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Journal ArticleDOI

Flagellated ectosymbiotic bacteria propel a eucaryotic cell.

01 Sep 1982-Journal of Cell Biology (The Rockefeller University Press)-Vol. 94, Iss: 3, pp 697-709
TL;DR: That the ectosymbiotic bacteria actually propel the protozoan was shown, and this motility-linked symbiosis resembles the association of locomotory spirochetes with the Australian termite flagellate Mixotricha, except that in this case propulsion is provided by bacterial flagella themselves.
Abstract: A devescovinid flagellate from termites exhibits rapid gliding movements only when in close contact with other cells or with a substrate. Locomotion is powered not by the cell's own flagella nor by its remarkable rotary axostyle, but by the flagella of thousands of rod bacteria which live on its surface. That the ectosymbiotic bacteria actually propel the protozoan was shown by the following: (a) the bacteria, which lie in specialized pockets of the host membrane, bear typical procaryotic flagella on their exposed surface; (b) gliding continues when the devescovinid's own flagella and rotary axostyle are inactivated; (c) agents which inhibit bacterial flagellar motility, but not the protozoan's motile systems, stop gliding movements; (d) isolated vesicles derived from the surface of the devescovinid rotate at speeds dependent on the number of rod bacteria still attached; (e) individual rod bacteria can move independently over the surface of compressed cells; and (f) wave propagation by the flagellar bundles of the ectosymbiotic bacteria is visualized directly by video-enhanced polarization microscopy. Proximity to solid boundaries may be required to align the flagellar bundles of adjacent bacteria in the same direction, and/or to increase their propulsive efficiency (wall effect). This motility-linked symbiosis resembles the association of locomotory spirochetes with the Australian termite flagellate Mixotricha (Cleveland, L. R., and A. V. Grimstone, 1964, Proc. R. Soc. Lond. B Biol. Sci., 159:668-686), except that in our case propulsion is provided by bacterial flagella themselves. Since bacterial flagella rotate, an additional novelty of this system is that the surface bearing the procaryotic rotary motors is turned by the eucaryotic rotary motor within.
Citations
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Journal ArticleDOI
TL;DR: Gut bacteria of other insects have also been shown to contribute to nutrition, protection from parasites and pathogens, modulation of immune responses, and communication, and the extent of these roles is still unclear and awaits further studies.
Abstract: Insect guts present distinctive environments for microbial colonization, and bacteria in the gut potentially provide many beneficial services to their hosts. Insects display a wide range in degree of dependence on gut bacteria for basic functions. Most insect guts contain relatively few microbial species as compared to mammalian guts, but some insects harbor large gut communities of specialized bacteria. Others are colonized only opportunistically and sparsely by bacteria common in other environments. Insect digestive tracts vary extensively in morphology and physicochemical properties, factors that greatly influence microbial community structure. One obstacle to the evolution of intimate associations with gut microorganisms is the lack of dependable transmission routes between host individuals. Here, social insects, such as termites, ants, and bees, are exceptions: social interactions provide opportunities for transfer of gut bacteria, and some of the most distinctive and consistent gut communities, with specialized beneficial functions in nutrition and protection, have been found in social insect species. Still, gut bacteria of other insects have also been shown to contribute to nutrition, protection from parasites and pathogens, modulation of immune responses, and communication. The extent of these roles is still unclear and awaits further studies.

1,633 citations


Cites background from "Flagellated ectosymbiotic bacteria ..."

  • ...Two specific ectosymbiotic bacteria have been shown to mediate motility of protists by synchronized movements of bacterial cells on the flagellate’s surface (Cleveland & Grimstone, 1964; Tamm, 1982; Hongoh et al., 2007)....

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Book ChapterDOI
01 Jan 2000
TL;DR: Isolation of a number of the prokaryotes (including spirochetes, which have proven to be H2/CO2-acetogens) reveals that termite guts are a source of novel microbial diversity, however, molecular biological analyses indicate that much of that diversity is still poorly represented in culture.
Abstract: The gut of wood- and litter-feeding termites harbors a dense and diverse community of prokaryotes that contribute to the carbon, nitrogen and energy requirements of the insects. Acetogenesis from H2 plus CO2 by hindgut prokaryotes supports up to 1/3 of the respiratory requirement of some termite species; and N2-fixing and uric acid-degrading microbes can have a significant impact on termite N economy. Microelectrode studies reveal that hindguts consist of an anoxic lumen surrounded by a microoxic periphery — a finding consistent with the occurrence of both anaerobic and O2-dependent microbial metabolism in hindguts. They also suggest that the enigmatic dominance of acetogens over methanogens as an H2 “sink” reflects a spatial separation of these H2-consuming populations, with the former being closer to sources of H2 production. Isolation of a number of the prokaryotes (including spirochetes, which have proven to be H2/CO2-acetogens) reveals that termite guts are a source of novel microbial diversity. However, molecular biological analyses indicate that much of that diversity is still poorly represented in culture.

166 citations

Journal ArticleDOI
TL;DR: A combination of single-species-targeting metagenomics, conventional metagenetics, and metatranscriptomics should be a powerful tool to dissect this complex, multi-layered symbiotic system of termites.
Abstract: Termites play a key role in the global carbon cycle as decomposers. Their ability to thrive solely on dead plant matter is chiefly attributable to the activities of gut microbes, which comprise protists, bacteria, and archaea. Although the majority of the gut microbes are as yet unculturable, molecular analyses have gradually been revealing their diversity and symbiotic mechanisms. Culture-independent studies indicate that a single termite species harbors several hundred species of gut microbes unique to termites, and that the microbiota is consistent within a host termite species. To elucidate the functions of these unculturable symbionts, environmental genomics has recently been applied. Particularly, single-species-targeting metagenomics has provided a breakthrough in the understanding of symbiotic roles, such as the nitrogen fixation, of uncultured, individual microbial species. A combination of single-species-targeting metagenomics, conventional metagenomics, and metatranscriptomics should be a powerful tool to dissect this complex, multi-layered symbiotic system.

155 citations

Book ChapterDOI
Andreas Brune1
01 Jan 2006

96 citations

Journal ArticleDOI
TL;DR: Growth of T. termopsidis strains was markedly improved by substituting heat-killed cells of Bacteroides sp.
Abstract: Putatively axenic cultures of Trichomitopsis termopsidis 6057, isolated by M. A. Yamin (J. Protozool. 25:535-538, 1978) from the hindgut of Zootermopsis termites, apparently contained methanogenic bacteria, inasmuch as small amounts of CH(4) were produced during growth. However, T. termopsidis could be "cured" of methanogenic activity by incubation in the presence of bromoethanesulfonate. Both the cured derivative (6057C) and the parent strain (6057) required NaHCO(3) and fetal bovine serum for good growth; the presence of yeast extract in media was stimulatory. Growth of both strains was markedly improved by substituting heat-killed cells of Bacteroides sp. strain JW20 (a termite gut isolate) for heat-killed rumen bacteria in media as a source of bacterial cell material. Heat-killed Bacteroides sp. strain JW20 was the best of a number of bacteria tested, and under these conditions H(2) was a major protozoan fermentation product. Growth of T. termopsidis strains was further improved by co-cultivation in the presence of Methanospirillum hungatii. M. hungatii was the best of a number of H(2)-consuming bacteria tested, and under these conditions CH(4), but not H(2), was produced, indicating interspecies transfer of H(2) between the protozoa and M. hungatii. Both strains of T. termopsidis used powdered, particulate forms of cellulose (e.g., pure cellulose, corncob, cereal leaves) as fermentable energy sources, although powdered wood, chitin, or xylan supported little or no growth. Cells of the cellulose-forming coccus Sarcina ventriculi also served as a fermentable energy source, but these were used poorly as a source of bacterial cell material. The only substantial difference between T. termopsidis 6057 and 6057C was that the latter grew poorly or not at all with rumen bacteria as a source of bacterial cell material. The improved growth of T. termopsidis in vitro should facilitate further studies on the cell biology and biochemistry of these symbiotic, anaerobic protozoa.

90 citations

References
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Journal ArticleDOI
19 Oct 1973-Nature
TL;DR: It is shown here that existing evidence favours a model in which each filament rotates, which is commonly believed that each filament propagates a helical wave3.
Abstract: IT is widely agreed that bacteria swim by moving their flagella, but how this motion is generated remains obscure1,2. A flagellum has a helical filament, a proximal hook, and components at its base associated with the cell wall and the cytoplasmic membrane. If there are several flagella per cell, the filaments tend to form bundles and to move in unison. When viewed by high-speed cinematography, the bundles show a screw-like motion. It is commonly believed that each filament propagates a helical wave3. We will show here that existing evidence favours a model in which each filament rotates.

877 citations


"Flagellated ectosymbiotic bacteria ..." refers background in this paper

  • ...In free-swimming peritrichous bacteria, individual helical filaments rotate (4, 5, 19, 34) and are spontaneously brought together and synchronized to form an in-phase bundle as a result of hydromechanical forces (1, 24-26)....

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Journal ArticleDOI
03 May 1974-Nature
TL;DR: BACTERIAL flagella are generally composed of three morphologically distinguishable regions: the long flagellar filament, the hook, and the basal structure which is composed of an intricate set of disks and rods attaching the hook to the cell membrane and cell wall.
Abstract: BACTERIAL flagella are generally composed of three morphologically distinguishable regions: (a) the long flagellar filament which accounts for more than 95% of the flagellar protein; (b) the hook, which is generally 80–90 nm long and has a characteristic shape, and (c) the basal structure which is composed of an intricate set of disks and rods attaching the hook to the cell membrane and cell wall1–3.

685 citations

Journal ArticleDOI

637 citations


"Flagellated ectosymbiotic bacteria ..." refers background in this paper

  • ...dependent motility that requires contact with other ceils and the presence of a surface (12, 35)....

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Journal ArticleDOI
03 May 1974-Nature
TL;DR: It is found that changes in the direction of flagellar rotation indeed constitute the basis of chemotaxis: addition of attractants causes counter clockwise (CCW) rotation, whereas repellents causeClockwise (CW) rotation.
Abstract: BERG and Anderson1 recently argued from existing evidence that bacteria swim by rotation of their helical flagella. Silver-man and Simon2 have now provided a clear demonstration of this. By means of antibodies specific for flagellar components, they tethered cells to microscope slides or to each other and observed rotation of the cell bodies. The cells were able to stop and to rotate in either direction. It seemed possible, as they proposed2, that cessation, or reversal of flagellar rotation might be involved in bacterial chemotaxis. Accordingly, we used wild-type and chemotaxis-defective mutant cells of Escherichia coli tethered to microscope slides in a manner similar to that of Silverman and Simon2, and stimulated them by sudden increases of chemotactic agents. We found that changes in the direction of flagellar rotation indeed constitute the basis of chemotaxis: addition of attractants causes counter clockwise (CCW) rotation, whereas repellents cause clockwise (CW) rotation.

440 citations

Journal ArticleDOI
TL;DR: It is concluded that the flagella are driven by a protonmotive force, and when starved cells are suspended in a potassium-free medium containing both valinomycin and an attractant, many cells initially run rather than twiddle.
Abstract: Streptococcus strain V4051 is motile in the presence of glucose. The cells move steadily along smooth paths (run), jump about briefly with little net displacement (twiddle), and then run in new directions. They stop swimming when deprived of glucose. These cells become motile when an electrical potential or a pH gradient is imposed across the membrane. Starved cells suspended in a potassium-free medium respond to the addition of valinomycin by a brief period of vigorous twiddling. They also twiddle, although less vigorously, when the external pH is lowered. Valinomycin-induced twiddling occurs in the absence of external alkali or alkaline earth cations and without significant net synthesis of ATP. When a chemoattractant is added to cells swimming in the presence of glucose, twiddles are transiently suppressed, and the cells run for a time. Similarly, when starved cells are suspended in a potassium-free medium containing both valinomycin and an attractant, many cells initially run rather than twiddle. We conclude that the flagella are driven by a protonmotive force.

393 citations


"Flagellated ectosymbiotic bacteria ..." refers background in this paper

  • ...Proton ionophores such as DNP collapse the proton gradient driving rotation of bacterial flagella, thereby inhibiting bacterial motility (16, 17, 27)....

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  • ...Advantage was taken of the fact that the immediate energy source for bacterial motility, unlike eucaryotic motile systems, is not ATP but a transmembrane electrochemical potential of protons (20, 27, 29)....

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