A model symbiosis reveals a role for sheathed-flagellum rotation in the release of immunogenic lipopolysaccharide

Autor: Jason R Hunt, Benjamin C. Krasity, Margaret J. McFall-Ngai, Natacha Kremer, Edward G. Ruby, Caitlin A. Brennan, Michael A. Apicella
Přispěvatelé: Génétique et évolution des interactions hôtes-parasites, Département génétique, interactions et évolution des génomes [LBBE] (GINSENG), Laboratoire de Biométrie et Biologie Evolutive - UMR 5558 (LBBE), Université Claude Bernard Lyon 1 (UCBL), Université de Lyon-Université de Lyon-Institut National de Recherche en Informatique et en Automatique (Inria)-VetAgro Sup - Institut national d'enseignement supérieur et de recherche en alimentation, santé animale, sciences agronomiques et de l'environnement (VAS)-Centre National de la Recherche Scientifique (CNRS)-Université Claude Bernard Lyon 1 (UCBL), Université de Lyon-Université de Lyon-Institut National de Recherche en Informatique et en Automatique (Inria)-VetAgro Sup - Institut national d'enseignement supérieur et de recherche en alimentation, santé animale, sciences agronomiques et de l'environnement (VAS)-Centre National de la Recherche Scientifique (CNRS)-Laboratoire de Biométrie et Biologie Evolutive - UMR 5558 (LBBE), Université de Lyon-Université de Lyon-Institut National de Recherche en Informatique et en Automatique (Inria)-VetAgro Sup - Institut national d'enseignement supérieur et de recherche en alimentation, santé animale, sciences agronomiques et de l'environnement (VAS)-Centre National de la Recherche Scientifique (CNRS)
Jazyk: angličtina
Rok vydání: 2014
Předmět:
Lipopolysaccharides
Immunogen
Lipopolysaccharide
cholerae
medicine.disease_cause
chemistry.chemical_compound
Aliivibrio fischeri
Biology (General)
Vibrio cholerae
ComputingMilieux_MISCELLANEOUS
Microbiology and Infectious Disease
integumentary system
biology
General Neuroscience
[SDV.BID.EVO]Life Sciences [q-bio]/Biodiversity/Populations and Evolution [q-bio.PE]
Decapodiformes
General Medicine
Flagella
[SDV.MP.VIR]Life Sciences [q-bio]/Microbiology and Parasitology/Virology
Medicine
Research Article
LPS
QH301-705.5
Science
Immunology
Vibrio fischeri
Flagellum
General Biochemistry
Genetics and Molecular Biology

Microbiology
[SDV.BBM.GTP]Life Sciences [q-bio]/Biochemistry
Molecular Biology/Genomics [q-bio.GN]

medicine
Animals
14. Life underwater
General Immunology and Microbiology
other
[SDV.BBM.BM]Life Sciences [q-bio]/Biochemistry
Molecular Biology/Molecular biology

biology.organism_classification
[SDV.MP.BAC]Life Sciences [q-bio]/Microbiology and Parasitology/Bacteriology
Vibrio
chemistry
Tissue tropism
biology.protein
bacteria
[SDE.BE]Environmental Sciences/Biodiversity and Ecology
Flagellin
[SDV.EE.IEO]Life Sciences [q-bio]/Ecology
environment/Symbiosis
Zdroj: eLife
eLife, eLife Sciences Publication, 2014, 3, ⟨10.7554/eLife.01579⟩
eLife, 2014, 3, ⟨10.7554/eLife.01579⟩
eLife, Vol 3 (2014)
ISSN: 2050-084X
DOI: 10.7554/eLife.01579⟩
Popis: Bacterial flagella mediate host–microbe interactions through tissue tropism during colonization, as well as by activating immune responses. The flagellar shaft of some bacteria, including several human pathogens, is encased in a membranous sheath of unknown function. While it has been hypothesized that the sheath may allow these bacteria to evade host responses to the immunogenic flagellin subunit, this unusual structural feature has remained an enigma. Here we demonstrate that the rotation of the sheathed flagellum in both the mutualist Vibrio fischeri and the pathogen Vibrio cholerae promotes release of a potent bacteria-derived immunogen, lipopolysaccharide, found in the flagellar sheath. We further present a new role for the flagellar sheath in triggering, rather than circumventing, host immune responses in the model squid-vibrio symbiosis. Such an observation not only has implications for the study of bacterial pathogens with sheathed flagella, but also raises important biophysical questions of sheathed-flagellum function. DOI: http://dx.doi.org/10.7554/eLife.01579.001
eLife digest While a few of the bacteria that live in and on the bodies of humans and other animals are harmful and can cause disease, most others can offer benefits to their hosts. Many bacteria—including some important human pathogens—have tails called flagella that rotate to move the bacteria inside its host. However, the immune system can detect parts of these flagella and eliminate the pathogen. Bacterial flagella are made from filaments of proteins, and some flagella are also enclosed by a sheath that is similar to the outer membrane that encloses certain bacteria. The function of this sheath is unclear, although some researchers have suggested that it might prevent the immune system from detecting the proteins in the flagellum. Now, by studying the interactions between the Hawaiian bobtail squid and a marine bacterium, Brennan et al. show that the sheath can actually alert the host that the bacteria are around. The Hawaiian bobtail squid collects bioluminescent bacteria within a so-called ‘light organ’. This organ undergoes a number of developmental changes to house the bacteria, and the squid then uses the light from the bacteria to mask its own shadow, which helps it to avoid being detected by predators. Brennan et al. compared how wild-type bacteria and mutant bacteria that either had no flagella, or had flagella that did not rotate, interacted with young squid. Only bacteria with working flagella were able to trigger the normal development of the squid’s light organ, which suggests that the rotating flagella are releasing the signal that tells the squid that the beneficial bacteria are present. Brennan et al. demonstrated that the rotation of sheathed flagella led to the release of a molecule called lipopolysaccharide. This molecule is known to activate the immune system in animals, and it is one of the bacterial signals that the squid responds to. Moreover, when the flagella of other bacteria with sheaths—such as those that cause cholera—are rotating, there is also an increase in the release of lipopolysaccharide. However, rotation of the flagella of bacteria without sheaths has no such effect. The next challenge will be to test the importance of this release of lipopolysaccharide from rotating flagella on the outcome of bacterial diseases of humans and other animals. DOI: http://dx.doi.org/10.7554/eLife.01579.002
Databáze: OpenAIRE