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Understanding physiological adaptations of the model yeast Saccharomyces cerevisiae grown in reduced gravity conditions Authors: R. Willaert, Y. Kayacan, C. Yvanoff, M. Perez Gonzalez, S. Kasas, H. Sahli, G. Dietler and B. Devreese Publication Date: Jul. 2019
Abstract: Purpose of workOn Earth, fungi (yeast) are used since a long time as microbial factories to produce many compounds, including foods and drugs. However, spaceflight and reduced gravity conditions presents a novel environment for organisms that evolved under the selection pressures of gravity on Earth. Additionally, space radiation influences the evolution by introducing genetic mutations at a high rate. Cellular responses to the environment are mediated by phenotypic changes ultimately driven by alterations in gene expression. A better understanding of the adaptation of microbial cells to reduced gravity space conditions is needed. We studied the adaptation of the model eukaryote S. cerevisiae that form multicellular clumps by expressing flocculation proteins under adverse growth conditions and can protect cells from harsh environmental stresses. Approach The yeast cells were grown in liquid medium or on agar medium in specifically designed hardware suitable to perform experiments in the International Space Station. A systems biology approach was performed by performing transcriptomics and proteomics measurements.ResultsMicrogravity research (ISS) revealed that microgravity conditions are experienced as a stress condition by yeast cells. Yeast cultivation in liquid culture resulted in a reduced cell growth rate and glucose consumption (especially for a strong flocculent strain). Cells showed an increased number of random bud scars, and strain dependent differences in gene up- and downregulation were detected using DNA microarrays. Cultivation of different strains on semi-solid agar in microgravity also resulted in a reduced growth rate of the yeast colonies and a changed budding pattern. Strain dependent differences in gene up- and downregulation were also observed. Analyzing the proteome of the ?1278b and ?1278b ?flo11 strain indicated that there is a higher requirement for glucose in microgravity conditions. Additionally, it was observed that there is a decrease in abundancy of several ribosomal proteins and a proteasome component, an increased abundance of proteins in the pentose phosphate pathways and Krebs cycle, and a lower expression level of tropomyosin (a structural protein that is able to bind and stabilize actin cables and filaments, and direct polarized growth in the cell), which can be linked to the changed budding profile. Based on the obtained microgravity data, a new role of cell flocculation was demonstrated i.e., flocculation is linked to cell conjugation and mating, and survival chances consequently increase significantly by spore formation and by introduction of genetic variability. The role of Flo1p in mating was demonstrated by showing that mating efficiency is increased when cells flocculate and by differential transcriptome analysis of flocculating versus non-flocculating cells in a low-shear microgravity environment. The results show that a multicellular clump (floc) provides a uniquely organized multicellular ultrastructure that provides a suitable microenvironment to induce and perform cell conjugation and mating. Flocculation is thus of crucial importance for the enhanced chance of survival of Flo-expressing yeast cells under sustained stress conditions. The benefits of flocculation with respect to cell survival are manifold: flocculation gives the cells a way to escape from harsh conditions in the growth medium, a floc protects the inner cells from environmental stress, and cells in the middle of the floc could lyse and act as a source of new nutrients for the other cells. The new findings concerning the increased mating efficiency in a floc suggest an additional role of flocculation in survival. Mating results in an offspring with genetic variation. Additionally, diploid cells can undergo meiosis and sporulation and can package the haploid nuclei into spores to increase the survival rate, since spores are highly resistant to a variety of environmental stresses. Therefore, flocculating cells have a significantly higher chance for survival than non-flocculent cells.Significance Human space exploration is envisioning long-term spaceflight missions that go far beyond Low Earth Orbit (LEO). These missions and colonization of planets will only be successful if human health can be assured. Microbes were reported to grow faster or to become more virulent in microgravity conditions. Furthermore, parts of the human immune system are suppressed under these conditions. The knowledge of microbial behaviour as well as the evaluation of the effectiveness of antimicrobial drugs in reduced gravity conditions is indispensable to assure human’s resistance to illness during spaceflights. On the other hand, microorganisms such as baker’s yeast could be used to produce many compounds of interest and assure that the necessary resources are available. Therefore, many space biotechnology processes will have to be developed and optimised. The installation of a Lunar Research Station could help considerably in this endeavour.
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