Temperature Promoting the Asexual Life Cycle Program in Bangia Fuscopurpurea (Bangiales, Rhodophyta) from Esashi in the Hokkaido Island, Japan

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Algal Resources (2018) 11：25-32

Temperature promoting the asexual life cycle program in Bangia fuscopurpurea (Bangiales, Rhodophyta) from Esashi in the Hokkaido Island, Japan

Koji MIKAMI1 * and Ikuya KISHIMOTO2

Abstract : In the asexual life cycle of the marine red seaweed Bangia fuscopurpurea gametophytic thalli produce multiple monospores that develop into thalli as clones. We investigated the effects of heat stress on the production and release of monospores in B. fuscopurpurea from Esashi, in northern Hokkaido Island of Japan. Non-lethal high temperatures of 25℃ and 28℃ strongly promoted monospore discharge, whereas no spore release was observed at 30℃, the limiting growth temperature of Esashi B. fuscopurpurea. These findings differed from previous reports using B. fuscopurpurea collected at Fukaura, the northern Japan, and at the Fujan province of southern China, for which growth and monospore release were observed at 30℃. Thus, the temperature range promoting asexual propagation with monospore discharge in B. fuscopurpurea varies and appears to be unrelated to the thermal conditions of harvesting areas. Since each B. fuscopurpurea strain had a unique upper-limit temperature for survival and release of monospores was accelerated under non-lethal high temperature conditions, the temperature range enabling the asexual life cycle program seems to be restricted by the degree of heat stress tolerance of the B. fuscopurpurea strains themselves.

Keywords : asexual propagation, Bangia fuscopurpurea, heat stress, life cycle

Introduction growth and development as a strategy for stress acclimation (Potters et al. 2007). Environmental fluctuation is a major factor As opposed to terrestrial plants, seaweeds are influencing the growth, development and sur- aquatic multicellular sessile organisms that ex- vival of terrestrial plants (Cramer et al. 2011; ist at the intertidal and subtidal zones. The Kumar et al. 2012; Pandey et al. 2017). For conditions in the intertidal zone especially ex- instance, an increase in the air temperature hibit drastic changes at both daily and yearly surrounding plants can lead to physiological scales (Rawlings 1999; Helmuth and Hofmann defects especially in reproductive processes 2001; Eckersley and Scrosati, 2012). Thus, sea- (Barnabas et al. 2008; Zinn et al. 2010; Hartfield weeds also are exposed to temperature fluctua- and Prueger 2015). However, stress-tolerance tions that influence their growth and develop- mechanisms can allow plants to acclimate to ment (Wiencke and Dieck 1989; Dudgeen et al. such environmental stresses (Nakashima et al. 1995; Ku bler and Davison 1993, 1995; Nejrup et 2014; Rejeb et al. 2014; Zhu 2016; Sade et al. 2017; al. 2013; De Silva and Asaeda 2017; Martins et Vishwakarma et al. 2017). Indeed, abiotic stres- al. 2017; Mikami et al. 2018; for review, Agrawal ses often bring about modulations of morpho- 2012; Singh and Singh 2015). Temperature is one genic responses, with inhibition or promotion of ofthemostvariablefactorsintheirenviron-

1 Faculty of Fisheries Sciences, Hokkaido University, 3-1-1 Minato-cho, Hakodate 041-8611, Japan 2 Graduate school of Fisheries Sciences, Hokkaido University, 3-1-1 Minato-cho, Hakodate 041-8611, Japan ＊Corresponding author : Tel / fax: +81-138-40-8899, e-mail: [email protected]

25 Koji MIKAMI and Ikuya KISHIMOTO ment, and seaweeds have acquired tolerance 2017). The asexual propagation in Bangiales has against temperature changes (Andersen et al. been studied mainly in Pyropia yezoensis and 2013; Smolina et al. 2016). However, it is un- Banga fuscopurpurea to date. In P. yezoensis, clear how heat stress-tolerance is regulated, which is a major cultivated species for nori although effects of temperature changes on production in Japan (Blouin et al. 2011), the compositions of amino acids and membrane production and release of monospores is accel- fatty acids have been demonstrated (Mikami et erated by a reduction in the extracellular al. 2011, 2018; de Costa et al. 2018; Song et al. calcium ion concentration (Takahashi et al. 2018), and transcriptional analyses have identi- 2010) and treatment of thalli with hydrogen fied a number of genes whose expression is up- peroxide (Takahashi and Mikami 2017). In or down-regulated by heat stress in various addition, asexual reproduction in thalli of P. seaweeds (Collen et al. 2007; Heinrich et al. 2012; yezoensis is also accelerated by irradiance (Li Choi et al. 2013; Im et al. 2015; Sun et al. 2015; 1984) and fragmentation associated with woun- Fan et al., 2017; Wang et al. 2018). ding (Hafting 1999). The effects of environmen- Seaweeds exhibit sexual reproduction with tal stresses on the asexual reproduction in B. isomorphic or heteromorphic diploid-haploid life fuscopurpurea have been examined only for cycle (Thornber 2006; Coelho et al. 2007; Cock et changes in temperature and photoperiod. These al. 2014; Liu et al. 2017). Among the Bangiales, studies indicated that heat stress stimulates the life cycle consists of a visible leafy thallus the formation and discharge of monospores and a microscopic filamentous conchocelis as a (Sommerfeild and Nichols 1973; Notoya and haploid gametophyte and a diploid sporophyte, Iijima 2003; Wang et al. 2008). Therefore, woun- respectively, both of which are multicellular and ding and heat stress might potentially act as live independently in different seasons of the triggers of the asexual life cycle program in year, and sexual reproduction is based on the Bangiales, suggesting that both biotic and abi- fertilization of male and female gametes pro- otic stresses are key regulators of both sexual duced in a gametophytic thallus to produce and asexual life cycle programs in red sea- carpospores that develop into a sporophytic weeds. conchocelis (Blouin et al. 2011; Mikami et al. Notoya and Iijima (2003) compared the opti- 2012; Takahashi and Mikami 2017). Since the mum temperature for growth and monospore rate of production of male and female gametes discharge and found differences in these pa- on gametophytes for sexual propagation is rameters for B. fuscopurpurea strains collected enhanced by increased temperature and photo- from Fukaura and Enoshima, located northern period (Kakinuma et al. 2006), it is possible that and central Japan, respectively. The Fukaura B. the sexual life cycle program is positively regu- fuscopurpurea was able to grow and release lated in part by heat stress in Bangiales, which monospores at 30℃,whereas25℃ was the would be similar to the green alga Volvox upper limit temperature for growth and mono- carteri (Kirk and Kirk 1986) and different from spore discharge for the Enoshima strain. Inter- the negative effects of heat stress on reproduc- estingly, B. fuscopurpurea from Fujan province tion in terrestrial plants (Barnaba s et al. 2008; in southern China was similar to the Fukaura Zinn et al. 2010; Hartfield and Prueger 2015). species [compare Notoya and Iijima (2003) and Therefore, effects of heat stress on the sexual Wang et al. (2008)]. These observations suggest reproductive process might differ between ter- that the prevailing temperature conditions in the restrial plants and algae. living areas do not correlate with the preferred As a remarkable characteristic, the life cycle temperature range for vegetative growth and of certain species of Pyropia, Porphyra, and the occurrence of asexual reproduction in B. Bangia in Bangiales includes an asexual pro- fuscupurpurea. gram via production of haploid neutral spores To address this possibility, we investigated or monospores from thalli (Blouin et al. 2011; whether B. fuscopurpurea collected at Esashi on Mikami et al. 2012; Takahashi and Mikami the northern Hokkaido Island of Japan exhibits

26 Temperature promoting the asexual life cycle program in Bangia fuscopurpurea (Bangiales, Rhodophyta) from Esashi in the Hokkaido Island, Japan difference in temperature range for survival and pores were determined daily for 7 days. monospore discharge compared to those col- To test viability, cells in thalli treated with lected in Fukaura, Enoshima, and Fujian. various temperatures for one to three weeks were visualized daily by staining with ESL Materials and Methods medium containing 0.01％ erythrosine (Wako Pure Chemical Industries, Japan). After stai- Algal material ning for 5 min at room temperature, thalli were Naturally growing B. fuscopurpurea gameto- gently rinsed with ESL medium to remove phytic thalli were collected at Esashi, Hokkaido, excess erythrosine and mounted on a slide with Japan on 14 May 2010. A clean single thallus ESL medium. Thalli were observed and photo- whose sex was unknown was cultured in graphed using an Olympus IX73 light micro- enriched sea life (ESL) medium (Kitade et al. scope equipped with an Olympus DP22 cam- 2002), which is made by dissolving commercially era, where cells stained by the dye were de- available SEALIFE powder (Marintech Co. Ltd., fined as dead cells. Viability was calculated by Japan) in distilled water (DW) with the addi- counting the living and dead cells using micro- tion of ESS２ solution, at 15℃ under irradiation graphs. of 60 mol m-2 s-1 provided by cool white fluo- The number of monospores discharged and rescent lamps (Neorumi super FL40SW, Mitsu- adheredonthebottomofa6well-microplate bishi, Japan) with a photo-period of 10 h light : with lid (Iwaki, Asahi Glass Co. Ltd., Japan) was 14 h dark. The medium was bubbled continu- counted daily for a week under the Olympus ously with filter-sterilized air and changed IX73 light microscope. weekly. Resultant unisexual B. fuscopurpurea gametophytes were subcultured continually as Results an experimental line. Effects of heat stress on cellular viability in ga- Determination of viability and the number of metophytes discharged monospores When B. fuscopurpurea gametophytes collect- Each 0.1 g (fresh weight) of B. fuscopurpurea ed at Esashi were incubated at 15, 20, 25 and gametophytic thalli was cultured in dishes 28℃, cells in every thallus were alive (Fig. 1). (Azunoru dish  90 × 20 mm height, As One) However, incubation at 30℃ reduced viability, containing 50 ml of the ESL medium under the such that ca. 50% of cells were dead after 3 same conditions mentioned above except for weeks of cultivation (Fig. 1). Thalli of this temperature at 20, 25, 28, 30, 32, and 34℃, while northern strain of B. fuscopurpurea did not control experiments were performed at 15℃. survive at 32℃ and 34℃ (Fig. 1). These results Under these various temperature conditions, indicated that 30℃ is the upper limit or par- viability and the number of released monos- tially lethal temperature for survival of thalli,

Fig. 1. Effects of temperature on the viability of Bagia fuscopurpurea gametophytic thalli. Samples of the laboratory-maintained culture strain were incubated at 15, 20, 25, 28, 30, 32, and 34℃ for 1 week (black bar), 2 weeks (gray bar) and 3 weeks (white bar) and then cells were stained with 0.01% erythrosine to calculate viability. Mean values (n = 3 ) ± SD are shown. Letters denote statistically significant differences (p ＜ 0.05) as determined by one-way ANOVA as described in Mikami et al. (2018).

27 Koji MIKAMI and Ikuya KISHIMOTO

Fig. 2. Early stages of the asexual life cycle program of Bangia fuscopurpurea. (A) Monospores discharged from a thallus. A cast-off uniseriate gametophyte remained as a cell wall skeleton after complete release of monospores. (B) Growing germlings of the two-cell stage. Scale bar=50 m.

meaning that 25℃ and 28℃ act as non-lethal Fig. 3. Promotion of the asexual life cycle by temperatures. non-lethal high temperature. Gametophytic thalli were incubated at 15, 20, 25, 28, 30, 32, Effects of heat stress on discharge of monos- and 34℃ for 1 week. The number of re- pores from gametophytic thalli leased monospores was counted every day Monospores were discharged from thalli (Fig. under the microscope. Mean values (n = 3 ) ± SD per 0.1 g of fresh weight samples were 2A) and then developed into gametophytes (Fig. calculated from results of three independ- 2B). Thus, we next examined the effects of high ent experiments. Letters denote statistically temperature on discharge of monospores. Dis- significant differences (p ＜ 0.05) as deter- charge of monospores was clearly observed 3 mined by one-way ANOVA as described in days after the temperature shift from 15℃ to Mikami et al. (2018). 25℃ and 28℃, and continued during further incubation under these temperatures, although the relationship between environmental thermal the number of released monospores varied conditions and specification of the temperature among triplicated experiments (Fig. 3). By con- range promoting the asexual life cycle in the red trast, 15℃ and 20℃ conditions had only a weak seaweed B. fuscopurpurea. Thus, we examined effect on monospore release, and no accumula- the effects of temperature on vegetative cell tion of monospores was observed upon incuba- survival and asexual life cycle propagation in B. tion at over 30℃ (Fig. 3). Together with the fuscopurpurea collected at Esashi in northern data shown in Fig. 1, we conclude that non- Japan to compare with established results from lethal, but not lethal, high temperature can Notoya and Iijima (2003) and Wang et al. (2008). stimulate asexual propagation in the northern B. We demonstrated that the upper limit for fuscopurpurea. viability of thalli was 30℃ and that non-lethal high temperatures such as 25℃ and 28℃ pro- Discussion moted the asexual life cycle program in Esashi B. fuscopurpurea (Figs. 1 and 3). These values The aim of the present study was to address were similar to those reported for Enoshima

28 Temperature promoting the asexual life cycle program in Bangia fuscopurpurea (Bangiales, Rhodophyta) from Esashi in the Hokkaido Island, Japan

B. fuscopurpurea (see Notoya and Iijima 2003) judge whether the classification of Bangia spe- and different from B. fuscopurprea strains cies into one genus should be revised. collected at Fukaura and Fujian, both of which As far as we know, heat stress-inducible were able to grow and release monospores at promotion of the asexual life cycle is unique to 30℃ (Notoya and Iijima 2003; Wang et al. 2008). B. fuscopurpurea. Indeed, our preliminary ex- Together, these results indicate that there is no periments showed that discharge of monos- correlation between thermal conditions of liv- pores from thalli of the marine red seaweed ing areas and the preferred temperature range Pyropia yezoensis andthefreshwaterredalgaB. for vegetative growth and asexual propagation; atropurpurea was not significantly accelerated however, it was found a relationship between under heat stress conditions (data not shown). growth under the non-lethal temperature and In addition, the regulatory mechanisms for promotion of asexual propagation. Therefore, we initiation of the asexual propagation in B. hypothesize that temperature ranges enabling fuscopurpurea collected in different areas might vegetative growth and asexual life cycle propa- have distinct temperature sensitivities. Al- gation in B. fuscopurpurea are determined by though the overall machinery regulating pro- the degree of thermotolerance in each organ- duction and release of monospores is thought to ism. be common in Bangiales, it is possible that there Our results clearly demonstrated the heat are components whose heat sensitivities differ stress-inducible promotion of the asexual prop- among species. How the strength of heat stress agation in B. fuscopurpurea; however, the ef- tolerance is differently determined among B. fects of heat stress on vegetative growth have fuscopurpurea strains from various areas has not been clarified, as we tested only survival not been elucidated. Thus, studies on regulato- rates of cells in gametophytic thalli. To per- ry mechanisms and heat stress-sensitive com- form a full comparison with previous reports ponents for formation and release of monos- (Notoya and Iijima 2003; Wang et al. 2008), as- pores are necessary to understand how the sessment of the effects of heat stress on growth degree of thermotolerance is determined and of monospore germlings should be performed in why the strength of heat stress tolerance varies the northern B. fuscopurpurea. These experi- among organisms collected in different areas. ments should help clarify the relationship be- Moreover, results from these studies could help tween heat stress tolerance and promotion of to judge the probability of the presence of asexual propagation in B. fuscopurpurea. taxonomic variation in the genus Bangia. Recent phylogenetic analyses show that seaweeds of the genus Bangia are highly diver- Acknowledgments gent and are classified into at least 4 distinct clades, based on combinational analysis of se- We thank Ryunosuke Irie for his assistance quences of the plastid Rubisco large subunit for data analyses. This study was supported in and nuclear small-subunit ribosomal RNA genes part by KAKENHI (15H04539). (Sutherland et al. 2011; Sanchez et al. 2014). These results suggest that the original genus References Bangia might be more correctly classified into different novel genera, although it is unclear Agrawal SC. Factors controlling induction of whether differences in heat sensitivities of reproduction in algae--review: the text. Re- the asexual life cycle programs of each B. view article. Folia Microbiol. 2012; 57 :87-407. fuscopurpurea strains correspond to differences Andersen GS, Pedersen MF, Nielsen SL. Tem- among clades of the phylogenetic trees. Thus, it perature acclimation and heat tolerance of is necessary to elucidate the relationship be- photosynthesis in Norwegian Saccharina tween heat stress sensitivity and phylogenetic latissima (Laminariales, Phaeophyceae). J. position in B. fuscopurpurea collected in vari- Phycol. 2013 ; 49 : 689-700. ous areas, which is an important approach to Barnaba sB,Ja ger K, Feher A. The effect of

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