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Communication

Heat Stress Memory Is Critical for Tolerance to Recurrent Thermostress in the Foliose Red Alga Pyropia yezoensis

by
Megumu Takahashi
1 and
Koji Mikami
2,*
1
Department of Ocean and Fisheries Science, Faculty of Bio-Industry, Tokyo University of Agriculture, 196 Yasaka, Abashiri 099-2493, Japan
2
Department of Food Resource Development, School of Food Industrial Sciences, Miyagi University, 2-2-1 Hatatate, Taihaku-ku, Sendai 982-0215, Japan
*
Author to whom correspondence should be addressed.
Phycology 2025, 5(3), 28; https://doi.org/10.3390/phycology5030028
Submission received: 27 May 2025 / Revised: 18 June 2025 / Accepted: 23 June 2025 / Published: 23 June 2025
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Abstract

Bangiales are photosynthetic organisms that grow in the intertidal zone, a region characterized by fluctuating environmental conditions. The order comprises genera exhibiting two different morphological variations, filamentous and foliose. It was recently demonstrated that the filamentous alga ‘Bangia’ sp. ESS1 possesses the intrinsic ability to “memorize” an experience of prior heat stress to enhance its survival under subsequent, normally lethal, high-temperature conditions via the acquisition of heat stress tolerance. Here, we investigated whether foliose red algae can similarly memorize heat stress to acquire thermotolerance. When Pyropia yezoensis thalli were primed with non-lethal, high-temperature treatments (22 and 25 °C) for 7 days, vegetative cells subsequently triggered with a normally lethal temperature of 30 °C showed dramatically increased survival rates, indicating that P. yezoensis can acquire heat stress tolerance via exposure to non-lethal high temperatures. In addition, when 22 °C-primed thalli were incubated at 15 °C for recovery, vegetative cells survived subsequent incubation at 30 °C; their survival rates varied depending on the duration of recovery. These findings indicate that, like filamentous red algae, the foliose species P. yezoensis memorizes heat stress to acquire tolerance to recurrent thermostress. The identification of heat stress memory in foliose Bangiales lays a foundation for improving the heat stress tolerance of these important algae, supporting the sustainability of the nori mariculture industry.

1. Introduction

Multicellular algae and terrestrial plants are photosynthetic organisms [1,2,3] whose sessile nature leaves them exposed to daily and seasonal changes in environmental conditions, including various types of abiotic stress [4]. To cope with these changes, these organisms sense and respond to stress signals and adjust their physiological status via the stress-inducible expression of genes that promote survival [5,6,7,8]. Among abiotic stress factors, heat is the most prominent environmental challenge experienced by sessile photosynthetic organisms. Indeed, two major factors critical for acclimation to heat stress are highly conserved in these organisms: heat shock proteins (HSPs), which help maintain the quality of intracellular proteins by functioning as molecular chaperones [9,10,11,12,13]; and heat shock factors (HSFs), which are transcription factors that direct heat-inducible expression of HSP genes [10,12,14,15,16]. In addition, recent findings on signal transduction pathways indicate the critical roles of the transient production of reactive oxygen species (ROS) and the influx of calcium ions (Ca2+) in promoting heat signal transduction, the activation of HSFs, and the induction of HSP gene expression [13,17,18,19,20,21]. Furthermore, heat stress causes physical changes in cellular membranes that activate heat stress signal transduction in both multicellular algae and terrestrial plants [22,23,24,25,26,27]. This suggests that these organisms sense stress-induced changes in membrane fluidity as heat stress, although they also seem to have membrane fluidity-independent, heat-sensing mechanisms [25]. Therefore, multicellular algae and terrestrial plants share similar mechanisms for regulating the heat stress response.
Most studies on the heat stress responses in photosynthetic organisms have involved a single exposure to high temperature. However, in natural environments, changes in conditions occur repeatedly, prompting the need to elucidate how sessile photosynthetic organisms acquire tolerance to recurrent exposure to heat stress. Studies addressing this issue have shown that stress memory is an important aspect of the intrinsic ability of these organisms to acquire tolerance to recurrent stress [28,29]. These studies have demonstrated that exposure of terrestrial plants to a moderate, non-lethal, high temperature (priming) establishes a stress memory, which enables the plants to survive subsequent exposure to higher temperatures that would normally be lethal [30,31]. In addition, studies on the regulatory mechanisms of stress memory have revealed that epigenetic regulation (via the methylation and acetylation of DNA and histones) helps maintain gene expression patterns altered by heat stress priming [31,32,33]. The resulting changes in physiological status lower the threshold of sensitivity to subsequent stress, allowing the plant to survive under normally lethal high temperatures. Furthermore, overexpressing and disrupting genes encoding HSFs, HSPs, and epigenetic-related factors increases and decreases plant tolerance to heat stress, respectively, indicating that these genes are involved in the establishment of heat stress memory [34,35]. These findings demonstrate that the acquisition of heat stress memory to “remember” prior exposure to heat stress is based on the functions of HSFs, HSPs, and epigenetic-related factors and that these factors are required for plant survival under recurrent changes in thermal conditions.
Although the regulatory mechanisms of heat stress memory in multicellular algae have not been fully elucidated, there have been several studies of heat stress memory on species of the filamentous red algal genus Bangia. Bangia species are currently classified into one genus, Bangia, and three additional groups: ‘Bangia’ 1, ‘Bangia’ 2, and ‘Bangia’ 3 [36]. Kishimoto et al. [37] demonstrated an intrinsic ability to acquire heat stress memory in ‘Bangia’ sp. ESS1, a member of ‘Bangia’ 2 [38], representing the first report of stress memory in algae. The intrinsic ability to memorize heat stress varies among filamentous Bangia species. For instance, the marine alga ‘Bangia’ sp. ESS2, belonging to ‘Bangia’ 3 [39], and the freshwater species Bangia atropurpurea [40] are unable to acquire heat stress memory to cope with recurrent heat stress exposure [39]. To date, ‘Bangia’ sp. ESS1 is the only multicellular alga known to memorize heat stress [37,39,41].
The heat stress response has been extensively studied in the marine foliose red alga Pyropia yezoensis. This edible alga serves as an important resource for the nori mariculture industries in Japan, South Korea, and China [42]. Genes encoding HSPs have been identified in this species genome-wide [11,13,25,43,44,45]. Expression analysis suggests the involvement of these genes in responses to heat stress and other abiotic stresses such as dehydration stress and cold stress, as well as stress-induced ROS accumulation [11,13,25,43,44,45]. Moreover, we previously demonstrated that P. yezoensis employs membrane fluidity-dependent and -independent intracellular heat signal transduction pathways that regulate their component heat stress- inducible genes [25,26].
Despite our understanding of the response to heat stress and the changes in HSP gene expression induced by heat stress priming, it is unclear whether P. yezoensis can establish heat stress memory to acquire tolerance to recurrent heat stress exposure. Therefore, in the present study, we investigated whether the foliose alga P. yezoensis can memorize heat stress. Our findings provide insight into the significance of heat stress memory in response to recurrent heat stress in a foliose Bangiales species.

2. Materials and Methods

2.1. Maintenance of Algal Materials

P. yezoensis (strain U-51) thalli were maintained in a Provasoli-enriched seawater (PES) medium [46] in which Tris [Tris (Hydroxymethyl) aminomethane] was replaced with HEPES [4-(2-hydroxyethyl)-1-piperazineethanesulfonic acid]. The thalli were cultured with 60 μmol photons m−2 s−1 light under a long-day photoperiod (10 h light/14 h dark) at 15 °C, with aeration using sterilized air filtered through a 0.22 μm filter (Whatman, Maidstone, UK). The PES medium was changed weekly.

2.2. Heat Stress Treatment

Before starting the experiments, the thalli under aeration culture at 15 °C were preincubated with aeration in a conical flask (500 mL) containing 500 mL of PES medium at 15 °C for 7 days. The thalli were exposed to three types of heat stress treatment. To examine sensitivity to heat stress, each 0.01 g (fresh weight) thallus sample was incubated at 22, 25, 28, or 30 °C for 1, 3, or 7 days. To confirm the ability to acquire heat stress tolerance, each 0.01 g (fresh weight) thallus sample was incubated at 22 or 25 °C for 7 days (priming) plus subsequent treatment at 25, 28, or 30 °C for 1, 3, 5, or 7 days (triggering). Finally, to confirm the ability to memorize heat stress, each 0.01 g (fresh weight) thallus sample was incubated at 22 or 25 °C for 7 days (priming), returned to 15 °C and incubated for 3 or 7 days (recovery), and subsequently treated at 28 or 30 °C for 1 to 7 days (triggering). All experiments were performed by incubation in conical flasks containing 500 mL PES medium with aeration. The experiments were repeated three times per condition.

2.3. Calculation of Viability Rate

Viability rate was determined as described in [39]. In brief, heat stress-treated thalli were stained with artificial seawater containing 0.01% (w/v) erythrosine (FUJIFILM Wako Pure Chemical Industries, Osaka, Japan) for 5 min at room temperature and gently rinsed with artificial seawater to remove the excess erythrosine. The stained thalli were mounted on a slide with artificial seawater and photographed under an Olympus IX73 light microscope (Olympus Corporation, Tokyo, Japan) equipped with an Olympus DP22 camera (Olympus Corporation, Tokyo, Japan); cells stained by the dye were defined as dead cells. Viability of vegetative cells in thalli was calculated as the number of living vs. dead cells in micrographs; analysis of samples under each heat stress treatment was repeated three times.

2.4. Statistical Analysis

Mean values ± SD were calculated from triplicate experiments. Statistically significant differences in the interactions between the duration of incubation under different heat stress conditions and viability were determined by Kruskal–Wallis coupled with Dunn–Bonferroni tests using a cut-off value of p < 0.05.

3. Results

3.1. Heat Stress Sensitivity of Thalli Cultured at 15 °C

Thalli precultured at 15 °C were subsequently incubated at 25, 28, or 30 °C (Figure 1A). Most vegetative cells in thalli were alive following incubation at 25 °C for 7 days (Figure 1B and Figure S1). However, incubation at 28 or 30 °C decreased the survival rate in a duration-dependent manner. Vegetative cells were completely dead following incubation at 30 °C for 7 days, whereas incubation at 28 °C had a weaker effect on reducing the proportion of living cells (Figure 1B). Photographs of the erythrosine staining results for these experiments are shown in Figure S1. These results indicate that 22 and 25 °C are non-lethal while 28 and 30 °C are lethal for P. yezoensis U-51 thalli grown under our experimental conditions.

3.2. Acquisition of Heat Stress Tolerance

The ability to acquire heat stress tolerance can be assessed by determining whether priming with non-lethal high temperatures leads to survival under subsequent exposure to lethal heat stress. Thus, we incubated P. yezoensis thalli at 22 or 25 °C for 7 days for priming, followed by incubation at 25, 28, or 30 °C for 1, 3, 5, or 7 days for triggering (Figure 2A). As shown in Figure 2B,C, priming by incubation at 22 or 25 °C for 7 days resulted in a 95–100% survival rate for vegetative cells in thalli subsequently exposed to 25 or 28 °C for 7 days. By contrast, incubation at 28 °C without priming dramatically reduced the survival rates of vegetative cells, with survival rates of only 33 and 10% after 5 and 7 days of incubation, respectively (Figure 1B). These findings indicate that P. yezoensis thalli can acquire thermotolerance by priming at 22 or 25 °C. Photographs of the erythrosine staining results for these experiments are shown in Figure S2.
When triggering was performed via incubation at 30 °C, we observed high viability rates of 90–100% after 1 day of heat stress (Figure 2B,C). In addition, survival rates of 60% and 15% were observed in thalli primed at 22 or 25 °C, respectively, after 3 days of triggering at 30 °C. These values are significantly higher than the 2% survival rate following incubation at 30 °C for 3 days without priming (Figure 1B and Figure 2B,C). Figure S2 shows the erythrosine staining results for these experiments. These findings are consistent with the results following 28 °C triggering described above.
Unexpectedly, 22 °C priming resulted in a higher survival rate in response to 30 °C triggering, especially after 1 or 3 days of incubation, compared with priming at 25 °C (compare Figure 2B,C). Thus, a priming temperature of 22 °C might be optimal for establishing high-level tolerance to subsequent heat stress in P. yezoensis thalli. Accordingly, we used the 22 °C priming treatment in subsequent experiments.

3.3. Memorization of Prior Heat Stress Enhances Survival Under Normally Lethal Temperatures

To test the ability of P. yezoensis thalli to acquire thermotolerance, we inserted a recovery phase at 15 °C for 0, 3, 5, or 7 days between the priming treatment at 22 °C for 7 days and triggering at 28 or 30 °C for 7 days (Figure 3A). Following 3, 5, or 7 days of recovery, almost 100% survival was detected after 1 day of triggering at 28 or 30 °C (Figure 3B,C). These results indicate that vegetative cells in P. yezoensis thalli can memorize prior non-lethal heat stress to enable them to survive subsequent exposure to normally lethal temperatures, meaning they can acquire heat stress tolerance.
However, the survival rate gradually decreased during triggering in a duration-dependent manner. For example, under 22 °C priming + 7-day recovery + 28 °C triggering treatment, the survival rate decreased to 61% and 17% after 5 or 7 days of triggering, respectively (Figure 3B), while 30 °C triggering for more than 5 days after a 7-day recovery resulted in quite low viability (Figure 3C). Photographs of the results of erythrosine staining after 28 °C and 30 °C triggering are shown in Figures S3 and S4, respectively. These findings indicate that vegetative cells in P. yezoensis thalli “forgot” heat stress under normally lethal temperatures, with a more severe loss in survival after 30 °C vs. 28 °C triggering (compare Figure 3B,C).

4. Discussion

Our results demonstrate that P. yezoensis thalli can “remember” the experience of exposure to non-lethal high temperatures such as 22 and 25 °C via the establishment of heat stress memory, which is responsible for the acquisition of heat stress tolerance and survival under subsequent exposure to normally lethal high temperatures such as 28 and 30 °C. In addition, the memory of heat stress exposure was maintained for at least 7 days after priming at 22 °C. However, heat stress memory was not stably maintained during triggering with normally lethal high temperatures, indicating the presence of a distinct period for the availability of memory. This is the first report to our knowledge of heat stress memory in a foliose Bangiales species.
We previously demonstrated that the presence or absence of the acquisition of thermostress tolerance based on heat stress memory is species-dependent among filamentous Bangia: ‘Bangia’ sp. ESS1 memorizes heat stress to acquire thermostress tolerance, whereas ‘Bangia’ sp. ESS2 and Bangia atropurpurea do not [37,39]. To the best of our knowledge, such variation in the capacity for heat stress memory appears to be a unique feature of filamentous Bangiales compared with terrestrial plants. However, the presence of heat stress memory in foliose Bangiales species other than P. yezoensis is unknown. In general, environmental conditions in the intertidal zone containing Bangiales species are seasonally variable, especially the temperature of the seawater, which determines the duration of survival of individual species. Thus, we propose that the requirement for heat stress memory in the thermostress response also differs among foliose Bangiales in a species-dependent manner. This hypothesis must be experimentally confirmed in order to understand the relationship between the temporal and latitudinal distributions of foliose Bangiales species with or without heat stress memory and the strategies of their heat stress responses.
The regulatory mechanisms that establish and maintain heat stress memory in Bangiales have not been elucidated. However, as previously demonstrated, in P. yezoensis, the heat stress-inducible expression of HSP70 genes is transient; heat stress is perceived by this organism as changes in membrane fluidity and other unknown changes in cells [25,26]. Moreover, in ‘Bangia’ sp. ESS1, the loss of heat stress memory is highly correlated with the rigidification of fluidized membranes during the recovery phase [37]. Accordingly, we reason that factors that maintain the expression of HSP70 genes and the fluidization status of membranes might be involved in the establishment and maintenance of heat stress memory in Bangiales. To test this hypothesis, it will be important to analyze the mechanisms regulating the expression of HSP genes by identifying transcription factors such as HSFs and signaling molecules that activate heat stress signal transduction pathways in Pyropia and Bangia species; however, little is known about how these factors contribute to heat stress memory. Therefore, functional analysis of these signaling molecules and HSFs will be indispensable for elucidating the molecular mechanisms regulating the establishment and maintenance of heat stress memory in both foliose and filamentous red algae in order to understand how the priming-dependent establishment of heat stress memory is maintained during the recovery phase to acquire tolerance to recurrent heat exposure.
We recently identified genes in ‘Bangia’ sp. ESS1 whose expression is induced only by exposure to recurrent heat stress [41]. Thus, it is possible that a regulatory mechanism directs heat stress-inducible gene expression that is activated by triggering but not priming. Identifying other triggering-inducible genes in both filamentous Bangia and foliose Pyropia species and elucidating the transcriptional regulation of these genes could increase our understanding of how heat stress memory functions in the acquisition of tolerance to recurrent heat stress exposure in Bangiales.
Our findings on heat stress memory could facilitate the breeding of novel varieties of Bangiales with enhanced tolerance to recurrent heat stress. Since global warming has recently led to increases in seawater temperature, causing considerable damage to the nori mariculture industry, there is a strong need to create novel Bangiales varieties with resistance to recurrent heat stress. Genetic modification targeting genes encoding factors involved in the establishment and maintenance of heat stress memory would be a highly reliable approach for creating heat stress-resistant Bangiales varieties and could contribute to the development of a sustainable mariculture industry. However, methods for reverse genetics and genetic modification have not yet been fully developed in Bangiales [47], although successful genome editing in P. yezoensis has been reported [48]. Therefore, developing methodologies for genetic modification and studying the regulatory mechanisms of heat stress memory in P. yezoensis will lay the foundation for identifying target genes for genetic modification and creating novel heat stress-resistant varieties of Bangiales, which would support the sustainability of the nori mariculture industry.

Supplementary Materials

The following supporting information can be downloaded at: https://www.mdpi.com/article/10.3390/phycology5030028/s1; Figure S1: Effects of heat treatment on the viability of vegetative cells in Pyropia yezoensis thalli; Figure S2: Effects of priming with non-lethal high temperatures on the viability of vegetative cells in Pyropia yezoensis thalli at normally lethal temperatures; Figure S3: Effects of priming and recovery on the viability of vegetative cells in 22 °C-primed Pyropia yezoensis thalli at the normally lethal temperature of 28 °C; Figure S4: Effects of priming and recovery on the viability of vegetative cells in 22 °C-primed Pyropia yezoensis thalli at the normally lethal temperature of 30 °C.

Author Contributions

Conceptualization, K.M.; Methodology, K.M. and M.T.; Validation, M.T.; Formal Analysis, K.M. and M.T.; Investigation, M.T.; Data Curation, M.T.; Writing—Original Draft Preparation, K.M.; Writing—Review and Editing, K.M.; Visualization, M.T.; Project Administration, K.M. All authors have read and agreed to the published version of the manuscript.

Funding

This research received no external funding.

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

Data are contained within this article or Supplementary Materials.

Acknowledgments

We are grateful to the Marine Resources Research Center of Aichi Fisheries Research Institute for kindly providing P. yezoensis strain U51.

Conflicts of Interest

The authors declare no conflicts of interest.

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Figure 1. Determination of non-lethal and lethal high temperatures in Pyropia yezoensis. (A) Schematic representation of the experimental design to assess the ability of vegetative cells in thalli to survive under high-temperature conditions. (B) Quantification of viability. Viability of vegetative cells in thalli incubated at 25, 28, or 30 °C was examined 1, 3, 5, and 7 days after the temperature shift by staining with 0.01% erythrosine. Error bars indicate the standard deviation of triplicate experiments (N = 3), and different lowercase letters denote significant differences in viability rate based on three independent experiments (n = 3), as determined by Kruskal–Wallis coupled with Dunn–Bonferroni tests (p < 0.05).
Figure 1. Determination of non-lethal and lethal high temperatures in Pyropia yezoensis. (A) Schematic representation of the experimental design to assess the ability of vegetative cells in thalli to survive under high-temperature conditions. (B) Quantification of viability. Viability of vegetative cells in thalli incubated at 25, 28, or 30 °C was examined 1, 3, 5, and 7 days after the temperature shift by staining with 0.01% erythrosine. Error bars indicate the standard deviation of triplicate experiments (N = 3), and different lowercase letters denote significant differences in viability rate based on three independent experiments (n = 3), as determined by Kruskal–Wallis coupled with Dunn–Bonferroni tests (p < 0.05).
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Figure 2. Confirmation of the ability to acquire heat stress tolerance in Pyropia yezoensis. (A) Schematic representation of the experimental design to assess the ability of P. yezoensis thalli to acquire heat stress tolerance. Thalli cultured at 15 °C were primed at 22 or 25 °C for 7 days and then triggered by incubation at 25, 28, or 30 °C for 1, 3, 5, or 7 days. (B,C) Quantification of viability. Viability of vegetative cells in thalli incubated at 25, 28, or 30 °C for 1, 3, 5, or 7 days after priming at 22 °C (B) or 25 °C (C), as determined by staining with 0.01% erythrosine. Error bars indicate the standard deviation of triplicate experiments (N = 3), and different lowercase letters denote significant differences in viability rate based on three independent experiments (n = 3), as determined by Kruskal–Wallis coupled with Dunn–Bonferroni tests (p < 0.05).
Figure 2. Confirmation of the ability to acquire heat stress tolerance in Pyropia yezoensis. (A) Schematic representation of the experimental design to assess the ability of P. yezoensis thalli to acquire heat stress tolerance. Thalli cultured at 15 °C were primed at 22 or 25 °C for 7 days and then triggered by incubation at 25, 28, or 30 °C for 1, 3, 5, or 7 days. (B,C) Quantification of viability. Viability of vegetative cells in thalli incubated at 25, 28, or 30 °C for 1, 3, 5, or 7 days after priming at 22 °C (B) or 25 °C (C), as determined by staining with 0.01% erythrosine. Error bars indicate the standard deviation of triplicate experiments (N = 3), and different lowercase letters denote significant differences in viability rate based on three independent experiments (n = 3), as determined by Kruskal–Wallis coupled with Dunn–Bonferroni tests (p < 0.05).
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Figure 3. Confirmation of the ability to memorize heat stress in Pyropia yezoensis. (A) Schematic representation of the experimental design to assess the ability of P. yezoensis thalli to memorize heat stress. Thalli maintained at 15 °C were primed at 22 °C for 7 days, allowed to recover by incubation at 15 °C for 1, 3, 5, or 7 days, and triggered by incubation at 28, or 30 °C for 1, 3, 5, or 7 days. (B,C) Quantification of viability. Viability of vegetative cells in thalli triggered at 28 °C (B) or 30 °C (C) for 7 days following recovery at 15 °C for 1, 3, 5, or 7 days after priming at 22 °C, as determined by staining with 0.01% erythrosine. Error bars indicate the standard deviation of triplicate experiments (N = 3), and different lowercase letters denote significant differences in viability rate based on three independent experiments (n = 3), as determined by Kruskal–Wallis coupled with Dunn–Bonferroni tests (p < 0.05).
Figure 3. Confirmation of the ability to memorize heat stress in Pyropia yezoensis. (A) Schematic representation of the experimental design to assess the ability of P. yezoensis thalli to memorize heat stress. Thalli maintained at 15 °C were primed at 22 °C for 7 days, allowed to recover by incubation at 15 °C for 1, 3, 5, or 7 days, and triggered by incubation at 28, or 30 °C for 1, 3, 5, or 7 days. (B,C) Quantification of viability. Viability of vegetative cells in thalli triggered at 28 °C (B) or 30 °C (C) for 7 days following recovery at 15 °C for 1, 3, 5, or 7 days after priming at 22 °C, as determined by staining with 0.01% erythrosine. Error bars indicate the standard deviation of triplicate experiments (N = 3), and different lowercase letters denote significant differences in viability rate based on three independent experiments (n = 3), as determined by Kruskal–Wallis coupled with Dunn–Bonferroni tests (p < 0.05).
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MDPI and ACS Style

Takahashi, M.; Mikami, K. Heat Stress Memory Is Critical for Tolerance to Recurrent Thermostress in the Foliose Red Alga Pyropia yezoensis. Phycology 2025, 5, 28. https://doi.org/10.3390/phycology5030028

AMA Style

Takahashi M, Mikami K. Heat Stress Memory Is Critical for Tolerance to Recurrent Thermostress in the Foliose Red Alga Pyropia yezoensis. Phycology. 2025; 5(3):28. https://doi.org/10.3390/phycology5030028

Chicago/Turabian Style

Takahashi, Megumu, and Koji Mikami. 2025. "Heat Stress Memory Is Critical for Tolerance to Recurrent Thermostress in the Foliose Red Alga Pyropia yezoensis" Phycology 5, no. 3: 28. https://doi.org/10.3390/phycology5030028

APA Style

Takahashi, M., & Mikami, K. (2025). Heat Stress Memory Is Critical for Tolerance to Recurrent Thermostress in the Foliose Red Alga Pyropia yezoensis. Phycology, 5(3), 28. https://doi.org/10.3390/phycology5030028

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