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Developmental Stage Influences Chromosome Segregation Patterns and Arrangement in the Extremely Polyploid, Giant Bacterium Epulopiscium Sp

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Developmental Stage Influences Chromosome Segregation Patterns and Arrangement in the Extremely Polyploid, Giant Bacterium Epulopiscium Sp SUNY Geneseo KnightScholar Biology Faculty/Staff Works Department of Biology 2018 Developmental stage influences chromosome segregation patterns and arrangement in the extremely polyploid, giant bacterium Epulopiscium sp. type B Elizabeth Hutchison SUNY Geneseo, [email protected] Follow this and additional works at: https://knightscholar.geneseo.edu/biology Part of the Bacteriology Commons Recommended Citation Hutchison, E., Yager, N. A., Taw, M. N., Taylor, M., Arroyo, F., Sannino, D. R., & Angert, E. R. (2018). Developmental stage influences chromosome segregation patterns and arrangement in the extremely polyploid, giant bacterium Epulopiscium sp. type B. Molecular Microbiology, 107(1), 68–80. This Article is brought to you for free and open access by the Department of Biology at KnightScholar. It has been accepted for inclusion in Biology Faculty/Staff Works by an authorized administrator of KnightScholar. For more information, please contact [email protected]. Molecular Microbiology (2018) 107(1), 68–80 ᭿ doi:10.1111/mmi.13860 First published online 23 November 2017 Developmental stage influences chromosome segregation patterns and arrangement in the extremely polyploid, giant bacterium Epulopiscium sp. type B Elizabeth Hutchison,1,2 Nicholas A. Yager,1 Introduction May N. Taw,2 Matthew Taylor,1 Francine Arroyo,2 David R. Sannino2 and Esther R. Angert 2* The bacterial chromosome is highly organized yet 1Department of Biology, SUNY Geneseo, Geneseo, dynamic, as its position and conformation change NY, USA. throughout the cell cycle (Toro and Shapiro, 2010; 2Department of Microbiology, Cornell University, Graumann, 2014; Le and Laub, 2014). Given that bacte- Ithaca, NY, USA. rial chromosomes are typically 1–10 Mb circular macro- molecules, approximately 0.15–1.5 mm long, and housed in a volume generally 1–5 lm3 (Young, 2006), a Summary chromosome must be compacted > 1000-fold to fit inside the cell (Holmes and Cozzarelli, 2000; Jun and Few studies have described chromosomal dynamics Wright, 2010; Reyes-Lamothe et al., 2012; Wang et al., in bacterial cells with more than two complete chro- 2013). Bacteria regulate chromosome organization such mosome copies or described changes with respect that newly replicated chromosomes can be partitioned to development in polyploid cells. We examined the with high fidelity to daughter cells upon reproduction. arrangement of chromosomal loci in the very large, The process has been studied in many model systems, highly polyploid, uncultivated intestinal symbiont including Caulobacter crescentus and Escherichia coli Epulopiscium sp. type B using fluorescent in situ (Toro and Shapiro, 2010; Wang et al., 2013). It also has hybridization. We found that in new offspring, been investigated during the development of specialized chromosome replication origins (oriCs) are arranged dormant cells such as endospores in Bacillus subtilis in a three-dimensional array throughout the cyto- (Webb et al., 1997), myxospores in Myxococcus xanthus plasm. As development progresses, most oriCs (Tzeng and Singer, 2005) and spores in Streptomyces become peripherally located. Siblings within a (Jakimowicz and van Wezel, 2012). mother cell have similar numbers of oriCs. When For many rod-shaped bacteria, chromosomes are organ- chromosome orientation was assessed in situ by ized longitudinally in the cell, with oriC (08) and ter (1808) labeling two chromosomal regions, no specific pat- regions at opposite cell poles (or subpolar regions) (Mohl tern was detected. The Epulopiscium genome codes for many of the conserved positional guide proteins and Gober, 1997; Webb et al., 1997; Jensen and Shapiro, used for chromosome segregation in bacteria. Based 1999; Maloney et al., 2009; Donovan et al., 2010; Harms on this study, we present a model that conserved et al., 2013; Vallet-Gely and Boccard, 2013; David et al., chromosomal maintenance proteins, combined with 2014). Chromosome arrangement in a cell can vary during entropic demixing, provide the forces necessary for the life cycle of a bacterium, or change during different distributing oriCs. Without the positional regulation growth conditions (Wang and Rudner, 2014). In slow- afforded by radial confinement, chromosomes are growing E. coli cells, the oriC and ter regions are located pri- more randomly oriented in Epulopiscium than in marily at the midcell, with the ter region more broadly dis- most small rod-shaped cells. Furthermore, we sug- tributed; with the left and right chromosome arms extending gest that the random orientation of individual chro- to either side, these chromosomes are in a transverse mosomes in large polyploid cells would not hamper arrangement (Nielsen et al., 2006; Wang et al., 2006; Toro reproductive success as it would in smaller cells with and Shapiro, 2010). Fast-growing E. coli adopt a more lon- more limited genomic resources. gitudinal orientation, emphasizing the adaptable nature of chromosome organization (Youngren et al., 2014). Likewise, Accepted 6 October, 2017. *For correspondence. E-mail in B. subtilis cells, the orientation of chromosomes alter- [email protected]; Tel. (11) 607 254 4778; Fax (11) 607 255 3904. nates between a longitudinal ori-ter pattern and a more VC 2017 John Wiley & Sons Ltd Chromosome dynamics in polyploid Epulopiscium sp. type B 69 transient transverse organization at different points in the indicate that Epulopiscium harbors tens of thousands of cell cycle (Wang et al., 2014). copies of its genome (Mendell et al., 2008). Genome copy A fine resolution study in C. crescentus examined 112 number scales with cell volume in Epulopiscium sp. type B sites around the entire chromosome and found that the and polyploidy appears to be key in allowing these giant physical location of a chromosomal locus within the cells to overcome diffusion-limited constraints on size. cell corresponded with its position on the chromosome How these cells manage their genomic resources has not (Viollier et al., 2004). A similar relationship has been been characterized. observed in B. subtilis, E. coli and V. cholerae (Teleman Epulopiscium sp. type B represents a diverse group of et al., 1998; Niki et al., 2000; Vallet-Gely and Boccard, surgeonfish intestinal symbionts called ‘epulos’, which vary 2013; David et al., 2014). This pattern does not entirely in size and reproductive mode (Clements et al., 1989; hold true for P. aeruginosa, where the chromosome Angert et al., 1993). Some epulos only reproduce via pro- appears to be organized into large regions, centered duction of internal offspring cells, others use multiple endo- around oriC and dif, and distant loci within one of these spore formation, and some can undergo binary fission or a nearly megabase-sized domains often appear to coloc- combination of binary fission and sporulation (Angert, alize (Vallet-Gely and Boccard, 2013). 2005). Early stages of development of intracellular off- Most of the work on chromosome organization has spring in epulos are similar to forespore formation in B. centered on bacteria that typically have one chromo- subtilis (Miller et al., 2011, 2012). While still contained in some per cell (or two after replication), are approxi- their mother cell, Epulopiscium sp. type B daughter cells mately rod shaped and reproduce via binary fission. begin a reproductive cycle by polar division and engulfment However, many bacteria have diverse cell and reproduc- of polar offspring cells (granddaughter cells) (Fig. 1). After tive morphologies and harbor greater numbers of engulfment, the newest generation of offspring grows completely replicated chromosomes (Hansen, 1978; within their mother cell. Throughout development, DNA in Minton, 1994; Jose Lopez-Sanchez et al., 2008; Mendell Epulopiscium sp. type B exhibits stage-specific patterns of et al., 2008; Michelsen et al., 2010; Ohtani et al., 2010; distribution (Angert and Clements, 2004). Griese et al., 2011; Pecoraro et al., 2011; Angert, Although epulos have not been cultured yet, these are 2012). Previous work on chromosome organization of attractive systems in which to address questions about polyploid bacteria has focused on cyanobacteria. Syne- chromosome organization in polyploid bacteria with diverse chocystis sp. PCC 6803 cells can contain tens to hun- cellular morphologies. In this study, we used fluorescence dreds of chromosome copies (Griese et al., 2011), and in situ hybridization (FISH) to locate individual chromo- it has been reported that they do not always distribute somal loci within cells at difference stages of their develop- DNA equally to daughter cells (Schneider et al., 2007). mental cycle and to begin to assess the organization of A study using fluorescently tagged chromosomes multiple chromosomes within large, highly polyploid revealed that Synechococcus elongatus PCC 7942 evenly spaces its 2–10 chromosome copies in a tandem array along the long axis of the cell (Jain et al., 2012). Another study showed that while S. elongatus chromo- somes were linearly organized in most cells, some cells had a random distribution (Chen et al., 2012). With so few studies, there is still much to be revealed about how diverse species of polyploid bacteria organize their genomic resources, and whether or not they require novel mechanisms for chromosome organization. The most extreme example of bacterial polyploidy known to date is Epulopiscium sp. type B, a member of the Fig. 1. The life cycle of Epulopiscium sp. type B. Firmicutes and an intestinal symbiont of an omnivorous In this illustration,
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