is clearly divergent from O. cf. ovata though it has similar
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morphological features to that of the latter clade [13]. Therefore, Ostreopsis sp. 1 has been considered to be a ‘cryptic’ species/clade of O. cf. ovata [13]. Ostreopsis sp. 6 is also clearly divergent from other Ostreopsis species [13]. Recently, Suzuki et al. [14] conducted chemical analytical experiments on toxin profiles of Japanese Ostreopsis and detected PTX and ovatoxins in strains of O. cf. ovata and Ostreopsis sp. 1, and also found ostreocin-D in a strain of Ostreopsis sp. 6. Sato et al. [13] also detected PTX-like toxicities in cultures of O. cf. ovata, Ostreopsis sp. 1 and Ostreopsis sp. 6 by mouse bioassays. Considering these issues, the causative agents for potential PTX-like toxification of marine organisms in coastal areas of Japan may be O. cf. ovata, Ostreopsis sp. 1 and Ostreopsis sp. 6. Among the toxic Ostreopsis species/clades, Ostreopsis sp. 1 is thought to be the dominant clade in Japan, being distributed widely in the southern to northern regions (27–44°N, 128–142°E) that are composed of the areas of Honsyu (A shown in Fig. 1), Shikoku (B), Kyusyu (C), Hachijojima (D), Okinawa (E) and Hokkaido [13]. In contrast, Ostreopsis sp. 6 is distributed in the southern region (24–27°N, 123–128°E), Okinawa (E) and Ishigaki, Kohama and Iriomote areas (shown as F in Fig. 1) [13].
A
Hokkaido
B C
40°
Otsuki: Isolation locale of Ostreopsis sp. 1 (strain s0716)
Materials and methods
A C
B
D
Cultures 30°
Haemida: Isolation locale of Ostreopsis sp. 6 (strain s0587)
E
E
F F 20° 0
120°
130°
140°
500 km
150°
Fig. 1 Isolation locales of Ostreopsis sp. 1 (s0716 strain), Ostreopsis sp. 6 (s0587 strain) used in this study and isolation regions of other strains of the Ostreopsis spp. reported by Sato et al. [13] around the coast of Japan. The letters and symbols on the map show the regions and locales for sampling around the Japanese coasts, respectively: Hokkaido (Hokkaido, closed triangle), Honsyu (A, closed circles), Shikoku (B, open circles), Kyusyu (C, open squares), Hachijojima (D, closed square), Okinawa (E, open triangles), and Ishigaki, Kohama and Iriomote areas (F, open rhombuses)
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Meanwhile, O. cf. ovata is distributed in the southern‘central’ regions (24–34°N, 123–134°E) that are composed of areas of B, C, E, and F shown in Fig. 1 [13]. The distribution areas of the Japanese toxic species/clades of genus Ostreopsis are clearly diverse among the species/ clades [13]. Therefore, it is important to elucidate the environmental conditions affecting growth of each toxic species/clade of Ostreopsis for understanding their distribution and bloom dynamics around Japanese coastal areas. Benthic epiphytic algae such as Ostreopsis species/ clades appear to be exposed to the drastic changes in temperature and salinity of coastal waters due to solar radiation, rainfall and riverine inputs in Japan. Hence, it is important to clarify the tolerable and optimal ranges of temperaturesalinity for growth of Ostreopsis species/clades. Our recent study has demonstrated that Japanese O. cf. ovata strain s0662 tolerated a wide range of temperature (17.5–30 °C) and salinity (25–40) [15]. Further, we showed that the strain grew rapidly at high water temperatures of 25–30 °C and salinities 30–35, enabling blooms to form [15]. However, there are no comparative data on the temperature and salinity conditions for growth of Ostreopsis sp. 1 and Ostreopsis sp. 6 for discussing their distribution and bloom dynamics around Japanese coastal areas. The purpose of the present study is to clarify the effects of temperature and salinity on growth of the toxic Ostreopsis sp. 1 and Ostreopsis sp. 6. We estimated growth rates of their strains at seven temperatures in combination with five salinities and discuss the distribution and bloom dynamics of Ostreopsis sp. 1 and Ostreopsis sp. 6 in the coastal environments of Japan.
Unialgal cultures of Ostreopsis sp. 1 (strain s0716) and Ostreopsis sp. 6 (strain s0587) used in this study were isolated from macroalgae collected from a depth of 0.5–1.0 m off Otsuki (32°470 53N, 133°420 30E, Fig. 1), Kochi Prefecture, when the water temperature was 27 °C on 1st August, 2009 and Haemida (24°150 11N, 123°510 E, Fig. 1), Iriomote Island, Okinawa Prefecture, Japan, when the water temperature was 27 °C on 24th June, 2009, respectively [13]. Strain s0716, which has a sequence of the 28S rDNA D8-D10 region (Accession no. AB674818), belongs to a clade of Ostreopsis sp. 1 and the s0587 strain, which has sequences of the 28S rDNA D8-D10 (Accession no. AB674897) and the ITS regions (Accession no. AB674922), belongs to a clade of Ostreopsis sp. 6 [13]. The unialgal cultures of the strains were maintained as the stock culture in 100-ml polypropylene
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(PP)-capped flasks containing 60 ml of autoclaved f/2 medium [16] at 25 °C under 90–100 lmol photons/m2/s of cool-white fluorescent illumination on a 12:12 h L:D cycle (light period 0600–1800 h). Effects of temperature and salinity on growth of the tested strains Following the culture experiment in Yamaguchi et al. [15], the culture experiments were conducted at seven temperatures (15.0, 17.5, 20.0, 25.0, 30.0, 32.5 and 35.0 °C) in combination with five salinities (20, 25, 30, 35 and 40) using growth cabinets (MLR-351H, Sanyo Co. Ltd., Japan) and temperature gradient growth chambers (TG-100-AD, Nippon Medical & Chemical Instrument Co. Ltd., Japan) under the light conditions as stated above. The salinity of seawater was adjusted to 20–40 by dilution with distilled water and by addition of artificial salts [17] according to the method reported by Yamaguchi et al. [15]. Cultures of strains s0716 (=Ostreopsis sp. 1) and s0587 (=Ostreopsis sp. 6) grown in PP-capped test tubes (25 9 150 mm) with flat bottoms and containing 25 ml of the f/2 medium, were pre-adapted to the experimental temperature and salinity conditions through stepwise transfer of stock cultures to each temperature and salinity regime in triplicate [15]. Growth rates in triplicate cultures in each experimental regime were determined by measuring the in vivo chlorophyll (chl.) a fluorescence, since it was reported that significant correlations (r [ 0.97, p \ 0.001) were observed between the cell density and the chl. a fluorescence in the cultures of Ostreopsis sp. 1 and Ostreopsis sp. 6 [18]. The in vivo fluorescence was measured at intervals of 2 or 3 days using a Turner Designs Model 10-100R fluorometer [19] after stirring the culture tube according to the method described by Yamaguchi et al. [18]. Growth rates (divisions/day) were calculated in triplicate [20]. By averaging the growth rates obtained in each regime, we calculated the average growth rate (l: divisions/day) [15]. Optimal temperatures were defined as temperatures that gave each strain growth rates of [90 % of maximal growth rate. Effects of temperature and salinity on the growth rates were statistically analyzed by multiple comparisons of a Tukey test and a two-way ANOVA. On the basis of the results, cubic equations of the form [21]: l ¼ b00 þ b10 T þ b20 T 2 þ b30 T 3 þ b01 S þ b02 S2 þ b03 S3 þ b11 TS þ b12 TS2 þ b21 T 2 S; where l is the growth rate, T is temperature (°C), S is salinity and bnm are regression coefficients in which the superscripts represent the multipliers of the variable TnSm, were fitted by the multiple regression analysis.
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Results The strain of Ostreopsis sp. 1 grew in a wide range of temperatures (15–30 °C) (Figs. 2, 3), showing tolerance to a low temperature of 15 °C. In contrast to Ostreopsis sp. 1, Ostreopsis sp. 6 strain did not show tolerance to 15 °C though it grew in a wide range of temperatures (17.5–30 °C) (Figs. 2, 3). Ostreopsis sp. 1 strain and Ostreopsis sp. 6 strain grew in the salinity ranges of 25–40 and 20–40, respectively (Figs. 2, 3). Results of multiple comparisons by a Tukey test (data not shown) found a significantly (p \ 0.05) high growth rate (0.549 divisions/ day) of Ostreopsis sp. 1 strain at 25 °C and salinity 35 among the experimental regimes (Figs. 3, 4). The surface response contours of Fig. 3 show that 22–25 °C gave Ostreopsis sp. 1 strain high growth rates of [90 % of maximal growth rate, thereby showing that the optimal temperature range of this organism was 22–25 °C. In the case of Ostreopsis sp. 6, significantly high growth rates (p \ 0.05, Tukey test) were observed at 25 °C and salinity 35, 30 °C and salinity 30, and 30 °C and salinity 35. The surface response contours of Fig. 3 show that the optimal temperature range of Ostreopsis sp. 6 was 24–30 °C. The maximal growth rate (1.32 divisions/day) of Ostreopsis sp. 6 strain was significantly (p \ 0.05) higher than that (0.549 divisions/day) of Ostreopsis sp. 1 obtained under optimal conditions (Figs. 3, 4). Results of a multiple comparison test (data not shown) and a two-way ANOVA test showed that temperature, salinity, and temperature-salinity interaction significantly influence the growth rate (p \ 0.001) of Ostreopsis sp. 1 and Ostreopsis sp. 6 (Table 1). In the ANOVA results, the sums of squares (SS) of temperature for growth rates of Ostreopsis sp. 1 and Ostreopsis sp. 6 were larger than those of salinity and temperature-salinity interaction, respectively (Table 1), indicating that the effect of temperature on growth of Ostreopsis sp. 1 and Ostreopsis sp. 6 was stronger than those of salinity or temperature-salinity interaction. On the basis of the ANOVA results, the obtained multiple regression equation of the growth rate of each strain on temperature and salinity was as follows: Ostreopsis sp. 1; l ¼ 4:97266 þ 0:51795T 0:01885T 2 þ 0:00026T 3 þ 0:00223S2 0:00006S3 þ 0:00007TS2 0:0001T 2 S; Ostreopsis sp. 6; l ¼ 2:617419 þ 0:001796T 2 0:0000683S3 þ 0:0115115TS þ 0:0001061TS2 0:000358T 2 S: The regression models fit the data with R values of 0.88
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Fig. 2 Growth curves of Ostreopsis sp. 1 and Ostreopsis sp. 6 strains under various temperatures in combination with salinities. Asterisk denotes no experimental data because the organism did not show any growth under the experimental 15 °C condition of the pre-cultures Fig. 3 Response surface contours of the growth rates (divisions/day) of Ostreopsis sp. 1 and Ostreopsis sp. 6 cultures as functions of temperature and salinity. ND not determined
Fig. 4 The maximal growth rates of Ostreopsis sp. 1 and Ostreopsis sp. 6 and those of other Ostreopsis spp. strains reported previously. Error bars show the standard deviation (SD, n = 3). Significance of differences among the maximal growth rate means of Ostreopsis sp. 1, Ostreopsis sp. 6 and O. cf. ovata [15] were tested using a multiple
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comparison of a Tukey–Kramer test. Means that showed significant differences are labeled with different letters (p \ 0.05). *1 Yamaguchi et al. [15], *2 Morton et al. [22], *3 Tosteson et al. [23], *4 Grane´li et al. [24], *5 Pearce et al. [25]
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Table 1 Results of a two-way ANOVA test for significant effects of temperature, salinity and their interaction on growth rates (divisions/ day) of Ostreopsis sp. 1 and Ostreopsis sp. 6 Clades
Source of variation
Ostreopsis sp. 1
Temperature
Ostreopsis sp. 6
Salinity
Degrees of freedom
Sum of squares
Mean square
F
6
1.71
0.2850
984.2*
4
0.72
0.1806
623.6*
Interaction
24
0.93
0.0389
134.4*
Error
70
0.02
0.0003
Total
104
Temperature Salinity
6
3.39 13.2
2.1996
693.7*
4
3.28
0.8205
258.8*
Interaction
24
3.74
0.1558
49.1*
Error
70
0.222
0.0032
Total
104
20.4
* p \ 0.001
(p \ 0.001) and 0.86 (p \ 0.001) for the growth rates of the Ostreopsis sp. 1 and Ostreopsis sp. 6 strains, respectively.
Discussion This paper provides the first evidence for significant effects of temperature, salinity and their interactions on the growth of toxic Ostreopsis sp. 1 and Ostreopsis sp. 6 strains isolated from Japanese coastal waters. The optimal and tolerable temperatures and salinities are different between Ostreopsis sp. 1 and Ostreopsis sp. 6 strains, which can explain their respective distributional areas, from the southern to northern regions (27–44°N, 128–142°E; A, B, C, D, E and Hokkaido as shown in Fig. 1) for the former, and southern region (24–27°N, 123–128°E; E and F as shown in Fig. 1) for the latter around the Japanese coastal areas reported by Sato et al. [13]. This study shows that Ostreopsis sp. 1 is capable of growing at a temperature of 15 °C. Among toxic benthic dinoflagellates [22–29] associated with harmful algal blooms, Coolia monotis [26] in New Zealand and Gambierdiscus carolinianus [27] in the US at \0.1 divisions/day at a temperature 15 °C, and Tasmanian O. siamensis [25] also grew at 15 °C. In contrast, it was reported that many benthic dinoflagellates [22, 24, 28] including Japanese O. ovata [29]/O. cf. ovata [15] did not grow at 15 °C. The present study also found no growth of Ostreopsis sp. 6 at 15 °C. Considering these issues, the unique physiological feature ‘low temperature tolerance’ of Ostreopsis sp. 1 makes it possible for the organism to distribute widely and predominate in Japanese coastal waters. The optimal temperature range for growth of Ostreopsis sp. 1 is 22–25 °C, whereas those of Ostreopsis sp. 6 and
Japanese O. cf. ovata [15] are 24–30 °C and 25–30 °C, respectively. As reported by Sato et al. [13], Ostreopsis sp. 1 in Japanese coastal waters formed blooms at 22–27 °C, whereas Ostreopsis sp. 6 and O. cf. ovata formed blooms at 27–28 and 24–31 °C, respectively. The temperatures seem to correspond to the optimal temperatures of the organisms as described above. Furthermore, the growth rate of Ostreopsis sp. 1 at 30 °C in the present experiments was \60 % of the maximal growth rate, whereas those of Ostreopsis sp. 6 and Japanese O. cf. ovata [15] at 30 °C were over 90 % of maximal growth rate. Considering the optimal temperatures of these strains and their growth responses to 30 °C, we suggest that Ostreopsis sp. 1 appears to prefer waters of 22–25 °C to that of [25 °C whereas Ostreopsis sp. 6 as well as O. cf. ovata appears to prefer waters of 24–30 °C. Therefore, Ostreopsis sp. 1 may not be well adapted to the southern region (24–27°N, 123–128°E; E and F as shown in Fig. 1) where the water temperature increases to 30 °C [30, 31] at which Ostreopsis sp. 6 and O. cf. ovata grow well. We suggest that temperature probably plays a crucial role in the divergent distribution of Ostreopsis sp. 1, Ostreopsis sp. 6 and O. cf. ovata in the coastal environments of Japan. This study revealed the fast growth of Ostreopsis sp. 6 strain s0587 whose maximal growth rate of [1.3 divisions/ day is the highest among those of the previously reported Ostreopsis spp. from Japan as well as various regions in the world (Fig. 4). Sato et al. [13] reported that O. cf. ovata also occurred in the southern region (24–27°N, 123–128°E; E and F as shown in Fig. 1) of Japan where Ostreopsis sp. 6 occurs. Considering previous and present results, we infer that Ostreopsis sp. 6, which is capable of growing rapidly ([1.3 divisions/day), appears to predominate over O. cf. ovata with a growth potential of 1.0 divisions/day [15] (Fig. 4). However, the field populations of Ostreopsis sp. 6 were not always dominant in the region [13]. The cellwidth (55 lm), -length (69 lm) and -thickness (34 lm) of Ostreopsis sp. 6 (Sato S, unpublished data) are different from those of Ostreopsis sp. 1 and O. cf. ovata (width 19–21 lm; length 27–28 lm; thickness 16–18 lm), but have similar cell morphology characteristics [13]. Following an equation described in Sun and Liu [32], we calculated the cell volumes of Ostreopsis sp. 6 and Ostreopsis sp. 1/O. cf. ovata, and clearly demonstrated that the cell volume of the former (6.8 9 104 lm3) is more than ten times larger than those of the latter species (4.3–5.5 9 103 lm3). Generally, large algal cells are considered to be inferior in nutrient uptake rate, relative to small cells [33–35]. Considering these issues, we suggest that Ostreopsis sp. 6 putatively requires more nutrients than those required by small Ostreopsis spp. such as Ostreopsis sp. 1 and O. cf. ovata for maintaining rapid growth and the large-sized cell, which may be one of the reasons why
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Ostreopsis sp. 6 was not always dominant over O. cf. ovata in the region. The relatively large cells of Ostreopsis sp. 6 would grow rapidly and predominate over the other Ostreopsis species/clades in the southern coastal areas when nutrients are not limiting factors to growth of the organism. The present study demonstrates that Ostreopsis sp. 6 strain has a great growth potential that enables the organism not only to proliferate rapidly at over 1.3 divisions/day but also to grow at C0.3 divisions/day even under the low salinity of 20 at which Ostreopsis sp. 1 (present study) and O. cf. ovata [15] do not grow. Ostreopsis sp. 6 might predominate over them and form blooms in the Shikoku area of Japan (B as shown in Fig. 1), such as Tosa Bay (33°310 10N, 133°450 20E), during rainy summer seasons, when the water temperature often increases to 25 °C [36–38] and the salinity sometimes decreases to B20 due to freshwater input [37]. The optimal salinity ranges for growth of Ostreopsis sp. 1 and Ostreopsis sp. 6 are 35 and 30–35, respectively, which are the average values of oceanic waters. Therefore, we suggest that Ostreopsis sp. 1 and Ostreopsis sp. 6 prefer coastal environments, especially non-enclosed areas affected directly by oceanic waters and thereby showing high salinity of [30. Ostreopsis sp. 1 and Ostreopsis sp. 6 strains produce palytoxin-like compounds, such as palytoxin and ovatoxins or ostreocin-D [14], which putatively affect marine organisms and human health. Thus, forecasting bloom developments of these organisms in the coastal waters of Japan on the basis of in situ growth is important for assessing the risk of toxification of marine organisms by their blooms. Our results suggest that it may be possible to estimate the in situ growth potential of Ostreopsis sp. 1 and Ostreopsis sp. 6 within their tolerable temperatures and salinities using our regression models and field data sets of temperature and salinity when other factors such as nutrients, light and grazing-pressure do not limit their growth. We hope that the regression models will help in forecasting the bloom development and decline of Ostreopsis sp. 1 and Ostreopsis sp. 6 in field environments. In the near future, we aim to clarify the effects of temperature, salinity and nutrient interaction on the growth of Japanese toxic species/clades of the genus Ostreopsis by using these axenic cultures. Acknowledgments This study was supported by Grant-in-Aid from the Food Safety Commission, Japan (no. 0904).
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29.
30.
31.
32.
33.
34. 35. 36.
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