'This information advances our understanding of important processes occurring during the winter and transition seasons when science activity is limited. Their findings are also important in the context of a rapidly changing polar ecosystem.' Diatoms are a dominant phytoplankton species of polar marine habitats and contribute significantly to primary production. Standing winter communities of diatoms, as well as community dynamics during the abrupt shift from winter to the annual ice break-up in the summer, are thought to contribute significantly to summer blooms (Niemi et al., 2011). Diatom communities are negatively impacted by climate-related change. For example, in the western Antarctic Peninsula, over time cryptophyte populations are replacing diatoms (Mendes et al., 2023).

Hypometabolism, or 'physiological fasting', is a common phenomenon among hibernating mammals as a winter survival strategy: it involves a massive rewiring of the metabolism to severely limit energy consumption (Heldmaier et al., 2004). Mammalian hibernation is of interest in human physiology: many potential problems faced by hibernating animals mimic human diseases, such as cardiovascular function, kidney failure, muscle wasting, and osteoporosis (Berg von Linde et al., 2015). While the ramping down of metabolism has been reported several times in overwintering polar algae (e.g. Baldisserotto et al., 2005;Lacour et al., 2019), the phenomenon of hypometabolism has not been considered for nonmammalian overwintering lifeforms. Joli et al. pose an interesting hypothesis that overwintering diatoms, specifically the Antarctic diatom Fragilariopsis cylindrus, rely on a hibernation-like metabolism to shore up their odds of survival during the long, cold and dark polar night. Phytoplankton from polar regions share a critical challenge with overwintering mammals: severe limitation of their primary energy source. For Antarctic and Arctic phytoplankton, this energy loss is directly due to the sun dropping below the horizon for 4-6 months.

Fragilariopsis cylindrus is a model diatom species for cold adaptation of photosynthesis (Mock et al., 2017) and is a significant member of Antarctic marine phytoplankton communities (Lizotte, 2001). Joli et al. used an integrative approach to dissect polar night survival of F. cylindrus at the level of transcriptomics, microscopy, biochemistry, and photobiology. Cultures stopped dividing 3 d into the 86-d polar night treatment; total cellular carbon, nitrogen, and pigments declined by 50% by the end of the dark period. Significant subcellular arrangements were associated with long-term dark adaptation, including a reduction in thylakoid size and the development of a large vacuole. Morphological changes were accompanied by the downregulation of photophysiology and carbon fixation; although, photosystem II photochemistry potential remained high throughout the dark treatment. In addition, significant changes in the transcriptome favored metabolism associated with autophagy processes. Autophagy appears to be a major survival strategy in the polar diatom to remobilize energy reserves to maintain energy homeostasis by slow metabolism of molecules such as energy-rich fatty acids. The large vacuole provides a location for these processes and protects other cellular components from oxidative damage (Fig. 1a).

Transition from polar winter conditions to summer is an abrupt and potentially stressful environment for polar phytoplankton. Following the incubation under winter conditions, F. cylindrus was returned to conditions that mimic the ice break-up during the transition from winter to summer. Upon reintroduction to summer conditions, F. cylindrus relied on the activation of photoprotection followed by rapid onset of photosynthetic activity. However, even before summer, there is evidence that the diatom keeps photosynthetic processes primed throughout the winter. The production of chlorophyll precursors in the dark appears to contribute to the rapid onset of photosynthesis when light returns. Preparation for the long polar winter, as well as winter survival, has been studied in other Antarctic phytoplankton species. In the Antarctic lake green alga, Chlamydomonas priscuii, studies under laboratory controlled and in situ incubation experiments have revealed that it maintains its major photosynthetic apparatus during the polar winter, albeit in a functionally downregulated state, in a physiological process resembling overwintering in evergreen trees (Morgan-Kiss et al., 2005;Morgan-Kiss et al., 2006;Fig. 1b). An in situ incubation experiment performed within the native environment (Lake Bonney, McMurdo Dry Valleys, Antarctica) showed that the expression of the reaction center and carbon fixation genes was gradually downregulated in transplanted C. priscuii cultures during the transition from summer to winter (Morgan-Kiss et al., 2016). These trends in the isolate fit well with responses to the polar night transition in native communities of chlorophytes, which are obligate photosynthetic microorganisms (Kong et al., 2012). By contrast, mixotrophic phytoplankton in Antarctic lakes, including the cryptophyte Geminigera sp. and a haptophyte Isochrysis sp., remain active during the winter by switching to bacteriovorus heterotrophic metabolism (Li et al., 2016;Patriarche et al., 2021;Fig. 1c).

Joli et al. have shed additional light on what polar phytoplankton are doing in the dark. Their findings contribute complementary data on adjustments made to carbon metabolism to a breadth of previous work that has focused on the light harvesting side of photosynthesis. Taken together, these studies show us that, in addition to the adaptive strategies that polar algae employ to conduct photosynthesis under permanent low temperatures, Antarctic phytoplankton have a toolbox of physiological responses to survive the long winter and hit the ground running when the sun comes over the horizon again. This information advances our understanding of important processes occurring during the winter and transition seasons when science activity is limited. Their findings are also important in the context of a rapidly changing polar ecosystem. Coastal marine Antarctic environments are threatened by warming temperatures and changes in sea ice extent. These changes will undoubtably impact the overwinter survival of the primary producers that fuel this diverse and productive ecosystem. The Antarctic marine diatom, Fragilariopsis cylindrus, acclimates to the polar night by rewiring its carbon metabolism and forming a large vacuole, which allows it to switch to a hibernation-like state of hypometabolism (Joli et al., 2024, in this issue of New Phytologist, 2193-2208). (b) The Antarctic lake chlorophyte, Chlamydomonas priscuii, switches its photosynthetic apparatus to a downregulated state during the polar night, similar to the overwintering process in evergreen trees (Morgan-Kiss et al., 2006, 2016). Both strategies allow the Antarctic marine and lake phytoplankton to rapidly switch back to light energy capture and carbon fixation when the sun returns. (c) However, mixotrophic algae, such as the Antarctic lake Isochrysis sp. MDV, remain active in the winter by switching from photosynthesis to predation, dominating lake phytoplankton communities throughout the winter months (Li et al., 2016;Patriarche et al., 2021). New Phytologist (2024) 241: 1885-1887 www.newphytologist.com Ó 2024 The Authors New Phytologist Ó 2024 New Phytologist Foundation Commentary Forum New Phytologist