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Reorganisation of Complex Ciliary Flows Around Regenerating Stentor

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Reorganisation of Complex Ciliary Flows Around Regenerating Stentor bioRxiv preprint doi: https://doi.org/10.1101/681908; this version posted June 26, 2019. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity.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-NC 4.0 International license. 1 Reorganisation of complex ciliary flows around 2 regenerating Stentor coeruleus 1,8 3 Kirsty Y. Wan* , Sylvia K. Hürlimann2,8, Aidan M. Fenix4,5,8, 4 Rebecca M. McGillivary3,8, Tatyana Makushok3,8, Evan Burns6,9, 5 Janet Y. Sheung7,9, Wallace F. Marshall*3,8 6 1. Living Systems Institute, University of Exeter, Stocker Road, Exeter, UK 7 2. Department of Molecular and Cellular Biology, Harvard University, Cambridge, MA, USA 8 3. Department of Biochemistry and Biophysics, UCSF, San Francisco, CA, USA 9 4. Department of Pathology, University of Washington, WA, USA 10 5. Center for Cardiovascular Biology, University of Washington, WA, USA 11 6. Department of Biology, Vassar College, NY, USA 12 7. Department of Physics and Astronomy, Vassar College, NY, USA 13 8. Marine Biological Laboratory, Physiology Course, Woods Hole, MA, USA 14 9. Marine Biological Laboratory, Whitman Center, Woods Hole, MA, USA 15 16 Keywords: Cilia coordination, metachronal waves, regeneration, development, ciliary flows, Stentor 17 18 19 Summary 20 21 The phenomenon of ciliary coordination has garnered increasing attention in recent decades, with multiple 22 theories accounting for its emergence in different contexts. The heterotrich ciliate Stentor coeruleus is a 23 unicellular organism which boasts a number of features which present unrivalled opportunities for 24 biophysical studies of cilia coordination. With their cerulean colour and distinctive morphology, these large 25 protists possess a characteristic differentiation between cortical rows of short body cilia used for swimming, 26 and an anterior ring structure of fused oral cilia forming a membranellar band. The oral cilia beat 27 metachronously to produce strong feeding currents. In addition to this complex body plan, Stentor have 28 remarkable regenerative capabilities. Minute fragments of single cells can over the period of hours or days, 29 regenerate independently into new, proportional individuals. Certain environmental perturbations elicit a 30 unique programmed response known as oral regeneration wherein only the membranellar band is shed and 31 a new, ciliated oral primordium formed on the side of the body. Here, we target oral regeneration induced by 32 sucrose-shock to reveal the complex interplay between ciliary restructuring and hydrodynamics in Stentor, 33 which accompanies the complete developmental sequence from band formation, elongation, curling, and 34 migration toward the cell anterior. 35 36 “When the anterior part is open, one may perceive about its Edges a very lively Motion; and when the Polyps 37 presents itself in a certain manner, it discovers, on either side of these edges of its anterior part, somewhat 38 very much resembling the wheels of a little Mill, that move with great velocity.” 39 40 A. Trembley F.R.S describing the membranellar band of Stentor, 41 Phil. Soc. Trans. Royal Society (London), 1744. 42 1. Introduction 43 1.1. Stentor - the trumpet animalcule 44 The first recorded account of these fascinating funnel-shaped creatures was made by Abraham Trembley F.R.S, 45 who in a letter to the president of the Royal Society [1], wrote “I have herewith the honour of transmitting to 46 you the particulars of several observations I have made, during the course of the last summer, upon some 47 species of very minute Water-Animals…” [2]. (In fact, at 1the time Trembley had misidentified these organisms *Authors for correspondence ([email protected], [email protected]) bioRxiv preprint doi: https://doi.org/10.1101/681908; this version posted June 26, 2019. 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-NC 4.0 International license. 1 as Hydra.) These unicellular ciliates, which are easily visible to the naked eye, are named Stentor for their 2 trumpet-like morphology, in honour of a loud-voiced Greek hero who fought in the Trojan War. Stentor are 3 widely-occurring in both freshwater and marine habitats, exhibiting both free-swimming and sedentary 4 characteristics depending on environmental circumstance. Individual cells undergo dynamic and extensive 5 shape changes due to a highly-contractile cortical structure, assuming a pear or tear-drop shape when free- 6 swimming, contracting into a ball when disturbed, or else extending up 1mm in a rest state in which cells 7 become attached to substrates via a posterior holdfast (Figure 1a). In the latter state, a large number of ciliated 8 feeding organelles are visible at the anterior end of the organism, which stir the fluid collectively to produce 9 strong feeding currents, drawing food and other particulates towards the mouth of the organism. Not only is 10 the oral apparatus the site of a remarkable degree of ciliary coordination and highly-coupled fluid-structure 11 interactions, it is the most differentiated cortical landmark of a Stentor, which can also be regenerated in 12 response to injury or damage. The present study solicits this dramatic regenerative capability to investigate 13 ciliary organisation and coordination - which remains an open and confounding problem in ciliary biology. 14 Here, state-of-the-art imaging and flow field tracking is combined for the first time, to explore the extreme 15 restructuring of cilia and extracellular flows during Stentor oral regeneration. 16 While diverse species of Stentor exist, we focus exclusively on S. coeruleus Ehrenberg 1830 -- a widely 17 distributed species, notable for their striking cerulean pigmentation. S. coeruleus, also called the Blue Stentor [2, 18 3], was favoured historically for cytological studies due to its large size and moniliform macronucleus [4], and 19 has been the subject of recent genomic studies [5]. The conical surface of the organism bears longitudinal 20 stripes of distinctive colouration 21 extending from the anterior all the 22 way down to the tapered holdfast: 23 cortical rows of constant width, 24 alternate with pigmented stripes of 25 graded width – thereby breaking 26 the patterning symmetry (Figure 27 1b). The pigmented bands increase 28 in width from left to right around 29 the cell, culminating in a special 30 region called the locus of stripe 31 contrast (LSC) or “ramifying zone”. 32 This region demarcates the location 33 where the new oral primordium 34 and a new field of basal bodies will 35 form. 36 The body cilia are inserted 37 in rows along the clear stripes all 38 over the body; the anterior body 39 cilia are somewhat shorter than 40 those at the posterior [4]. 41 Contractile fibres called myonemes 42 subtend each row of body cilia, and 43 are involved in whole-body 44 contractions. The broad anterior 45 end of the organism is encircled by 46 an adoral zone of external cilia that 47 are fused into rows of transverse 48 plates termed membranelles (sensu 49 Sterki 1878). In SEM studies, Figure 1a) Schematic of a single Stentor cell with key features highlighted. Inset - 50 Randall and Jackson showed [6] ultrastructure of membranellar band [6] showing rows of oral cilia arranged in 51 that these adoral structures were parallel stacks (each approximately 7.5µm x1.5µm); b) confocal immunofluorescence 52 not individual large cilia but rather images showing the structure and organisation of the membranellar band (M), cortical 53 two or three rows of tightly-packed striation patterns (notice the sharp change in width at the locus of stripe contrast: 54 cilia (20-25 cilia per row), so that LSC), and associated rows of short body cilia, c) top view of the frontal field and gullet region (G). [Scalebars = 10 µm.] 55 each membranelle maintains 56 functional unity as an intercalated ciliary sheath (Figure 1a, inset). The entire membranellar band, also known 57 as the peristome, contains around 250 such stacked membranelles; one end terminates freely, while the other 58 end spirals into a funnel-shaped invagination or gullet (Figure 1c). The region enclosed by the membranellar 59 band is the frontal field, which is distinguished by a change in stripe orientation – the frontal field stripes are 60 also narrower since they originated as ventral stripes that have been shifted forward over the course of oral 61 primordium formation (see section 2), together with the new stripes which will go on to develop in this zone. 62 bioRxiv preprint doi: https://doi.org/10.1101/681908; this version posted June 26, 2019. 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-NC 4.0 International license. 1 1.2. Regenerative prowess of Stentor 2 Regeneration of ciliated structures provides a unique way of probing the emergence and reorganisation of 3 ciliary interactions over developmental timescales. A hallmark of life is its ability to repair, heal wounds, or 4 replenish lost or damaged cellular structures [7, 8]. Single cells are of special interest, for regeneration must 5 necessarily take place entirely within the same cell. One classic example is flagellar regeneration in the 6 biflagellate alga Chlamydomonas, where amputated flagella can be regrown to full length in about 1.5 hours [9, 7 10], whereupon biflagellar coordination also recovers [11, 12]. Early researchers demonstrated the versatility 8 of Stentor as a model system for studies of regeneration, made possible by their large size and manoeuvrability, 9 as well as remarkable regenerative capabilities [13, 14].
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