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The Wall-Less Bacterium Spiroplasma Poulsonii Builds a Polymeric

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The Wall-Less Bacterium Spiroplasma Poulsonii Builds a Polymeric bioRxiv preprint doi: https://doi.org/10.1101/2021.06.08.447548; this version posted June 8, 2021. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-ND 4.0 International license. 1 The wall-less bacterium Spiroplasma poulsonii builds a polymeric 2 cytoskeleton composed of interacting MreB isoforms 3 Florent Masson1*, Xavier Pierrat1,2, Bruno Lemaitre1, Alexandre Persat1,2* 4 5 1Global Health Institute, School of Life Sciences, École Polytechnique Fédérale de Lausanne (EPFL), 6 Lausanne, Switzerland 7 2Institute of Bioengineering, School of Life Sciences, École Polytechnique Fédérale de Lausanne 8 (EPFL), Lausanne, Switzerland 9 10 *Corresponding author: 11 Phone number: +41 21 693 12 51 12 Email address: [email protected] ; [email protected] 13 14 ORCID numbers: 15 FM: 0000-0002-5828-2616 16 XP: 0000-0002-3522-2514 17 BL: 0000-0001-7970-1667 18 AP: 0000-0001-8426-8255 19 20 Running title: MreB isoforms of Spiroplasma 21 22 Keywords: MreB, cytoskeleton, Spiroplasma, Mollicutes 23 24 Classification: Biological sciences, Microbiology. 25 26 This PDF file includes: 27 Main Text 28 Figures 1 to 4 bioRxiv preprint doi: https://doi.org/10.1101/2021.06.08.447548; this version posted June 8, 2021. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-ND 4.0 International license. 29 Abstract 30 A rigid cell wall defines the morphology of most bacteria. MreB, a bacterial 31 homologue of actin, plays a major role in coordinating cell wall biogenesis and 32 defining a cell’s shape. In contrast with most bacteria, the Mollicutes family is devoid 33 of cell wall. As a consequence, many Mollicutes have undefined morphologies. 34 Spiroplasma species are an exception as they robustly grow with a characteristic 35 helical shape, but how they maintain their morphology remains unclear. Paradoxal to 36 their lack of cell wall, the genome of Spiroplasma contains five homologues of MreB 37 (SpMreBs). Since MreB is a homolog of actin and that short MreB filaments 38 participate in its function, we hypothesize that SpMreBs form a polymeric 39 cytoskeleton. Here, we investigate the function of SpMreB in forming a polymeric 40 cytoskeleton by focusing on the Drosophila endosymbiont Spiroplasma poulsonii. We 41 found that in vivo, Spiroplasma maintain a high concentration of all five MreB 42 isoforms. By leveraging a heterologous expression system that bypasses the poor 43 genetic tractability of Spiroplasma, we found that strong intracellular levels of SpMreb 44 systematically produced polymeric filaments of various morphologies. Using co- 45 immunoprecipitation and co-expression of fluorescent fusions, we characterized an 46 interaction network between isoforms that regulate the filaments formation. Our 47 results point to a sub-functionalization of each isoform which, when all combined in 48 vivo, form a complex inner polymeric network that shapes the cell in a wall- 49 independent manner. Our work therefore supports the hypothesis where MreB 50 mechanically supports the cell membrane, thus forming a cytoskeleton. 51 52 53 bioRxiv preprint doi: https://doi.org/10.1101/2021.06.08.447548; this version posted June 8, 2021. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-ND 4.0 International license. 54 Significance statement 55 Bacteria shape is determined by their cell wall. The actin homologue MreB 56 essentially determines shape by organizing cell wall synthesis at the subcellular 57 level. Despite their lack of cell wall, Spiroplasma robustly grow into long helical 58 bacteria. Surprisingly, its genome retains five copies of mreB while it lost genes 59 encoding canonical MreB interactors. We sought to delineate the exact function of 60 Spiroplasma MreBs (SpMreBs). We leveraged in vivo data along with functional 61 studies to systematically investigate MreB polymerization behavior. We uncovered 62 that SpMreBs build into filaments, which structure it determined by a complex 63 interaction network between isoforms. Our results support the hypothesis that MreB 64 can mechanically support the membrane of Spiroplasma, hence acting as a load- 65 bearing cytoskeletal protein. 66 67 1 bioRxiv preprint doi: https://doi.org/10.1101/2021.06.08.447548; this version posted June 8, 2021. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-ND 4.0 International license. 68 69 Introduction 70 Bacteria grow into an astonishing variety of shapes including spheres, straight 71 and curved rods, disks, trapezoids, helices and even stars (1). The stability of these 72 morphologies within each species suggests that they confer important fitness 73 advantages in the natural ecological niches of these microbes (2). Bacteria typically 74 maintain their morphologies by virtue of their rigid cell wall (3). Local constraining of 75 cell wall peptidoglycan patterning by short MreB polymers provides a cell with its 76 shapes (4). As a consequence, degrading the bacterial cell wall is sufficient to relax 77 its shape into a spherical membrane (5, 6). In contrast, most mamalian cells are 78 plastic and actively control their shapes by virtue of a dynamic actin cytoskeleton (7). 79 All but one bacterial family (Mollicutes) synthesize a peptidoglycan cell wall. 80 The cell envelope of Mollicutes is essentially a lipid bilayer. Mollicutes underwent a 81 genome reduction, including loss of cell wall synthesis genes, by regressive evolution 82 upon their adaptation to a strict host-associated lifestyle (8, 9). As one could expect 83 from their lack of cell wall, the class encompasses genera such as Mycoplasma and 84 Phytoplasma with no distinctive cell shape, adapting their morphology to the 85 constraints of their close environment (10). Spiroplasma makes exception as this 86 genus is uniformly composed of long, helical bacterial species (11) (Figure 1A and 87 Supplemental movie 1). Furthermore, Spiroplasma cells actively deform their body to 88 propel themselves in high viscosity fluid environments (12, 13). How does 89 Spiroplasma maintain and actively controls its morphology? No external rigid 90 structure has been identified in these bacteria. We therefore hypothesize that, by 91 analogy with eukaryotes, an internal cytoskeleton maintains Spiroplasma membrane 92 morphology. 2 bioRxiv preprint doi: https://doi.org/10.1101/2021.06.08.447548; this version posted June 8, 2021. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-ND 4.0 International license. 93 Early electron cryotomograms of Spiroplasma have revealed intracellular 94 filament that may function as a membrane-associated cytoskeleton (14). One 95 candidate protein called Fibril (Fib), whose polymerization forms an internal ribbon 96 spanning the entire length of the bacterium, may provide structural support for the 97 membrane (12, 14–18). Therefore, Fib was initially thought to be necessary and 98 sufficient to maintain the helical shape of Spiroplasma. Yet, the serendipitous 99 isolation of a non-helical Spiroplasma variant still harboring fibrils indicates that Fib is 100 not sufficient to maintain helical shape (19). A proteomic analysis of purified ribbons 101 confirmed the massive presence of Fib, but also revealed the presence of MreB, a 102 bacterial homologue of the eukaryotic actin (17, 20, 21), indicating it could play a role 103 in maintining Spiroplasma’s helical shape. 104 MreB plays an essential function in determining the shape of almost all non- 105 spherical bacteria (4, 22). MreB polymerizes in an ATP-dependent fashion to form 106 anti-parallel double filaments that interact with the cytoplasmic tail of the 107 transmembrane protein RodZ (23–25). The periplasmic part of RodZ then positions 108 the cell wall synthesis machinery, thus linking the cell wall expansion sites (hence 109 cell elongation) to the MreB subcellular localization (26). Early studies indicated that 110 MreB forms filaments spanning the cell length (27, 28), crystallizing a hypothesis 111 wherein MreB is a cytoskeletal protein, providing mechanical support to the cell 112 envelope. Despite mechanical characterization that was consistent with this 113 hypothesis, subsequent experiments suspected these filaments were artifactual (23, 114 29, 30). Fluorescent protein fusions with improved functionality and limited artifacts 115 have helped demonstrate that MreB forms short polymers in close interaction with 116 the membrane. These filaments undergo a processive circumferential movement 117 around the cell as they coordinate the synthesis of new peptidoglycan (31–35). In E. 3 bioRxiv preprint doi: https://doi.org/10.1101/2021.06.08.447548; this version posted June 8, 2021. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-ND 4.0 International license. 118 coli, MreB forms ~100 nm-long filaments, too short to mechanically support the cell 119 envelope and constitute a cell wall. Helical filaments were however observed in other 120 fusions in B. subtilis and E. coli, reviving the helix model (35, 36). These conflicting 121 localization data could however be partially explained by variations between strains 122 or observation protocols (35). In summary, MreB polymers maintain cell shape by 123 patterning the cell wall, but not by directly bearing load as would be expected for a 124 cytoskeleton.
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