Elsevier

Estuarine, Coastal and Shelf Science

Volume 135, 20 December 2013, Pages 128-136
Estuarine, Coastal and Shelf Science

Effect of temperature on changes in size and morphology of the marine diatom, Ditylum brightwellii (West) Grunow (Bacillariophyceae)

https://doi.org/10.1016/j.ecss.2013.05.007Get rights and content

Highlights

  • Different morphological types of Ditylum brightwellii (Prism and Cylinder types).

  • Temperature-induced size and morphological changes in D. brightwellii.

  • The change might provide a competitive advantage by bypassing sexual reproduction.

Abstract

The objective of the present study was to assess size and morphological changes in response to temperature in the marine diatom, Ditylum brightwellii (West) Grunow, using ecological, morphological and physiological approaches. D. brightwellii has two distinct cell morphologies: prism (large-sized cell) and cylinder types (small-sized cell). In the coastal waters of South Korea, the prism type was found to be present at high frequency at low temperatures, whereas the cylinder type was predominant at high temperatures. Other environmental factors did not affect the presence of either cell type significantly. In growth experiments to determine the effect of temperature on the size of D. brightwellii, the abundance of the prism type increased at low temperature, but the abundance of the cylinder type increased at high temperature. These results are important for understanding temperature-induced size and morphological changes in D. brightwellii, and their potential role as an adaptive strategy.

Introduction

Diatom species exhibit morphological variability, with cell shapes that range between spherical and cylindrical or centric and pennate (Round et al., 1990); in addition, the cells can either remain solitary or cluster into colonies. The most characteristic feature of a diatom is the ornamentation of the silica cell wall, which follows a species-specific pattern that is preserved and reproduced faithfully between generations. However, upon exposure to different kinds of environmental stress, the morphology and size of the frustules of diatom cells can be modified in different ways (Falasco et al., 2009). This variation in shape and size is important for the survival of diatoms under natural conditions, in terms of suspension in the water column, nutrient uptake, and absorption of light (e.g. Parsons and Takahashi, 1973; Jiang et al., 2005). Durbin (1977) reported that changes in temperature and available nutrients could cause the deformation of Thalassiosira nordenskioeldii. In T. weissflogii, the location and size of the labiate process (a structural feature of some diatoms) is affected by the concentration of silicate (Kang et al., 1996). Nagai and Imai (1999) have demonstrated that light intensity and salinity are important factors that affect the morphology of Coscinodiscus wailesii. Thus, in order to survive environmental changes, the morphology and size of many diatoms can vary often becoming either simpler or more elaborate (Geitler, 1932; Granetti, 1975). For example, in Eunotia species affected by environmental stresses, the undulation of the valve outline increases markedly across generations (Hustedt, 1955).

The marine diatom Ditylum brightwellii (West) Grunow is a cosmopolitan coastal species (Rynearson et al., 2006). In a life history of D. brightwellii, male gametangia (spermatogonangia) were observed in natural populations of the diatom during late summer and early autumn (e.g. Waite and Harrison, 1992), but were not found in an extensively sampled spring bloom (Rynearson and Armbrust, 2005). However, auxospores of D. brightwellii have apparently never been observed in natural populations (Koester et al., 2007). On a few occasions, gametes and auxospores have been reported in laboratory cultures, but published descriptions of the morphology of eggs and auxospores are inconsistent and misleading. Thus, information on sexual reproduction in D. brightwellii is mostly indirect or anecdotal. Many researchers have studied D. brightwellii with diverse goals, such as understanding its physiology, ecology, or molecular diversity. Montagnes and Franklin (2001) have examined the relationship between volume and growth rate and how it is affected by temperature. Rijstenbil et al. (1994) have reported that the cell volume of D. brightwellii increases upon the uptake of copper. Anderson and Sweeney (1977) have explained the relationship between exposure to light and rate of sinking, which is related to increases in cell density that are caused by the accumulation of carbohydrate. Brussaard et al. (1998) have examined cell growth under conditions of nutrient depletion or supplementation. Pickett-Heaps et al. (1988) have observed changes in the form of the labiate process during cell division. Rynearson and Armbrust (2004) have demonstrated the genetic diversity of two populations of D. brightwellii by analyzing microsatellite regions. Thereafter, Rynearson et al. (2006) observed that the populations of D. brightwellii in two regions with different environments were morphologically different: one population had a small cell diameter and the other a large cell diameter. Two forms of D. brightwellii have been described: a triangular or prism type (PT; see for example plate 48 on p. 228 in Hasle and Syvertsen, 1997), and a round or cylindrical type (CT; see for example Fig. 5 on p. 586 in Rijstenbil et al., 1994). However, it is not yet clear why different sizes and morphological types of D. brightwellii exist.

It has long been accepted that the eco-physiological variation of diatoms is influenced by ambient temperature (e.g. Eppley, 1972; Goldman and Carpenter, 1974). Many researchers have emphasized that the size of diatom cells decreases with increasing temperature (e.g. Atkinson, 1995; Montagnes and Franklin, 2001). However, some other studies have indicated that cell size increases with temperature (e.g. Thompson et al., 1992), or shows no clear trend with respect to temperature (e.g. Sournia, 1982). In D. brightwellii, Waite and Harrison (1992) have demonstrated that the CT becomes enlarged to form the PT after the haploid stage of the life cycle, and they have suggested that this morphological change is caused by physiological rather than environmental factors. On the other hand, Koester et al. (2007) have demonstrated that D. brightwellii in the vegetative state fluctuates between the CT and the PT, but it is not yet clear how the morphology of D. brightwellii changes between the CT and the PT. Moreover, little attention has been paid to the effect of environmental factors on the morphology of D. brightwellii.

The aims of the present study were as follows: (1) to investigate PT and CT cells of D. brightwellii using morphological characteristics described in our previous work (Lee and Youn, 2007); (2) to investigate the relationships between environmental factors and the dynamics of the size and morphological transition of D. brightwellii cells between PT and CT through field observations in the coastal waters of South Korea; and (3) to assess the effect of temperature on the transition between PT and CT cells of D. brightwellii in controlled laboratory experiments.

Section snippets

Morphological observations and measurement of cell volume

Morphological differences between PT and CT cells of D. brightwellii were assessed by light microscopy (LM) using an Axioskop 40 microscope (Zeiss, Göttingen, Germany) and scanning electron microscopy (SEM) using a JSM-5600LV microscope (Jeol, Tokyo, Japan). Cells were photographed using an MRc5 digital camera (Zeiss, Göttingen, Germany) attached to the light microscope. Diatom specimens were prepared for SEM as described by Jung et al. (2010). Briefly, live samples were fixed with a fixative

Morphological characteristics

The shape of the valve was triangular in PT and round in CT cells (Fig. 2). The mean valve diameter and pervalvar axis were 78.1 ± 3.9 μm and 94.3 ± 1.7 μm for PT cells, and 18.3 ± 1.9 μm and 97.8 ± 4.1 μm for CT cells, respectively. The mean cell volumes (size) of the PT and CT cells were 90,064 ± 1981 μm3 and 33,761 ± 1988 μm3, respectively (Table 2). The ratio of the valve-to-pervalvar diameters was 0.83 and 0.19 in PT and CT cells, respectively. The marginal spines were dotted on the valve

Discussion

Although the two Ditylum brightwellii cell types differ morphologically in terms of cell size, valve shape, marginal spines on the valve face, girdle surface, and diameters of the valve and pervalvar axis, the cell types are very similar genetically. Rynearson et al. (2006) have reported differences at only 10 bp out of a total of 2873 (18s rDNA to ITS2 region), which include 7 bp in ITS1 and 3 bp in ITS2. Thus, the two cell types show genetic homogeneity, although they differ morphologically.

Acknowledgments

We thank Professor David G. Mann for helpful comments and suggestions. Some field samples were obtained from Library of Marine Samples of Korea Institute of Ocean Science and Technology (KIOST), South Korea. This study was supported by a research fund from KIOST (PE98988, Study for promotion of ecological realism in enclosed mesocosm) and (PE98933, Standardization of in-situ diagnostic techniques on the dynamics of marine ecosystem structure), and from Korea Ministry of Environment (#416-111-008

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    Present address: Han River Environment Research Center, Yangsu-ri 476-823, Republic of Korea.

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