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Stress Signalling in Acellular Slime Moulds and Its Detection by Conspecifics Léa Briard, Clément Gourjade, Christophe Bousquet, Audrey Dussutour

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Stress Signalling in Acellular Slime Moulds and Its Detection by Conspecifics Léa Briard, Clément Gourjade, Christophe Bousquet, Audrey Dussutour Stress signalling in acellular slime moulds and its detection by conspecifics Léa Briard, Clément Gourjade, Christophe Bousquet, Audrey Dussutour To cite this version: Léa Briard, Clément Gourjade, Christophe Bousquet, Audrey Dussutour. Stress signalling in acellular slime moulds and its detection by conspecifics. Philosophical Transactions of the Royal Society B: Biological Sciences, Royal Society, The, 2020, 375 (1802), pp.20190470. 10.1098/rstb.2019.0470. hal-02992843 HAL Id: hal-02992843 https://hal.archives-ouvertes.fr/hal-02992843 Submitted on 17 Nov 2020 HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. The documents may come from émanant des établissements d’enseignement et de teaching and research institutions in France or recherche français ou étrangers, des laboratoires abroad, or from public or private research centers. publics ou privés. Stress signalling in acellular slime moulds and its detection by conspecifics royalsocietypublishing.org/journal/rstb L. Briard, C. Goujarde, C. Bousquet and A. Dussutour Research Centre on Animal Cognition (CRCA), Centre for Integrative Biology (CBI), Toulouse University, CNRS, UPS, Toulouse 31062, France Research LB, 0000-0002-4769-1932; CB, 0000-0003-1650-8004; AD, 0000-0002-1377-3550 Cite this article: Briard L, Goujarde C, Unicellular organisms live in unpredictable environments. Therefore, they Bousquet C, Dussutour A. 2020 Stress need to continuously assess environmental conditions and respond appro- priately to survive and thrive. When subjected to rapid changes in their signalling in acellular slime moulds and its environment or to cellular damages, unicellular organisms such as bacteria detection by conspecifics. Phil. Trans. R. Soc. B exhibit strong physiological reactions called stress responses that can be 375: 20190470. sensed by conspecifics. The ability to detect and use stress-related cues http://dx.doi.org/10.1098/rstb.2019.0470 released by conspecifics to acquire information about the environment con- stitutes an adaptive survival response by prompting the organism to avoid potential dangers. Here, we investigate stress signalling and its detection by Accepted: 10 February 2020 conspecifics in a unicellular organism, Physarum polycephalum. Slime moulds were subjected to either biotic (i.e. nutritional) or abiotic (i.e. chemical One contribution of 22 to a theme issue ‘Signal and light) stressors or left undisturbed while they were exploring a homo- detection theory in recognition systems: from geneous environment. Then, we observed the responses of slime moulds evolving models to experimental tests’. facing a choice between cues released by stressed clone mates and cues released by undisturbed ones. We found that slime moulds actively avoided environments previously explored by stressed clone mates. These results Subject Areas: suggest that slime moulds, like bacteria or social amoeba, exhibit physiologi- behaviour, cognition cal responses to biotic and abiotic stresses that can be sensed by conspecifics. Our results establish slime moulds as a promising new model to investigate the use of social information in unicellular organisms. Keywords: This article is part of the theme issue ‘Signal detection theory in Physarum polycephalum, social information recognition systems: from evolving models to experimental tests’. use, caffeine, light, nutrient, decision-making Author for correspondence: L. Briard 1. Introduction e-mail: [email protected] Unicellular organisms live in unpredictable environments. They need to continu- ously monitor environmental parameters and adjust their behaviour in response to potentially life-threatening changes [1,2]. Unicellular organisms are capable of responding to a large range of stressors including extreme pH, drought, heat, osmotic challenge, oxidative stress, nutrient limitation and the presence of toxic molecules originating from their abiotic and biotic environment [3]. The specific mechanisms used to sense stressors and trigger adequate cellular responses have been extensively reviewed in bacteria [3]. These stress responses can be specific and specialized for a particular kind of stress or general and adapted to multiple stresses. Stress responses in single-cell organisms include the development of spores and competence, activation of motility, synthesis of antibiotics and enzymes, and changes in energy production systems (e.g. improving acquisition and use of growth-limiting nutrients). To respond appropriately to stressful changes in their immediate environment and/or seek optimal living conditions, single-celled organisms must be able to process many external cues simultaneously and integrate them to adjust their response [1,4]. These cues might be environmental, such as temperature change or nutrient scarcity, or can be derived from conspecifics in the form of secreted molecules [3,5,6]. Unicellular organisms are capable of sensing and processing Electronic supplementary material is available the metabolic activities of their conspecifics and use them to learn about the online at https://doi.org/10.6084/m9.figshare. current status of the population [7]. For instance, many unicellular organisms, c.4946079. including prokaryotes and eukaryotes, can obtain information about their © 2020 The Author(s) Published by the Royal Society. All rights reserved. surroundings using a process called quorum sensing [8–10]. sense nutritive cues such as amino acids [39–41], sugars 2 Quorum sensing involves the production, release and percep- [42,43], minerals [44], salts [45,46] and so on. They also respond royalsocietypublishing.org/journal/rstb tion of signalling molecules often referred as autoinducers to changes in oxygen, pH, osmolarity, temperature and light and is implicated in many group activities, including aggrega- [22]. Physarum polycephalum is capable of directing its move- tion, swarming, bioluminescence, biofilm formation, secretion ment towards cues that are favourable for growth and of virulence factors, sporulation, antibiotic production and survival such as nutrients [36] and away from cues that threa- extracellular digestion [9,11,12]. Quorum sensing is considered ten survival such as toxins [47] or light [48]. Vogel et al. [44] to be a means of assessing local population density and its demonstrated that slime moulds can sense and respond to physiological state [12–14]. It facilitates adaptation to environ- chemical cues released in the environment by conspecifics in mental stress as it improves access to nutrients, promotes a foraging context. In their experiment, they identified that defence against competitors and enhances cell differentiation slime moulds release calcium while foraging and that calcium to survive harsh environmental conditions [15]. For instance, is attractive to other slime moulds. in the social bacterium Myxococcus xanthus, the production of In the present study, we tested the hypotheses that: (i) slime a mixture of amino acids termed A-factor, an early extracellular moulds release chemical cues in the environment when facing Phil. Trans. R. Soc. B cell-density signal, increases under nutrient stress [3,16]. This various stressors, and (ii) these cues can be sensed and used way the bacteria can assess the physiological status of each adaptively by other slime moulds. To test our hypotheses, we other to properly coordinate their motion, aggregate and manipulated the physiological conditions of slime moulds sporulate to resist starvation [17]. Another similar example exploring an environment using biotic or abiotic stresses. can be found in the social amoeba Dictyostelium discoideum We then recorded the behavioural response of slime moulds also known as cellular slime moulds. These single-celled amoe- facing substrates explored by stressed or undisturbed clone 375 bae feed on bacteria and other microbes in the soil. When food mates. To date, to our knowledge, no studies have demon- : 20190470 becomes scarce, the starving amoebae secrete and respond to strated that slime moulds convey information regarding cAMP, an extracellular signalling molecule, causing them to stressful situations that can be sensed by conspecifics. Sensing aggregate, form a multicellular assemblage called ‘slug’, and clone mates’ stress would allow slime moulds to rapidly escape sporulate [18,19]. conditions that limit their growth by orienting their movement Yet, we know little about how chemical cues produced by towards a more favourable environment. conspecifics in response to stress influence the decision- making process in single-cell organisms. Can cells glean information from extracellular metabolites released by conspe- 2. Material and methods cifics to anticipate potential danger and move towards safer environments? In other words, are unicellular organisms able (a) Species and rearing conditions to extract information about the environment directly from the Acellular slime moulds live in shady, cool and humid organic sub- chemical cues released bystressed conspecificsto respond adap- strates where they feed on bacteria, yeasts and fungi [49]. Under tively in the absence of the eliciting stressor? In the present adverse conditions (i.e. decreased humidity and food availability), study, we attempt to answer this question using the acellular slime moulds can turn
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