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1.
Proc Natl Acad Sci U S A ; 114(36): 9510-9516, 2017 09 05.
Article in English | MEDLINE | ID: mdl-28835539

ABSTRACT

We show that mucociliary membranes of animal epithelia can create fluid-mechanical microenvironments for the active recruitment of the specific microbiome of the host. In terrestrial vertebrates, these tissues are typically colonized by complex consortia and are inaccessible to observation. Such tissues can be directly examined in aquatic animals, providing valuable opportunities for the analysis of mucociliary activity in relation to bacteria recruitment. Using the squid-vibrio model system, we provide a characterization of the initial engagement of microbial symbionts along ciliated tissues. Specifically, we developed an empirical and theoretical framework to conduct a census of ciliated cell types, create structural maps, and resolve the spatiotemporal flow dynamics. Our multiscale analyses revealed two distinct, highly organized populations of cilia on the host tissues. An array of long cilia ([Formula: see text]25 [Formula: see text]m) with metachronal beat creates a flow that focuses bacteria-sized particles, at the exclusion of larger particles, into sheltered zones; there, a field of randomly beating short cilia ([Formula: see text]10 [Formula: see text]m) mixes the local fluid environment, which contains host biochemical signals known to prime symbionts for colonization. This cilia-mediated process represents a previously unrecognized mechanism for symbiont recruitment. Each mucociliary surface that recruits a microbiome such as the case described here is likely to have system-specific features. However, all mucociliary surfaces are subject to the same physical and biological constraints that are imposed by the fluid environment and the evolutionary conserved structure of cilia. As such, our study promises to provide insight into universal mechanisms that drive the recruitment of symbiotic partners.


Subject(s)
Aliivibrio fischeri/physiology , Decapodiformes/microbiology , Sense Organs/cytology , Aliivibrio fischeri/genetics , Animals , Cilia , Decapodiformes/cytology , Epithelium/ultrastructure , Microbiota , Microscopy, Video , Mucus , Sense Organs/microbiology , Symbiosis
2.
Cell Microbiol ; 18(11): 1642-1652, 2016 Nov.
Article in English | MEDLINE | ID: mdl-27062511

ABSTRACT

Recent research has shown that the microbiota affects the biology of associated host epithelial tissues, including their circadian rhythms, although few data are available on how such influences shape the microarchitecture of the brush border. The squid-vibrio system exhibits two modifications of the brush border that supports the symbionts: effacement and repolarization. Together these occur on a daily rhythm in adult animals, at the dawn expulsion of symbionts into the environment, and symbiont colonization of the juvenile host induces an increase in microvillar density. Here we sought to define how these processes are related and the roles of both symbiont colonization and environmental cues. Ultrastructural analyses showed that the juvenile-organ brush borders also efface concomitantly with daily dawn-cued expulsion of symbionts. Manipulation of the environmental light cue and juvenile symbiotic state demonstrated that this behaviour requires the light cue, but not colonization. In contrast, symbionts were required for the observed increase in microvillar density that accompanies post dawn brush-border repolarization; this increase was induced solely by host exposure to phosphorylated lipid A of symbiont cells. These data demonstrate that a partnering of environmental and symbiont cues shapes the brush border and that microbe-associated molecular patterns play a role in the regulation of brush-border microarchitecture.


Subject(s)
Decapodiformes/physiology , Microvilli/microbiology , Vibrio/physiology , Animals , Circadian Rhythm , Decapodiformes/cytology , Decapodiformes/microbiology , Epithelial Cells/microbiology , Epithelial Cells/ultrastructure , Light , Microvilli/ultrastructure , Sense Organs/cytology , Sense Organs/microbiology , Symbiosis/radiation effects
3.
Arthropod Struct Dev ; 36(1): 1-9, 2007 Mar.
Article in English | MEDLINE | ID: mdl-18089083

ABSTRACT

Females of a solitary digger wasp, the European beewolf (Philanthus triangulum F.), cultivate symbiotic bacteria of the genus Streptomyces in specialized antennal glands. The streptomycetes are secreted in the subterranean brood cells and protect the offspring against mould fungi. We reconstructed the complex morphology of the antennal glands using 3D-visualization software, investigated the ultrastructure of the glands, and examine the role of the antennal glands as organs for the cultivation of the symbiotic bacteria. The bacteria are cultivated in five antennomeres within large reservoirs that consist of two slightly bent lobes. Each gland reservoir is bordered by a monolayered epithelium lined with a partially reinforced cuticle and when completely filled with bacteria it comprises about half of the antennomere's volume. The opening of the reservoir is covered by gelatinous appendage of the cuticle. The cells of the monolayered epithelium bordering each reservoir show basal invaginations, apical microvilli and numerous vesicles. Each reservoir is surrounded by approximately 400 class 3 gland units that are connected to the reservoir lumen through conducting canals. The class 3 gland cells contain numerous vesicles and a high density of rough endoplasmatic reticulum. In the reservoir lumen, large numbers of symbiotic Streptomyces bacteria are embedded in secretion droplets. Thus, the bacteria are apparently provided with large amounts of nutrients via the gland epithelium and the class 3 gland cell units.


Subject(s)
Hymenoptera/microbiology , Hymenoptera/ultrastructure , Sense Organs/anatomy & histology , Sense Organs/ultrastructure , Streptomyces/physiology , Animals , Female , Sense Organs/microbiology , Streptomyces/isolation & purification , Symbiosis
4.
J Wildl Dis ; 31(4): 562-5, 1995 Oct.
Article in English | MEDLINE | ID: mdl-8592393

ABSTRACT

Two of five scalloped hammerhead sharks (Sphyrna lewini) captured May 1987 in Hawaii (USA) developed granulomatous exudative mycotic dermatitis localized in the lateral line canal system. The lesion initially was noted in the cephalic canals, but over a period of months extended into the lateral canal. Fusarium solani and Vibrio spp. were isolated from the canal exudate of both sharks. Bacterial colonies were not observed in the canal walls or surrounding tissues. Fusarium solani infection resulted in a chronic physical and behavioral deterioration of the two sharks; one shark was euthanized in September 1988 and the other in July 1989. This is the first report of Fusarium solani infection in the lateral line canal system and the third account in hammerhead sharks.


Subject(s)
Dermatomycoses/veterinary , Fish Diseases/pathology , Fusarium/isolation & purification , Sense Organs/pathology , Sharks , Animals , Animals, Zoo , Dermatomycoses/microbiology , Dermatomycoses/pathology , Fish Diseases/microbiology , Hawaii , Male , Sense Organs/microbiology
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