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Symbiont succession during embryonic development of the European medicinal leech, Hirudo verbana.

ABSTRACT: The European medicinal leech, Hirudo verbana, harbors simple microbial communities in the digestive tract and bladder. The colonization history, infection frequency, and growth dynamics of symbionts through host embryogenesis are described using diagnostic PCR and quantitative PCR. Symbiont species displayed diversity in temporal establishment and proliferation through leech development.

SUBMITTER: Rio RV

PROVIDER: S-EPMC2772434 | biostudies-literature | 2009 Nov

REPOSITORIES: biostudies-literature

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Symbiont succession during embryonic development of the European medicinal leech, Hirudo verbana.

Rio Rita V M RV Maltz Michele M McCormick Benjamin B Reiss Alexander A Graf Joerg J

Applied and environmental microbiology 20090731 21

The European medicinal leech, Hirudo verbana, harbors simple microbial communities in the digestive tract and bladder. The colonization history, infection frequency, and growth dynamics of symbionts through host embryogenesis are described using diagnostic PCR and quantitative PCR. Symbiont species displayed diversity in temporal establishment and proliferation through leech development. ...[more]

PMID: 19648363

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Characterization of a monoacylglycerol lipase in the medicinal leech, Hirudo verbana.

Project description:Endocannabinoids are a class of lipid neuromodulators found throughout the animal kingdom. Among the endocannabinoids, 2-arachydonoyl glycerol (2-AG) is the most prevalent endocannabinoid and monoacylglycerol lipase (MAGL) is a serine hydrolase primarily responsible for metabolizing 2-AG in mammals. In the medicinal leech, Hirudo verbana, 2-AG has been found to be an important and multi-functional modulator of synaptic transmission and behavior. However, very little is known about the molecular components of its synthesis and degradation. In this study we have identified cDNA in Hirudo that encodes a putative MAGL (HirMAGL). The encoded protein exhibits considerable sequence and structural conservation with mammalian forms of MAGL, especially in the catalytic triad that mediates 2-AG metabolism. Additionally, HirMAGL transcripts are detected in the Hirudo central nervous system. When expressed in HEK 293 cells HirMAGL segregates to the plasma membrane as expected. It also exhibits serine hydrolase activity that is blocked when a critical active site residue is mutated. HirMAGL also demonstrates the capacity to metabolize 2-AG and this capacity is also prevented when the active site is mutated. Finally, HirMAGL activity is inhibited by JZL184 and MJN110, specific inhibitors of mammalian MAGL. To our knowledge these findings represent the first characterization of an invertebrate form of MAGL and show that HirMAGL exhibits many of the same properties as mammalian MAGL's that are responsible for 2-AG metabolism.

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Antimicrobial Role of RNASET2 Protein During Innate Immune Response in the Medicinal Leech Hirudo verbana.

Project description:The innate immune response represents a first-line defense against pathogen infection that has been widely conserved throughout evolution. Using the invertebrate Hirudo verbana (Annelida, Hirudinea) as an experimental model, we show here that the RNASET2 ribonuclease is directly involved in the immune response against Gram-positive bacteria. Injection of lipoteichoic acid (LTA), a key component of Gram-positive bacteria cell wall, into the leech body wall induced a massive migration of granulocytes and macrophages expressing TLR2 (the key receptor involved in the response to Gram-positive bacteria) toward the challenged/inoculated area. We hypothesized that the endogenous leech RNASET2 protein (HvRNASET2) might be involved in the antimicrobial response, as already described for other vertebrate ribonucleases, such as RNase3 and RNase7. In support of our hypothesis, HvRNASET2 was mainly localized in the granules of granulocytes, and its release in the extracellular matrix triggered the recruitment of macrophages toward the area stimulated with LTA. The activity of HvRNASET2 was also evaluated on Staphylococcus aureus living cells by means of light, transmission, and scanning electron microscopy analysis. HvRNASET2 injection triggered the formation of S. aureus clumps following a direct interaction with the bacterial cell wall, as demonstrated by immunogold assay. Taken together, our data support the notion that, during the early phase of leech immune response, granulocyte-released HvRNASET2 triggers bacterial clumps formation and, at the same time, actively recruits phagocytic macrophages in order to elicit a rapid and effective eradication of the infecting microorganisms from inoculated area.

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Identification of Aeromonas veronii genes required for colonization of the medicinal leech, Hirudo verbana.

Project description:Most digestive tracts contain a complex consortium of beneficial microorganisms, making it challenging to tease apart the molecular interactions between symbiont and host. The digestive tract of Hirudo verbana, the medicinal leech, is an ideal model system because it harbors a simple microbial community in the crop, comprising the genetically amenable Aeromonas veronii and a Rikenella-like bacterium. Signature-tagged mutagenesis (STM) was used to identify genes required for digestive tract colonization. Of 3,850 transposon (Tn) mutants screened, 46 were identified as colonization mutants. Previously we determined that the complement system of the ingested blood remained active inside the crop and prevented serum-sensitive mutants from colonizing. The identification of 26 serum-sensitive mutants indicated a successful screen. The remaining 20 serum-resistant mutants are described in this study and revealed new insights into symbiont-host interactions. An in vivo competition assay compared the colonization levels of the mutants to that of a wild-type competitor. Attenuated colonization mutants were grouped into five classes: surface modification, regulatory, nutritional, host interaction, and unknown function. One STM mutant, JG736, with a Tn insertion in lpp, encoding Braun's lipoprotein, was characterized in detail. This mutant had a >25,000-fold colonization defect relative to colonization by the wild-type strain at 72 h and, in vitro, an increased sensitivity to sodium dodecyl sulfate, suggesting the presence of an additional antimicrobial property in the crop. The classes of genes identified in this study are consistent with findings from previous STM studies involving pathogenic bacteria, suggesting parallel molecular requirements for beneficial and pathogenic host colonization.

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Exploring the attachment of the Mediterranean medicinal leech (<i>Hirudo verbana</i>) to porous substrates.

Project description:Haematophagous ectoparasites must ensure a reliable hold to their host during blood meals and, therefore, have evolved a broad spectrum of versatile and effective attachment mechanisms. The Mediterranean medicinal leech (Hirudo verbana), for example, uses suction on both smooth and textured air-tight substrates. However, preliminary studies showed that H. verbana is also capable of attaching itself to air-permeable substrates, where suction does not work. Using high-speed videography and mechanical tests, we comparatively investigated the attachment of H. verbana on both smooth and textured air-tight as well as on porous artificial substrates, also considering the influence of mucus on sucker surfaces. In general, the leech-specific locomotion cycle did not differ between the tested surfaces, and the leeches were able to reliably attach to both air-tight and porous substrates. From our results, we conclude that suction is presumably the primary attachment mechanism of H. verbana. However, secondary mechanisms such as mechanical interlocking with surface asperities and pores or capillary forces occurring at the interface between the mucus-covered suckers and the substratum are also employed. In any case, the rich repertoire of applicable attachment principles renders the organs of H. verbana functionally highly resilient.

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Closed Genome Sequence of Aeromonas veronii Strain Hm21, an Isolate from the Medicinal Leech Hirudo verbana.

Project description:Aeromonas veronii strain Hm21 was isolated from the medicinal leech Hirudo verbana and is used for genetic studies. We present here the 4.71-Mbp genome with a 56-kb plasmid and identify the mutations present in strains commonly used for genetic engineering.

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Functional morphology of suction discs and attachment performance of the Mediterranean medicinal leech (Hirudo verbana Carena).

Project description:Medicinal leeches use their suction discs for locomotion, adhesion to the host and, in the case of the anterior disc, also for blood ingestion. The biomechanics of their suction-based adhesion systems has been little understood until now. We investigated the functional morphology of the anterior and posterior suckers ofH irudo verbena by using light and scanning electron microscopy. Furthermore, we analysed the adhesion qualitatively and quantitatively by conducting behavioural and mechanical experiments. Our high-speed video analyses provide new insights into the attachment and detachment processes and we present a detailed description of the leech locomotion cycle. Pull-off force measurements of the anterior and posterior suction organs on seven different substrates under both aerial and water-submersed conditions reveal a significant influence of the surrounding medium, the substrate surface roughness and the tested organ on attachment forces and tenacities.

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Metatranscriptomics provides insight into the physiologies of the digestive tract symbionts within the medicinal leech, Hirudo verbana

Project description:Here, we report the use of Illumina RNA-Seq for investigating the physiology of the digestive-tract microbiome within the medicinal leech, Hirudo verbana. About 12 million cDNA reads were mapped against the genomes of the two dominant members of this simple microbiome. Results suggested that the most abundant, yet uncultured Rikenella-like bacterium forages host mucin glycans and ferments the carbohydrates to acetate that is secreted into the environment. The second dominant symbiont, Aeromonas veronii, appears to utilize the acetate secreted by Rikenella as a carbon and energy source, possibly linking the physiologies of the dominant symbionts. This study demonstrates how RNA-seq can be used to reveal the physiology of a naturally occurring microbiome.

2011-03-25 | GSE23786 | GEO

Reciprocal immune benefit based on complementary production of antibiotics by the leech Hirudo verbana and its gut symbiont Aeromonas veronii.

Project description:The medicinal leech has established a long-term mutualistic association with Aeromonas veronii, a versatile bacterium which can also display free-living waterborne and fish- or human-pathogenic lifestyles. Here, we investigated the role of antibiotics in the dynamics of interaction between the leech and its gut symbiont Aeromonas. By combining biochemical and molecular approaches, we isolated and identified for the first time the antimicrobial peptides (AMPs) produced by the leech digestive tract and by its symbiont Aeromonas. Immunohistochemistry data and PCR analyses evidenced that leech AMP genes are induced in the gut epithelial cells when Aeromonas load is low (starved animals), while repressed when Aeromonas abundance is the highest (post blood feeding). The asynchronous production of AMPs by both partners suggests that these antibiotic substances (i) provide them with reciprocal protection against invasive bacteria and (ii) contribute to the unusual simplicity of the gut microflora of the leech. This immune benefit substantially reinforces the evidence of an evolutionarily stable association between H. verbana and A. veronii. Altogether these data may provide insights into the processes making the association with an Aeromonas species in the digestive tract either deleterious or beneficial.

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