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When Unity Is Strength: the Strategies Used by Chlamydomonas to Survive Environmental Stresses

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When Unity Is Strength: the Strategies Used by Chlamydomonas to Survive Environmental Stresses cells Review When Unity Is Strength: The Strategies Used by Chlamydomonas to Survive Environmental Stresses Félix de Carpentier 1,2 , Stéphane D. Lemaire 1 and Antoine Danon 1,* 1 Institut de Biologie Physico-Chimique, UMR 8226, CNRS, Sorbonne Université, 75005 Paris, France; [email protected] (F.d.C.); [email protected] (S.D.L.) 2 Faculty of Sciences, Doctoral School of Plant Sciences, Université Paris-Sud, Paris-Saclay, 91400 Orsay, France * Correspondence: [email protected]; Tel.: +33-158415100 Received: 13 September 2019; Accepted: 21 October 2019; Published: 23 October 2019 Abstract: The unicellular green alga Chlamydomonas reinhardtii is a valuable model system to study a wide spectrum of scientific fields, including responses to environmental conditions. Most studies are performed under optimal growth conditions or under mild stress. However, when environmental conditions become harsher, the behavior of this unicellular alga is less well known. In this review we will show that despite being a unicellular organism, Chlamydomonas can survive very severe environmental conditions. To do so, and depending on the intensity of the stress, the strategies used by Chlamydomonas can range from acclimation to the formation of multicellular structures, or involve programmed cell death. Keywords: stress responses; acclimation; palmelloid; aggregation; programmed cell death 1. Introduction The photosynthetic green alga Chlamydomonas reinhardtii is the most prominent model organism in the green algae lineage for both basic research and biotechnological applications. One of the current challenges for a better understanding of the functioning of this unicellular model organism is to understand how it adapts to hostile environmental conditions. While the different stress response strategies of multicellular photosynthetic organisms are now well known (e.g., programmed cell death (PCD), hypersensitive reaction, and autophagy) [1], much less is known for unicellular organisms like Chlamydomonas. Nevertheless, several reports have described the response to environmental stresses of Chlamydomonas, showing how this alga is able to adapt and trigger specific responses according to the intensity of the stress it faces. For instance, in Chlamydomonas, like in other photosynthetic organisms, environmental stresses most often result in the disturbance of photosynthesis and the production of reactive oxygen species (ROS) [2–6]. The first line of defense aims at containing the occurrence of this oxidative stress by decreasing ROS production and increasing ROS degradation using multiple strategies, such as non-photochemical quenching [7], alternative electron transport pathways [7,8], or the activation of antioxidant enzymes and pathways [6]. If these strategies are not sufficient to limit the impact of environmental stresses on the cell, Chlamydomonas will trigger alternate processes. The first strategy is acclimation which consists of building stronger defenses to protect the cell against future stress episodes. If acclimation does not provide sufficient protection to the cell, the socialization processes will be triggered, which ranges from the formation of multicellular structures to the outbreak of PCD. In all cases, interaction between Chlamydomonas cells will allow survival under severe stress conditions. In this review, we will describe the different strategies implemented by Chlamydomonas to survive environmental stresses. Cells 2019, 8, 1307; doi:10.3390/cells8111307 www.mdpi.com/journal/cells Cells 2019, 8, 1307 2 of 16 2. Coping Strategies for Moderate Stress Cells 2019, 8, x FOR PEER REVIEW 2 of 16 2.1. Acclimation: Building Defenses to Protect Cells from Future Stresses 2. Coping Strategies for Moderate Stress Acclimation is regarded as an environmentally-induced, short-term response leading to an improved2.1. Acclimation: tolerance Building to subsequent Defenses to Protect stresses Cells [9 from]. In FutureChlamydomonas Stresses , acclimated cells are known to survive stress that would kill non-acclimated cells. Acclimation has been shown to be induced by Acclimation is regarded as an environmentally-induced, short-term response leading to an several stresses, including ROS [10,11], UV-B [12], salt [13], and ionic stress [14]. Interestingly ROS, improved tolerance to subsequent stresses [9]. In1 Chlamydomonas, acclimated cells are known to suchsurvive as hydrogen stress peroxidethat would (H kill2O 2non) or-acclimated superoxide cells. ( O Acclimation2), induce specific has been acclimation shown to be pathways, induced by and no crossseveral acclimation stresses, between including di ROSfferent [10,11] ROS, UV is- observedB [12], salt [[13]9,10, ].and Similarly, ionic stress in [14] plants,. Interestingly specific ROS, signaling pathwayssuch as are hydrogen associated peroxide with (H di2Offerent2) or superoxide ROS [15]. (1O In2),Chlamydomonas induce specific acclimation, singlet oxygen pathways, acclimation and no is mediatedcross byacclimation the key regulator between SAK1different (singlet ROS is oxygen observed acclimation [9,10]. Similarly, knocked-out in plants, 1) and specific the sak1signaling mutant is 1 unablepathways to acclimate are associated to O2 [10 with]. SAK1 different is a basicROS [15] leucine. In Chlamydomonas zipper (bZIP), transcription singlet oxygen factor acclimation that regulates is the expressionmediated by of the important key regulator genes SAK1 involved (singlet inoxygen acclimation, acclimation including knockedglutathione-out 1) and the peroxidase sak1 mutant—GPXH , and glutathioneis unable to S-transferase acclimate to— GSTS11O2 [10][. 10SAK1]. SOR1 is a (Singletbasic leucine Oxygen zipper Resistant (bZIP) 1) transcription is also a bZIP factor transcription that regulates the expression of important genes involved in acclimation,1 including glutathione factor, and the corresponding mutant, which is more resistant to O2, has higher levels of GPXH and peroxidase—GPXH, and glutathione S-transferase—GSTS1 [10]. SOR1 (Singlet Oxygen Resistant 1) is GSTS1 transcripts [16]. also a bZIP transcription factor, and the corresponding mutant, which is more resistant to 1O2, has Ithigher seems levels that of atGPXH least and some GSTS1 of thetranscripts mechanisms [16]. controlling acclimation in Chlamydomonas are conservedIt inseems plants. that at For least example some of UV-B the mechanisms acclimation controlling in plants acclimation is mainly controlledin Chlamydomonas by UVR8 are (UV resistanceconserved locus in 8) plants. that interacts For example with COP1UV-B acclimation (constitutively in plants photomorphogenic is mainly controlled 1) to by induce UVR8 a signaling(UV pathwayresistance involving locus the8) that bZIP interacts transcription with COP1 factors (constitutively HY5 (elongated photomorphogenic hypocotyl 5)1) andto induce HYH a (HY5 homolog)signaling [17]. pathway In Chlamydomonas involving the, the bZIP roles transcription of UVR8 and factors COP1 HY5 appear (elongated to be hypocotyl similar, suggesting 5) and HYH a very early(HY5 evolution homolog) of UV-B [17]. In acclimation Chlamydomonas in photosynthetic, the roles of UVR8 organisms and COP1 [12 appear]. to be similar, suggesting Acclimationa very early evolution is triggered of UV in-B conditions acclimation ofin moderatephotosynthetic stress organisms that do not[12]. kill cells. While in the face of harsherAcclimation stresses, Chlamydomonas is triggered in conditionswill be of able moderate to enable stress a that range do ofnot alternate kill cells. While strategies in the involving face of harsher stresses, Chlamydomonas will be able to enable a range of alternate strategies involving interaction between multiple cells and/or programmed cell death (Figure1). interaction between multiple cells and/or programmed cell death (Figure 1). FigureFigure 1. The 1. The strategies strategies used used by byChlamydomonas Chlamydomonas to survive survive increasing increasing stress stress intensities. intensities. Under Under optimal optimal conditionsconditionsChlamydomonas Chlamydomonascan can grow grow normally normally (green(green cell); cell); under under moderate moderate stress stress conditions conditions (light (light green cell), several acclimation processes can be triggered to allow the cells to better adapt and resist green cell), several acclimation processes can be triggered to allow the cells to better adapt and resist the occurrence of any additional stress of similar or greater magnitude. Under more intense stress the occurrence of any additional stress of similar or greater magnitude. Under more intense stress conditions (orange cell), cells can form multicellular structures such as palmelloids or aggregates that conditionscan dissociate (orange when cell), environmental cells can form conditions multicellular improve. structures Under very such harsh as palmelloids stress conditions or aggregates (red cell), that can dissociate when environmental conditions improve. Cells 2019, 8, 1307 3 of 16 Under very harsh stress conditions (red cell), the most exposed cells will self-destruct and release in the medium, molecules that will allow other cells to survive, to avoid the disappearance of the entire population. In the case of a stress of an intensity such that the cell cannot overcome (skull), the cell is physically destroyed by its environment through necrosis. 2.2. Protection by Degradation There are two main degradative pathways to recycle cellular components in eukaryotic cells: the ubiquitin-proteasome system
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