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Motility in the colonial and multicellular Volvocales: structure, function, and evolution

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Summary

The colonial Volvocales are often said to be composed of Chlamydomonas-like cells, but there are substantial differences in motility and flagellar apparatus construction between the unicellular forms and the individual members of a colony or spheroid. These changes appear to be required for effective organismal motion and might possibly limit the rate at which new colonial forms evolve from unicellular ones. The flagellar-beat envelopes in colonial members are modified such that they beat in the same direction and in parallel planes with their effective strokes at right angles to the cellular anterior-posterior axis. These changes result from a series of developmental events of the flagellar apparatus of the colonial forms while the colony is still an embryo. Differences in the flagellar-apparatus structure in the members of the Goniaceae and Volvocaceae are not obviously correlated with the traditional placement of these algae in a simple volvocine lineage. Effective colonial motion clearly requires precise positioning and rotational orientation of the cells within the colony. Almost any arrangement where the cells are placed with rotational symmetry within the colony results in colonial progression with rotation. Such rotational symmetry is present from the time of embryogenesis. The mechanism that leads to organismal steering in behavioral responses (e.g., phototaxis) must likewise differ between colonial and unicellular forms. In at least some cases, this appears to result from changes in beat frequency in some parts of the spheroid, but changes in beat direction cannot be ruled out for all forms.

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References

  • Adair WS, Steinmetz SA, Mattson DM, Goodenough UW, Heuser JE (1987) Nucleated assembly ofChlamydomonas andVolvox cell walls. J Cell Biol 105: 2373–2382

    Google Scholar 

  • Aleyev MY (1992) Active metabolism of planktonic flagellates. Hydrobiol J 28: 62–68

    Google Scholar 

  • Bell G (1985) The origin and early evolution of germ cells as illustrated by the Volvocales. In: Halvorson HO, Monroy A (eds) The origin and evolution of sex. Alan R Liss, New York, pp 221–256

    Google Scholar 

  • Birchem R, Kochiert G (1979) Mitosis and cytokinesis in androgonidia ofVolvox carteri f.weismannia. Protoplasma 100: 1–12

    Google Scholar 

  • Brighton M, Clement P, Stickles S, Hoops HJ (1996) The mechanism for phototactic turning inVolvox carteri. J Phycol 31 Suppl: 8–9

    Google Scholar 

  • Brokaw CJ, Luck DJL (1983) Bending patterns ofChlamydomonas flagella I. Wild-type bending patterns. Cell Motil 3: 131–150

    Google Scholar 

  • Brooks AE (1966) The sexual cycle and outcrossing in the genusAstrephomene. J Protozool 13: 367–375

    Google Scholar 

  • Buchheim MA, Chapman RL (1991) Phylogeny of colonial green flagellates: a study of 18S and 26S rRNA sequence data. BioSystems 25: 85–100

    Google Scholar 

  • —, McAuley MA, Zimmer EA, Theriot EC, Chapman RL (1994) Multiple origins of colonial green flagellates from unicells: evidence from molecular and organismal characters. Mol Phylogenet Evol 3: 322–343

    Google Scholar 

  • Coggin SJ, Kochiert G (1986) Flagellar development and regeneration inVolvox carteri (Chlorophyta). J Phycol 22: 370–381

    Google Scholar 

  • Crawford DW (1992) Metabolic cost of motility in planktonic protists: theoretical considerations on size scaling and swimming speed. Microbial Ecol 24: 1–10

    Google Scholar 

  • Crow WB (1918) The classification of some colonial chlamydomonads. New Phytol 17: 151–159

    Google Scholar 

  • Deason TR, Darden WH Jr (1971) The male initial and mitosis inVolvox. In: Parker B, Brown RM (eds) Contributions in phycology. Allen Press, Lawrence, KS, pp 67–79

    Google Scholar 

  • Desnitski AG (1993) On the origins and early evolution of multicellularity. BioSystems 29: 129–132

    Google Scholar 

  • Droop MR (1956)Haematococcus pluvialis and its allies. I. The Sphaerellaceae. Rev Algol 2: 53–77

    Google Scholar 

  • Ettl H (1976) Die GattungChlamydomonas Ehrenburg. Nova Hedwigia 49: 1–1122

    Google Scholar 

  • Feinleib MEH (1985) Behavioral studies of free swimming photoresponsive organisms. In: Colombetti G, Song PS (eds) Sensory perception and transduction in aneural organisms. Plenum, New York, pp 119–146

    Google Scholar 

  • Floyd GL, Hoops HJ, Swanson JA (1980) Fine structure of the zoospore ofUlothrix belkae with emphasis on the flagellar apparatus. Protoplasma 104: 17–31

    Google Scholar 

  • Foster KW, Smyth RD (1980) Light antennas in phototactic algae. Microbiol Rev 44: 572–630

    Google Scholar 

  • Fritsch FE (1929) Evolutionary sequence and affinities among the Protophyta. Biol Rev 4: 103–151

    Google Scholar 

  • — (1935) The structure and reproduction of the algae, vol. 1. Cambridge University Press, Cambridge

    Google Scholar 

  • Gerisch G (1959) Die Zelldifferenzierung beiPleodorina californien Shaw und die Organisation der Phytomonadinenkolonien. Arch Protistenk 104: 292–358

    Google Scholar 

  • Goldstein ME (1964) Speciation and mating behavior inEudorina. J Protozool 11: 317–344

    Google Scholar 

  • Goodenough UW, Heuser JE (1988) Molecular organization of cell wall crystals fromChlamydomonas reinhardtii andVolvox carteri. J Cell Sci 90: 717–734

    Google Scholar 

  • —, Weiss RL (1978) Interrelationships between microtubules, a striated fiber, and the gametic mating structure ofChlamydomonas reinhardi. J Cell Biol 76: 430–438

    Google Scholar 

  • Greuel BT, Floyd GL (1985) Development of the flagellar apparatus and flagellar orientation in the colonial green algaeGonium pectorale (Volvocales). J Phycol 21: 358–371

    Google Scholar 

  • Hamilton BS, Nakamura K, Roncari DA (1992) Accumulation of starch inChlamydomonas reinhardtii flagellar mutants. Biochem Cell Biol 70: 255–258

    Google Scholar 

  • Hambright KD, Trebatoski RJ, Drenner RW (1986) Experimental study of the impacts of bluegill (Lepomis macrochirus) and largemouth bass (Micropterus salmoides) on pond community structure. Can J Fish Aquat Sci 43: 1171–1176

    Google Scholar 

  • Hand WG, Haupt W (1971) Flagellar activity of the colony members ofVolvox aureus Ehrb. during light stimulation. J Protozool 18: 361–364

    Google Scholar 

  • Heimann K, Reize IB, Melkonian M (1989) The flagellar developmental cycle in algae: flagellar transformation inCyanophora paradoxa (Glaucocystophyceae). Protoplasma 148: 106–110

    Google Scholar 

  • Holmes JA, Dutcher SK (1989) Cellular asymmetry inChlamydomonas reinhardtii. J Cell Sci 94: 273–285

    Google Scholar 

  • Hoops HJ (1984) Somatic cell flagellar apparatuses in two species ofVolvox (Chlorophyceae). J Phycol 20: 20–27

    Google Scholar 

  • — (1993) Flagellar, cellular and organismal polarity inVolvox carteri. J Cell Sci 104: 105–117

    Google Scholar 

  • —, Floyd GL (1982a) Mitosis, cytokinesis and colony formation in the colonial green algaeAstrephomene gubernaculifera. Br Phycol J 17: 297–310

    Google Scholar 

  • — — (1982b) Ultrastructure of the flagellar apparatus ofPyrobotrys (Chlorophyceae). J Phycol 18: 455–462

    Google Scholar 

  • — — (1982c) Ultrastructure and taxonomic position of the rare Volvocalean algaChlorcorona bohemica. J Phycol 18: 462–466

    Google Scholar 

  • — — (1983) Ultrastructure and development of the flagellar apparatus and flagellar motion in the colonial green algaeAstrephomene gubernaculifera. J Cell Sci 63: 21–41

    Google Scholar 

  • —, Witman GB (1983) Outer doublet heterogeneity reveals structural polarity related to beat direction inChlamydomonas flagella. J Cell Biol 97: 902–908

    Google Scholar 

  • —, Wright RL, Jarvik JW, Witman GB (1984) Flagellar waveform and rotational orientation in aChlamydomonas mutant lacking normal striated fibers. J Cell Biol 98: 818–824

    Google Scholar 

  • —, Long JJ, Hile ES (1994) Flagellar apparatus structure is similar but not identical inVolvulina steinii, Eudorina elegans andPleodorina illinoisensis (Chlorophyta): implications for the “volvocine evolutionary lineage”. J Phycol 30: 679–689

    Google Scholar 

  • —, Moran JP, Nordman EE (1995) The flagellar apparatus and evolutionary relationships in the genusVolvox: V. spermatosphaera, V. capensis, V. rousseletii andV. carteri f.weismannia. J Phycol 31 Suppl: 7

    Google Scholar 

  • Horst CJ, Witman GB (1993)Ptxl, a nonphototactic mutant ofChlamydomonas, lacks control of flagellar dominance. J Cell Biol 120: 733–741

    Google Scholar 

  • Huang B, Ramanis Z, Dutcher SK, Luck DJL (1982) Uniflagellar mutants ofChlamydomonas: evidence for the role of basal bodies in transmission of positional information. Cell 29: 745–753

    Google Scholar 

  • Huskey (1979) Mutants affecting vegetative cell orientation inVolvox carteri. Dev Biol 72: 236–243

    Google Scholar 

  • Huth K (1970) Bewegung und Orientierung beiVolvox aureus Ehrb. I. Mechanismus der phototaktischen Reaktion. Z Pflanzenphysiol 62: 436–450

    Google Scholar 

  • Johnson UG, Porter KR (1968) Fine structure of cell division inChlamydomonas reinhardi. J Cell Biol 38: 403–425

    Google Scholar 

  • Kamiya R, Hasegawa E (1987) Intrinsic difference in beat frequency between the two flagella ofChlamydomonas reinhardtii. J Exp Res 173: 299–304

    Google Scholar 

  • —, Witman GB (1984) Submicromolar levels of calcium control and balance of beating between the two flagella in demembranated models ofChlamydomonas. J Cell Biol 98: 97–107

    Google Scholar 

  • Lang NC (1963) Electron microscopy of Volvocaceae and Astrephomenaceae. Am J Bot 50: 280–300

    Google Scholar 

  • Larson A, Kirk MM, Kirk DL (1992) Molecular phylogeny of the volvocine flagellates. Mol Biol Evol 9: 85–105

    Google Scholar 

  • Lechtreck K-F, Reize IB, Melkonian M (1997) The cytoskeleton of the naked green flagellateSpermatozopsis similis (Chlorophyta): flagellar and basal body developmental cycle. J Phycol 33: 254–265

    Google Scholar 

  • Mast SO (1911) Light and the behavior of organisms. John Wiley, London

    Google Scholar 

  • — (1926) Reaction to light inVolvox, with special references to the process of orientations. Z Vergl Physiol 4: 637–658

    Google Scholar 

  • Matsuda Y (1988) TheChlamydomonas cell walls and their degrading enzymes. Jpn J Phycol (Sorui) 36: 246–264

    Google Scholar 

  • Melkonian M (1982) The functional analysis of the flagellar apparatus in green algae. In: Amos WB, Duckett JG (eds) Prokaryotic and eukaryotic flagella. Cambridge University Press, Cambridge, pp 589–606

    Google Scholar 

  • —, Reize IB, Preisig HR (1987) Maturation of a flagellum/basal body requires more than one cell cycle in algal flagellates: studies onNephroselmis olivacea (Prasinophyceae). In: Wiessner W, Robinson DG, Starr RC (eds) Algal development: molecular and cellular aspects. Springer, Berlin Heidelberg New York Tokyo, pp 102–113

    Google Scholar 

  • Mertens J, Munuswamy N, De Walsche C, Dumont HJ (1990) Predatory tendencies in the feeding ecology of the fairy shrimpStreptocephalus proboscideus (Frauenfeld, 1873) (Crustacea: Anostraca). Hydrobiologia 198: 119–123

    Google Scholar 

  • Nozaki H (1994) Unequal flagellar formation inVolvox (Volvocaceae, Chlorophyta). Phycologia 33: 58–61

    Google Scholar 

  • —, Itoh M (1994) Phylogenetic relationships within the colonial Volvocales (Chlorophyta) inferred from cladistic analysis based on morphological data. J Phycol 30: 353–365

    Google Scholar 

  • — —, Sano R, Uchida H, Watanabe MM, Kuroiwa T (1995) Phylogenetic relationships within the colonial Volvocales (Chlorophyta) inferred fromrbcL gene sequence data. J Phycol 31: 970–979

    Google Scholar 

  • — — — — —, Takashashi H, Kuroiwa T (1997) Phylogenetic analysis ofYamagishiella andPlatydorina (Volvocaceae, Chlorophyta) based onrbcL gene sequences. J Phycol 33: 272–278

    Google Scholar 

  • Olson LW, Kochert G (1970) Ultrastructure ofVolvox carteri. Arch Mikrobiol 74: 31–40

    Google Scholar 

  • Pickett-Heaps JD (1975) Structural and phylogenetic aspects of microtubular systems in gametes and zoospores of certain green algae. In: Duckett JG, Racey PA (eds) The biology of the male gamete. Academic Press, New York, pp 37–44 plus 4 plates

    Google Scholar 

  • Pocock MA (1933)Volvox and associated algae from Kimberly. Ann S Afric Museum: 14: 473–521

    Google Scholar 

  • Rausch H, Larsen N, Schmitt R (1989) Phylogenetic relationships of the green algaVolvox carteri deduced from small subunit ribosomal RNA comparisons. J Mol Evol 29: 255–265

    Google Scholar 

  • Raven JA, Richardson K (1984) Dinophyte flagella: a cost-benefit analysis. New Phytol 98: 259–276

    Google Scholar 

  • Ringo DL (1967) Flagellar motion and fine structure of the flagellar apparatus inChlamydomonas. J Cell Biol 33: 543–571

    Google Scholar 

  • Roberts K (1974) Crystalline glycoprotein cell walls of algae: their structure, composition and assembly. Philos Trans R Soc Lond Biol 268: 129–146

    Google Scholar 

  • Ruffer U, Nultsch W (1985) High-speed cinematographic analysis of the movement ofChlamydomonas. Cell Motil 5: 251–263

    Google Scholar 

  • — — (1987) Comparison of the beating of cis- and trans-flagella ofChlamydomonas cells held on micropipettes. Cell Motil 7: 87–93

    Google Scholar 

  • — — (1990) Flagellar photoresponses ofChlamydomonas cells held on micropipettes: I. Change in flagellar beat frequency. Cell Motil Cytoskeleton 15: 162–167

    Google Scholar 

  • — — (1991) Flagellar photoresponses ofChlamydomonas cells held on micropipettes: II. Change in flagellar beat pattern. Cell Motil Cytoskeleton 18: 269–278

    Google Scholar 

  • Sakaguchi H, Iwasa K (1979) Two photophobic responses inVolvox carteri. Plant Cell Physiol 20: 909–916

    Google Scholar 

  • Sakaguchi H, Tawada K (1977) Temperature effect on the photoaccumulation and phobic response ofVolvox aureus. J Protozool 24: 284–288

    Google Scholar 

  • Schmitt R, Fabry S, Kirk DL (1992) In search of molecular origins of cellular differentiation inVolvox and its relatives. Int Rev Cytol 139: 189–265

    Google Scholar 

  • Shaw WR (1922)Copelandosphaera, a new genus of the Volvocaceae. Philip J Sci 21: 207–237

    Google Scholar 

  • Smith GM (1944) A comparative study of the species ofVolvox. Trans Am Microsc Soc 63: 265–310

    Google Scholar 

  • Sleigh MA, Blake JA (1977) Methods of ciliary propulsion and their size limitations. In: Pedley TJ (ed) Scale effects in animal locomotion. Academic Press, London, pp 243–256

    Google Scholar 

  • Smyth RD, Berg HC (1982) Change in flagellar beat frequency ofChlamydomonas in response to light. Cell Motil Suppl 1: 211–215

    Google Scholar 

  • Sommer U (1988) Some size relationships in phytoflagellate motility. Hydrobiologia 161: 125–131

    Google Scholar 

  • —, Gliwicz ZM (1986) Long range vertical migration ofVolvox in tropical Lake Cahora Bassa (Mozambique). Limnol Oceanogr 31: 650–653

    Google Scholar 

  • Starr RC (1980) Colonial chlorophytes. In: Cox ER (ed) Phytoflagellates. Elsevier/North-Holland, New York, pp 147–163

    Google Scholar 

  • Taft CE (1940) Asexual and sexual reproduction inPlatydorina caudata. Trans Am Microsc Soc 59: 1–11

    Google Scholar 

  • Taylor MG, Floyd GL, Hoops HJ (1985) Development of the flagellar apparatus and flagellar position in the colonial green algaePlatydorina caudata (Chlorophyceae). J Phycol 21: 533–546

    Google Scholar 

  • Treasurer JW (1990) The food and daily food consumption of lacustrine O+ perch,Perca fluviatilis L. Freshwater Biol 24: 361–374

    Google Scholar 

  • Triemer RE, Brown RM Jr (1974) Cell division inChlamydomonas moewusii. J Phycol 10: 419–433

    Google Scholar 

  • Vogel S (1994) Life in moving fluids, 2nd edn. Princeton University Press, Princeton, NJ

    Google Scholar 

  • Witman GB (1993)Chlamydomonas phototaxis. Trends Cell Biol 3: 403–408

    Google Scholar 

  • Woessner JP, Goodenough UW (1994) Volvocine cell walls and their constituent glycoproteins: an evolutionary perspective. Protoplasma 181: 245–258

    Google Scholar 

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  1. Department of Biology, State University of New York at Geneseo, 1 College Circle, 14454, Geneseo, NY, USA

    H. J. Hoops

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Hoops, H.J. Motility in the colonial and multicellular Volvocales: structure, function, and evolution. Protoplasma 199, 99–112 (1997). https://doi.org/10.1007/BF01294499

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