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The Social Amoeba Polysphondylium Pallidum Loses Encystation University of Dundee The Social Amoeba Polysphondylium pallidum Loses Encystation and Sporulation, but Can Still Erect Fruiting Bodies in the Absence of Cellulose Du, Qingyou; Schaap, Pauline Published in: Protist DOI: 10.1016/j.protis.2014.07.003 Publication date: 2014 Licence: CC BY Document Version Publisher's PDF, also known as Version of record Link to publication in Discovery Research Portal Citation for published version (APA): Du, Q., & Schaap, P. (2014). The Social Amoeba Polysphondylium pallidum Loses Encystation and Sporulation, but Can Still Erect Fruiting Bodies in the Absence of Cellulose. Protist, 165(5), 569-579. https://doi.org/10.1016/j.protis.2014.07.003 General rights Copyright and moral rights for the publications made accessible in Discovery Research Portal are retained by the authors and/or other copyright owners and it is a condition of accessing publications that users recognise and abide by the legal requirements associated with these rights. • Users may download and print one copy of any publication from Discovery Research Portal for the purpose of private study or research. • You may not further distribute the material or use it for any profit-making activity or commercial gain. • You may freely distribute the URL identifying the publication in the public portal. Take down policy If you believe that this document breaches copyright please contact us providing details, and we will remove access to the work immediately and investigate your claim. Download date: 10. Oct. 2021 Protist, Vol. 165, 569–579, September 2014 http://www.elsevier.de/protis Published online date 14 July 2014 ORIGINAL PAPER The Social Amoeba Polysphondylium pallidum Loses Encystation and Sporulation, but Can Still Erect Fruiting Bodies in the Absence of Cellulose 1 Qingyou Du, and Pauline Schaap College of Life Sciences, University of Dundee, MSI/WTB/JBC complex, Dow Street, Dundee, DD15EH, UK Submitted May 20, 2014; Accepted July 8, 2014 Monitoring Editor: Michael Melkonian Amoebas and other freely moving protists differentiate into walled cysts when exposed to stress. As cysts, amoeba pathogens are resistant to biocides, preventing treatment and eradication. Lack of gene modification procedures has left the mechanisms of encystation largely unexplored. Genetically tractable Dictyostelium discoideum amoebas require cellulose synthase for formation of multicellular fructifications with cellulose-rich stalk and spore cells. Amoebas of its distant relative Polysphondylium pallidum (Ppal), can additionally encyst individually in response to stress. Ppal has two cellulose syn- thase genes, DcsA and DcsB, which we deleted individually and in combination. Dcsa- mutants formed fruiting bodies with normal stalks, but their spore and cyst walls lacked cellulose, which obliterated stress-resistance of spores and rendered cysts entirely non-viable. A dcsa-/dcsb- mutant made no walled spores, stalk cells or cysts, although simple fruiting structures were formed with a droplet of amoeboid cells resting on an sheathed column of decaying cells. DcsB is expressed in prestalk and stalk cells, while DcsA is additionally expressed in spores and cysts. We conclude that cellulose is essential for encystation and that cellulose synthase may be a suitable target for drugs to prevent encystation and render amoeba pathogens susceptible to conventional antibiotics. © 2014 The Authors. Published by Elsevier GmbH. This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/3.0/). Key words: Encystation; Amoebozoa; Acanthamoeba keratitis; cellulose synthase; cell wall biosynthesis; Polysphondylium pallidum. Introduction in the case of pathogenic protozoa, resist the chal- lenges of antibiotic treatment and immune clear- Amoebas and many other freely moving proto- ance. This resilience is due to the fact that the cells zoa differentiate into immobile dormant cysts when are metabolically inactive and surrounded by an exposed to nutrient depletion or other forms of envi- impermeable cell wall. In fungi, the polysaccharide ronmental stress. As cysts, the organisms can sur- chitin is the main structural component of the cell vive adverse conditions from months to years, and, wall (Free 2013), but in chromalveolate algae and oomycetes, green algae, and amoebozoa, such 1 as Dictyostelium discoideum and Acanthamoeba Corresponding author; fax +44 1382 345386 e-mail [email protected] (P. Schaap). castellani, the structural component is cellulose http://dx.doi.org/10.1016/j.protis.2014.07.003 1434-4610/© 2014 The Authors. Published by Elsevier GmbH. This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/3.0/). 570 Q. Du and P. Schaap (Blanton et al. 2000; Dudley et al. 2009; Fugelstad roles of cellulose synthase genes in encystation. et al. 2009; Michel et al. 2010; Roberts et al. 2002). The differentiation of spores, stalk cells and cysts In the social amoeba Dictyostelium discoideum in Dictyostelia as well as encystation in Acan- (Ddis), a single cellulose synthase gene is essential thamoeba all require cyclic AMP acting on PKA (Du for the construction of multicellular fruiting bod- et al. 2014; Kawabe et al. 2009; Reymond et al. ies, by synthesizing a cellulose stalk tube and the 1995; Ritchie et al. 2008), which led to the work- cellulose-rich walls of individual stalk cells and ing hypothesis that walled spore and stalk cells are spores (Blanton et al. 2000). Many Dictyostelium evolutionary derived from cysts. Ppal can differen- species, such as the genetic model Polysphon- tiate into all three cell types, allowing us to retrace dylium pallidum (Ppal), can alternatively encyst as how complexity in cell wall biosynthesis emerged. single cells. Ppal also constructs architecturally A pilot study revealed the presence of two cel- more complex fruiting structures than D.discoideum lulose synthase genes in Ppal. In this work, we with multiple regular whorls of side branches. studied the expression patterns of both genes For synthesis of the stalk tube, cellulose microfib- and abrogated the genes individually and together. rils are deposited at the exterior face of the plasma Inspection of the null mutant phenotypes show both membrane of prestalk cells by single linear arrays unique and overlapping roles for the cellulose syn- of membrane-spanning cellulose synthases. While thases and an absolute requirement of cellulose prestalk cells are maturing into stalk cells, the long synthesis for encystation and sporulation. linear arrays rearrange into multiple parallel rows for synthesis of the thicker fibrils of the stalk cell wall (Grimson et al. 1996). The spore wall consists of Results a cellulose layer sandwiched between two protein- rich layers. Spore coat proteins are presynthesized Conservation of Cellulose Synthase in Golgi-derived vesicles, which synchronously fuse Genes in Dictyostelia with the plasma membrane at the onset of spore The D. discoideum (Ddis) genome contains a sin- maturation. Cellulose deposition occurs somewhat gle cellulose synthase gene, DcsA, and we first later, starting at one pole of the spore and travel- investigated whether DcsA is conserved through- ling towards the other pole. The spore wall cellulose out the dictyostelid phylogeny. The genomes of is essential for proper deposition of the two pro- species representing the four major groups of teinaceous layers of the spore coat (Zhang et al. Dictyostelia and the solitary amoebozoan Acan- 2001). Cellulose also makes up 28% of the Ppal thamoeba castellani (Acas) (Clarke et al. 2013; cyst wall (Toama and Raper 1967), but cellulose Eichinger et al. 2005; Heidel et al. 2011; Sucgang synthases do not appear to form linear arrays in et al. 2011) as well as all non-redundant sequences the plasmamembrane of encysting cells (Erdos and in Genbank were queried with the Ddis DcsA pro- Hohl 1980). tein sequence, yielding single orthologues of DcsA Acanthamoeba castellani is an opportunistic in groups 1, 3 and 4 of Dictyostelia and an addi- pathogen that causes vision-destroying kerati- tional gene, DcsB, in A. subglobosum (Asub) and tis and lethal encephalitis, with cysts preventing Ppal, which represent the two major clades of group effective treatment (Siddiqui et al. 2013). Cell 2. The dictyostelid cellulose synthase genes were wall biosynthesis is a major target for bacte- more similar to bacterial and oomycete cellulose rial and fungal antibiotics and herbicides (Bush synthases than to the Acas cellulose synthase. 2012; McCormack and Perry 2005; Wakabayashi and Böger 2002). Acanthamoeba encystation was Phenotype of a Ppal dcsa- Mutant shown to be reduced by 85% by 0.48 mM of the herbicide 2,6-dichlorobenzonitrile, which inhibits The group 2 species Ppal is the only encysting plant cellulose synthesis (Dudley et al. 2007), dictyostelid that is amenable to gene knockout pro- and to 50% by incubation with small interfer- cedures. To identify the respective roles of DcsA ing RNAs against the Acanthamoeba cellulose and DcsB in Ppal, we generated null mutants synthase (Aqeel et al. 2013). Although not fully in either gene by transformation with a floxed penetrant, these treatments show the potential neomycin cassette (Faix et al. 2004; Kawabe et al. importance of cellulose synthase for amoebozoan 2009) flanked by ∼1 kb fragments of the DcsA or encystation. No gene knock-out strategies are as DcsB coding regions. Clones carrying gene knock- yet available for Amoebozoa outside Dictyostelia. out (KOs) and random integration (RI)
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